Advances in Agronomy, Volume 30

ADVANCES IN

AGRONOMY VOLUME 30

CONTRIBUTORS TO THIS VOLUME

LINDOJ . BARTELLI DICKD . DAVIS E. C. DOLL

F. E. KHASAWNEH BETTYKLEPPER

JAY D. MANN

R. L. PARFITT PETERL. STEPONKUS

H. M. TAYLOR

ADVANCES IN

AGRONOMY Prepared under the Auspices of the

AMERICAN SOCIETY

OF

AGRONOMY

VOLUME 30

Edited by N. C. BRADY International Rice Research Institute Manila, Philippines

ADVISORY BOARD

H.J. GORZ,CHAIRMAN K.M. KIM G.R. BLAKE R . B . GROSSMAN E.A. WERNSMAN

M. STELLY,EX

T.M. STARLING OFFICIO,

ASA Headquarters

I978

ACADEMIC PRESS New York San Francisco London A Subsidiary of Harcourt Brace Jovanovich, Publishers

COPYRIGHT @ 1978, BY ACADEMIC PRESS, INC. ALL RIGHTS RESERVED. NO PART OF THIS PUBLICATION MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM OR BY ANY MEANS, ELECTRONIC OR MECHANICAL, INCLUDING PHOTOCOPY, RECORDING, OR ANY INFORMATION STORAGE AND RETRIEVAL SYSTEM, WITHOUT PERMISSION IN WRITING FROM THE PUBLISHER.

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CONTENTS

CONTRIBUTORS TO VOLUME 30 ..................................

PREFACE....................................................

ix xi

ANION ADSORPTION BY SOILS AND SOIL MATERIALS

R. L . P d i t t I. I1. I11. IV . V. VI . VII .

Introduction ............................................ Techniques ............................................ Determination of Adsorption Sites on Mineral Surfaces . . . . . . . . . Adsorption Mechanisms .................................. Identification of Adsorption Sites in Soils . . . . . . . . . . . . . . . . . . . Adsorption by Soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Summary and Conclusions ................................ References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

i

2 7 12 24 26 41 42

COLD HARDINESS AND FREEZING INJURY OF AGRONOMIC CROPS

Peter L . Steponkus I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I1. Characterization of the Freezing Process and Freezing Injury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Environmental Factors Affecting Cold Hardiness . . . . . . . . . . . . . IV . Effect of Developmental Stage on Cold Hardiness . . . . . . . . . . . . V . Physiological and Biochemical Aspects of Cold Acclimation .......................................... VI . Screening and Stress Procedures for Determining Cold Hardiness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VII . Summary and Conclusions ................................ References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

51 54 65 71 73 88 92 93

THE ROLE OF ROOTING CHARACTERISTICS IN THE SUPPLY OF WATER TO PLANTS

H . M . Taylor and Betty Klepper I . Introduction ............................................ 99 100 I1. A Model of Water Uptake by Roots ........................ I11. Diurnal Water Potentials in the Soil-Plant System . . . . . . . . . . . . 105

CONTENTS

vi

Axial Resistances . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Resistances in the Absorption Pathway ..................... Rooting Volume . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The Real World ........................................ Factors that Man Can Control ............................. A Final Thought . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

IV . V. VI . VII . VIII . IX .

106 i12 116 120 122 125 125

HYBRID COTTON: SPECIFIC PROBLEMS AND POTENTIALS

Dick D . Davis

I . Introduction ............................................ I1. Heterotic Expression of Cotton Hybrids .....................

111. IV . V. VI . VII. VIII . IX . X.

XI .

Effects of Heterosis on Phenology ......................... Plant Type and Harvest Efficiency ......................... Pest Resistance Potential for Hybrids ....................... Fiber Properties of Hybrids ............................... Breeding Hybrids with Marketable Fiber Properties . . . . . . . . . . . The Production of Hybrid Seed ............................ The Association of Heterosis and Plant Pubescence ........... Breeding Methodology ................................... Summary .............................................. References .............................................

130 131 134

138 140

142 144 147 150 152 153 153

THE USE OF PHOSPHATE ROCK FOR DIRECT APPLICATION TO SOILS

F . E . Khasawneh and E . C . Doll I . Introduction ............................................

............... I11. Reactions of Phosphate Rocks in Soils ......................

159 161 166

IV . Agronomic Evaluation of Phosphate Rock for Direct Application .......................................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

183 204

I1. Mineralogy and Chemistry of Phosphate Rock

PRODUCTION

OF SOLASODINE FOR THE PHARMACEUTICAL INDUSTRY

Jay D . Mann

I . Perspective ............................................ 207 11. Solasodine-Containing Species of Solanurn .................. 209

CONTENTS

111. Chemistry

IV . V. VI . VII . VIII .

.............................................

Biochemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Isolation and Determination of Solasodine . . . . . . . . . . . . . . . . . . . Agronomy of Poroporo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Medical Aspects of the Glycoalkaloids ...................... Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

vii

217 221 226 229 238 240 240

TECHNICAL CLASSIFICATION SYSTEM FOR SOIL SURVEY INTERPRETATION

Lindo J . Bartelli

I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I1. Principles of Technical Classification .......................

247 249 253 261 265

Systems for Organizing Soil Survey Interpretations . . . . . . . . . . . . Plant Suitability Evaluation Systems ........................ Systems to Evaluate Engineering Properties . . . . . . . . . . . . . . . . . . The Application of Technical Classification to Soil Surveys . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 273 VII . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 288 111. IV . V. VI .

SUBJECT INDEX . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

291

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CO NTRIBUTORS Numbers in parentheses indicate the pages on which the authors' contributions begin.

LINDO J. BARTELLI (247), School of Forestry and Wood Products, Michigan Technological University, Houghton, Michigan 49931 DICK D. DAVIS (129), Department of Agronomy, New Mexico State University, Las Cruces, New Mexico 88001 E. C. DOLL (159), Division of Agricultural Development, Tennessee Valley Authority, Muscle Shoals, Alabama 35660 F . E . KHASAWNEH (159), Division of Agricultural Development, Tennessee Valley Authority, Muscle Shoals, Alabama 35660 BETTY KLEPPER (99), USDA, Science and Education Administration, Columbia Plateau Conservation Research Center, Pendleton, Oregon 97801 JAY D. MANN (207), Applied Biochemistry Division, Department of Scientific and Industrial Research, Christchurch, New Zealand R . L. PARFI'IT ( l ) , Soil Bureau, Department of Scientific and Industrial Research, Lower Hutt, New Zealand PETER L. STEPONKUS (5 l ) , Department of Agronomy, Cornell University, Ithaca, New York 14853 H. M . TAYLOR (99), USDA, Science and Education Administration, Ames, Iowa 50010

ix

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PREFACE The genetic yield potential of most crop plants is severalfold greater than the average yields actually achieved by farmers. Even the best performing cultivars commonly yield in the field no more than about half the level that under ideal conditions we know they can yield. Obviously in nature yields are constrained and often by factors of direct concern to agronomists. One of the primary responsibilities of crop and soil scientists is to identify the agronomic constraints on yield and then through research to find ways of removing these constraints. The contributions in this volume help us understand some of the constraints on crop yields and performance. Two reviews deal with variables related to climate. The effects of low temperatures on plants and the response of agronomic crops to these temperatures is the subject of one review. The nature of the roots in relation to the plants’ ability to meet its water supply needs is covered in a second review. Modern sensitivity to chemical hazards is expressed in this volume in keeping with a similar concern in the last few volumes. Two reviews deal with anions commonly found in soils. One gives a general coverage of the reactions and behavior of anions in different soils. The second focuses on a very important supplier of one of the most significant of these anions from a nutritional viewpoint-the phosphates. Rising costs of sulfur needed to manufacture superphosphates make it essential that rock phosphates be examined critically as sources of direct application for this important element. The potential of hybrid cotton along with the problems encountered with attempts to realize this potential are covered in this volume. The final review concerns soil survey interpretations, not only for agricultural purposes but for other uses as well. The authors who prepared these contributions have helped maintain the internationality of Advances in Agronomy. Likewise, the subjects they review are of considerable significance in most parts of the world. We are indebted to them for their efforts. N . C. BRADY

xi

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ADVANCES IN AGRONOMY, VOL. 30

ANION ADSORPTION BY SOILS AND SOIL MATERIALS

R. L. Parfitt Soil Bureau, D.S.I.R.,Lower Hutt, New Zealand

I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. Techniques.

................

.

1 2

A. Crystal Structure . . . . . . . . . . . . . . . B. Infrared Spectroscopy . . . . . . . . . . . . . . C. . . . . . . . ................... ..... C. Kinetics Surface Charge.. D. Ligand Exchange . . . . . . . . . . . . . . . . . . Adsorption Mechanisms . . . . . . . . . . . . . . . . A. Goethite (a-FeOOH) . . . . . . . . . . . . . . . C. . . .. .. .. ... . . . . . . . . . . . B . Surface HematiteCharge.. (a-Fe203) C. Other Iron Oxides . . . . . . . . . . . . . . . . . D. Gibbsite and Other Aluminum Surfaces E. Amorphous Hydroxides . . . . . . . . . . . . . F. Clay Minerals.. ................... G. Calcite ( C a C 0 3 ) .. . . . . . . . . . . . . . . . . .

............ ................................................. Calcite (CaC03) . . . . . . . ....

20 21 23 24 24 24 25 25 26

........ Arsenate .................... Molybdate ......................................................... ......................... D. Selenite.. . . . . . . . . . . . . E. Sulfate ... ...................... F. Boric Acid ............................................... G. Silicic Acid ...............................

34 34 35 36 36

E.

Amorphous Hydroxides ......................

G. V. Identification of Adsorption Si ............................. A. Surface Iron and Aluminum ........................................... B. Organometallic Complexes ............................................ C. Extraction of Phosphate.. .. ........ VI. Adsorption by S o i l s . . ......................................... B.

C.

............................................... .........................

Halides . . . . . . . . . . . . . . J . Nitrate.. . . . . . . . . . . . . . . . . . VII. Summary and Conclusions . . References .................................... I.

38

39 40

I. Introduction

In recent years there has been an increasing volume of literature dealing with the topic of anion adsorption by soils and soil materials, including the important I

Copyright @ 1978 by Academic Ress, Inc. All rights of reproduction in any form r e ~ e ~ e d .

ISBN-0-12-MX)730.4

2

R. L. PARFITT

iron and aluminum sesquioxide components. This has been due, in part, to the increased research effort going into tropical and subtropical areas, where many soils contain significant amounts of hydrous iron oxides and aluminum hydroxides. However, these reactive iron and aluminum surfaces are also common in many temperate soils (Mitchell et al., 1964; Wada and Harward, 1974). In particular, volcanic ash soils (andepts) often contain large amounts of reactive aluminum and iron gels, which can cause severe deficiencies of phosphate and sulfate in plants. In .4ustralia, Posner, Quirk, and co-workers have used iron and aluminum oxides with well-defined surfaces to study ion adsorption. This has stimulated much further research and has led to the development of a general model for ion adsorption on hydrous oxide surfaces, which takes account of the pH-dependent charge on the surface and the charge on the adsorbing ion (Bowden et al., 1977). It has become apparent that the adsorption behavior of many anions, in particular the important nutrients phosphate, sulfate, and molybdate. is very similar (Barrow, 1970). Work with synthetic iron and aluminum oxides has shown that fluoride, selenite, silicate, arsenate, carbonate, and other anions, including organic anions, are also adsorbed by similar mechanisms. This article attempts to review the work with soils, and with hydrous oxides of iron and aluminum, with particular reference to mechanisms and structural aspects of anion adsorption. Anion adsorption on clay minerals and calcium carbonate is also considered. II. Techniques

A. ADSORPTION ISOTHERMS

The determination of adsorption isotherms is one of the most useful experimental procedures in the study of the interaction of anions with hydrous oxides or soils. Most of the adsorption isotherms reported in the literature belong either to the Langmuir (L) type or to the high-affinity (H)type, as defined by Giles et al. (1960). Some examples are given in Fig. 1. The isotherms for phosphate adsorption on pure hydrous oxides are usually of the H type, indicating a large negative free energy, AG, of adsorption. On soils L-type isotherms can also be obtained, but the shape of the isotherm will depend on other factors such as the amount of native phosphate in the soil, the presence of fertilizer phosphate, and the influence of organic matter (Ryden and Syers, 1977). Several models have been used to describe anion adsorption, with most workers favoring the Langmuir model, which is described by the following equation:

3

ANION ADSORPTION BY SOILS

where c = solution concentration ;0 = XI&, where x = amount of ion adsorbed and x, = the sorption maximum; and K is a constant related to the adsorption energy. The equation may be written in the linear form: -c = - c x xlrl

+ Kxn, -1

and a plot of c/x against c should give a straight line of slope lh,,,, from which x, may be calculated and the constant K obtained from the intercept (Fig. 2). For anion adsorption the plot of clx against c does not give a straight line over a wide concentration range, and the simple Langmuir equation is not obeyed (Fig. 2). In the Langmuir model derived for the adsorption of gases onto solid surfaces, it is assumed that adsorption is restricted to a monolayer and that the energy of adsorption does not vary with surface coverage. Thus, the sites must be isolated and uniform, and the adsorbed molecules must not interact with each other.

100

0.2

0.4

OC? C

0.04 C

FIG. 1. Adsorption isotherms showing examples of high-affinity (H-type) isotherms for phosphate adsorption on goethite (a-FeOOH) in 0.1 M NaCl, pH 3.5,over different concentration ranges (A, B);Langmuir-typeisotherm for phosphate adsorption by soil (C); and an isotherm of an intermediate nature for phosphate adsorption on amorphous A1 (OH), in 0.1 M NaCI, pH 6.0 (D).x = anion adsorbed; c = final solution concentration.

R. L. PARFITT

4

Slope

1

=

qi /

/

C

FIG. 2. Langmuir plot of clx against c for phosphate adsorption on soil.

The failure of the simple Langmuir model to describe anion adsorption at solid-solution interfaces has led to the use of two- or three-term Langmuir equations, which give much better descriptions of experimental data (Muljadi et al., 1966a; Holford et al., 1974; Rajan, 1975c; Ryden et al., 1977b). These models assume that there are two or three sites for adsorption, with the energy of adsorption constant at each site. An equation similar to the Langmuir equation can be derived from considering adsorption equilibria (Graham, 1953). For adsorption: Anions "vacant sites" occupied sites desorbed ligands. If all sites are identical, and if there is no interaction between adsorbed anions, and if the activity coefficients of the occupied and unoccupied sites are the same, then

+

+

where K = the equilibrium constant, 8 = the fraction of the surface covered, and c A and c L = activities of the anion and desorbed ligand. If c L = 1 , the equation can be rewritten

which is identical to the Langmuir equation. If the activity coefficient is assumed to be unity, K may be determined from Langmuir plots and the standard free energy of adsorption AGO = -RT In K. Then -AGO gives a measure of the energy of adsorption due to bonding energy (AH") and entropy changes (AS"), where AGO = AH" - TAS". Ryden et al. (1977b) have used this approach to calculate AGO for three regions of the isotherm for phosphate adsorption on soils over a

ANION ADSORPTION BY SOILS

5

wide concentration range. The procedure was less successful for adsorption on Fe(OH), , where initial adsorption was of the high-affinity type. Attempts to use the Langmuir equation for phosphate adsorption on synthetic goethite have not been successful (Bowden el al., 1974), although synthetic goethite crystals have only one site available for anion adsorption (Parfht et al., 1976). This suggests that the assumptions made in using the Langmuir equation are not valid and that results obtained with this approach should be treated with caution. The Langmuir model is also inadequate when adsorption conditions such as pH or salt concentration are changed, because these factors affect both x , and K (Bowden et al., 1977). The inadequacy of the simple Langmuir model is perhaps hardly surprising. Being formulated for solid-gas systems, it takes no account of the charge on the anion being adsorbed nor of the surface charge. New models have recently been developed that are general and take account of charges during adsorption of anions and cations on amphoteric oxide surfaces (Yates et al., 1974; Bowden et al., 1977). In the approach used by Bowden el al. (1977), the free energy of adsorption (AGadB)is separated into three components: AGcoul,the coulombic or electrostatic component; hGchem,the chemical component; and AGint, the interaction component, which gives specificity to the coulombic binding. Thus,

Indifferent ions, such as nitrate, are adsorbed only on a positively charged surface, and AGcoul is significant, but hGchem is low. Adsorption is due to electrostatic interaction between the ion and the electric field of the surface. If an ion is adsorbed out of proportion to its activity in solution because of the size and polarizability of the ion, then AGlnt is also important. Potential-determiningions and ligand-exchanged ions can adsorb on a surface of like charge or zero charge, and AGchemis significant because of a specific interaction. Potential-determining ions are ions such as H30+ and OH-, which give their charge to a surface. Ions that are ligand-exchanged or specifically adsorbed are ions, such as phosphate, that are not present in the oxide lattice but that can also affect the surface charge on adsorption. Although these general models treat the surface as a continuum of sites, in energy terms, they are not inconsistent with the concept of discrete sites identified by infrared spectroscopy, since other factors such as proton adsorption and the presence of counter-ions may give sites of the same geometry a distribution of energy levels. The strength of the general model is that it describes experimental data obtained over a wide range of conditions (Bowden et al., 1973, 1974). Other simple equations that have been used to describe anion adsorption include the empirical Freundlich equation and the Temkin equation (Bache and

6

R. L. PARFITT

Williams, 1971). The Temkin equation includes the condition that the energy of adsorption decreases linearly with surface coverage. This model can be used over a wide concentration range, but the plot of x against log c is not linear over the whole range. Nevertheless, an equation that takes account of the continuous change in energy of adsorption with surface coverage during anion adsorption (Bache, 1964) should give a better description than the Langmuir equation. Adsorption isotherms can sometimes be used to give an indication of different adsorption mechanisms. The adsorption of oxalic acid on goethite (a-FeOOH) is an example. The shape of the isotherm has three distinct regions, suggesting that there are three different adsorption mechanisms (Parfin et al., 1977a). Infrared spectroscopy confirmed that oxalate was adsorbed as a bridging complex in Region I, and as a monodentate complex in Region 11, and it was suggested that dissolution occurred in Region 111. The isotherm for benzoic acid adsorption had a lower slope than that for oxalic acid adsorption, indicating a lower adsorption energy (Bache, 1964). Subsequently it was shown that this was due to monodentate adsorption of the benzoate, compared with bridging adsorption by the oxalate ( P d i t t et al., 1977a). Other examples have been described by Aylmore et al. (1967) and Theng (1971). Some other techniques that are related to adsorption isotherms include desorption studies. The rate of desorption of an adsorbed anion will give an indication of the energy of adsorption. Desorption is usually carried out by washing the adsorption complex with the same indifferent electrolyte used for adsorption and using the same pH conditions. With this method Hingston et al. (1974) were able to show that small amounts of phosphate could be desorbed from goethite, whereas fluoride could be desorbed almost completely. The desorption of OH ions during anion adsorption has also been studied, but it is usually difficult to interpret these results unambiguously (Rajan, 1975a). However, it has been possible to show that phosphate will displace silicate during adsorption on allophane clay, whereas selenite does not cause silicate desorption. This suggests that phosphate can be sorbed by displacing silicate (Rajan and Watkinson, 1976).

B. INFRARED SPECTROSCOPY Infrared spectroscopy can be used to study both the nature of adsorbing surfaces and the mechanism of adsorption on those surfaces (Little, 1966; Hair, 1967). Sample preparation is very important, since good films are required to minimize losses of radiation by scattering. Self-supporting films are ideal, but films that are evaporated onto infrared windows can also be used. Water molecules are usually adsorbed on hydrous oxide surfaces, and it is necessary to remove the water by evacuation in a vacuum cell, which prevents

ANION ADSORPTION BY SOILS

7

rehydration while the spectrum is being run. If the surface OH groups are discrete and if they represent a reasonable proportion of the total OH, including OH within the bulk of the oxides, then good resolution should be possible. Improved resolution is usually obtained by exchanging OH with b0 to give OD groups. Information on the coordination of anions to surfaces and their mechanism of adsorption can be obtained by comparing the spectra of the OH and OD groups before and after anion exchange. If the adsorbing ion itself has a spectrum in a range not obscured by lattice vibrations, then additional data are available on the coordination of the ion to the surface. It may also be possible to study the form of bonding in the presence of solvent as well as under vacuum. Thus, for phosphate adsorption on goethite it was possible to identify the mechanism of adsorption from the spectrum of the goethite surface groups and the spectrum of the adsorbed phosphate ion (Pditt et d , 1976; P d i t t and Atkinson, 1976). Further details on techniques used in infrared spectroscopy are available in a review by Russell (1974).

C. KINETICS

A study of the kinetics of anion adsorption can be used to gain information about the mechanism of the adsorption reaction. The data are usually presented to show the change in adsorption with time or the change in anion concentration with time. These basic experiments have indicated that the adsorption reaction is followed by a slow reaction on some systems (Chen et al., 1973b). A study of the effect of pH, temperature (which enables the activation energy to be calculated), or successive additions of anion may give further useful information about reaction mechanisms or rate-limiting steps, but generally it is difficult to interpret kinetic data without some reasonable theory. Studies on the kinetics of isotopic exchange of adsorbed anions have provided useful information about adsorption mechanisms. When Elovich kinetics have been applied, concentration-independent rate constants can be determined and comparisons made with other systems. This led Atkinson et al. (1972) to postulate that phosphate formed a bridging complex on goethite. Experiments on rates of isotopic exchange of phosphate have also provided useful information about the nature of labile phosphate in soils (Mattingly, 1975). 111. Determination of Adsorption Sites on Mineral Surfaces

The surfaces of iron and aluminum oxides and hydrous oxides usually consist of mixtures of OH- ions and water molecules, which &e coordinated to Fe3+ or

8

R. L. PARFITT

FIG. 3. Structure of the (100) face of goethite (a-FebOH) in plan a and section b. A, B, and C are hydroxyl groups, and C’ is an oxide ion.

A13+ ions directly below the surface. In the ideal structure the surface is assumed to have no net charge, and therefore at a freshly cleaved surface OH- ions and water molecules replace the structural 02-and OH- ions, which become exposed. The OH- ions may be in one, two, or three coordination to the metal ions below. From work with goethite (Fig. 3), it appears that only the one-coordinated OH- ions (A type) are able to take part in ligand exchange reactions (Parfitt er al., 1976). Under acid conditions they adsorb protons, giving positively charged OH+ ions, which are readily exchanged with other ligands. Lewis acid sites occur where water molecules are coordinated to metal ions exposed at a surface. In the presence of OH- ions a proton may be lost from these M*O& sites to give M-OH-at the surface (Mott, 1970). A. CRYSTAL STRUCTURE

The crystal structures of most minerals that occur in the clay fraction of soils are now known. If the adsorbent is well crystallized, then the crystal structure can be used as the starting point for determining the structure of the crystal faces. For goethite, electron diffraction has been used to show that the (100) face

9

ANION ADSORPTION BY SOILS

predominated, the other exposed faces being the (010) and (001) faces. The arrangement of the exposed surface ions could then be deduced (Atkinson, 1969; Russell et al., 1974), and the number of sites could be estimated from the size of the crystals. It was predicted that there were three types of OH groups (A, B, and C) on the (100) face, and in addition there were Lewis acid sites (Fe*OH2)on the (010) face (Fig. 3). On a high-surface-area goethite it was estimated that there were 410 pmol g-' A, B,and C-type OH groups, and 220 pmol g-I of Lewis acid sites (Pditt et al., 1976). These results were consistent with adsorption isotherm data and infrared spectra.

B. INFRARED SPECTROSCOPY Surface sites can often be identified on hydrous oxides by infrared spectroscopy after the adsorbed water has been removed. Figure 4 gives an example of the bands obtained for the OH sites on geothite. These bands are more clearly

3800

I '

I

3400 I

3ooo

I

I

2600

I

I

I

2200 mi' I

FIG. 4. Infrared spectra of goethite showing surface OH bands, which exchange with 40, giving OD bands.

10

R. L. PARFIT

resolved after exchange with 40, giving OD vibrations at 2584 cm-' and 2701 cm-'. The main band at 3 150 cm-' is due to the structural OH groups within the goethite crystals. The A-, B-, and C-type surface OD (OH) vibrations are shown in Fig. 5a. The B- and C-type OD vibrations are clearly resolved near 2700 cm-' after the 410pmol A-type OD at 2584 cm-' have been exchanged with 410pmol F- or 205 p mol HPOi- (Fig. 5 , b, c) (Parfitt et al., 1976). Lewis acid sites (M-OH,) can also be identified from infrared spectra by adsorbing ammonia or pyridine and examining the spectrum of the adsorbed ligand. On goethite, the pyridine bands occurred at 1608 cm-' and 1592 cm-', indicating that pyridine was held on Lewis acid sites (1608 cm-') and by hydrogen bonding (1592 cm-'). No band near 1540 cm-' was observed, implying that Bronsted acid sites were absent (Parfin et al., 1976).

FIG.5. Infrared spectra of goethite surface OD groups showing A-, B-, and C-type OD (a); showing A-type OH replaced by F and HPQ-, and the B- and C-type OD clearly resolved in the 2700-cm-' region (b, c).

ANION ADSORPTION BY SOILS

C . SURFACE CHARGE

The important sites for adsorption are the M*OHand M*OH2sites, which may become charged in the presence of excess H+ or OH- ions. Since the charge on oxide surfaces is pH-dependent, potentiometric titrations in indifferent electrolytes (for example, NaN03) are used to give information on the charge characteristic of these surfaces. The pH where the titration curves cross over is referred to as the pH of the point of zero charge (pzc). The pzc occurs between pH 7.5 and 9 for iron and aluminum oxides (Hingston ef al., 1972).

On the acid side of the pzc, H+ ions are adsorbed on the oxide surface at the first layer of coordinated OH or oxide ions (inner Helmholtz plane), and the counter-ions (for example NO,-) are adsorbed in the diffuse double layer. On the basic side of the pzc, H+ ions are desorbed from the first coordination shell, and the counter-ions (Na+ or K+) are in the diffuse double layer. For goethite and hematite the uptake of H+ or OH-, measured by potentiometric titration, did not reach any maximum value within the pH range 3.5-1 1. The largest uptake of protons in KCl solution occurred in 1 M solution at pH 3.5, giving one excess proton per 0.34 nm2 and 0.43 nm2 for hematite and goethite, respectively, assuming uniform distribution over the BET area (Atkinson et al., 1967; Hingston et al.. 1972). The calculated charge on goethite is one positive charge per 0.30 n d on the (100) face, assuming that there is one proton per unit cell on the (100) face, and one negative charge per 0.14 n d on the (010) face, assuming that there is one Lewis acid site per unit cell on the (010) face. This corresponds with positive and negative charges of one per 0.37 n d and 0.70 nm', respectively, where the total surface area is used in the calculation, which agrees with the experimental results of Atkinson et al. (1967). Breeuwsma and Lyklema (1971, 1973) measured the surface charge of hematite with a range of electrolytes and found that divalent cations were more strongly adsorbed than monovalent cations, which were weakly adsorbed. The maximum negative charge occurred with Mg2+ ions, where one proton desorbed per 0.20 n d . They concluded that the results could be explained satisfactorily in terms of the Gouy-Stern theory. The surface charge can also be determined by measuring the adsorption of indifferent ions at a range of pH values (Bolland et al., 1976). Hingston et al. (1972) found that the positive charge on a synthetic gibbsite in 0.005 M NaCl increased from 20 peq g-I at pH 7 to 50 p eq g-' at pH 4, using both C1 adsorption and potentiometric titrations. The sites that accept protons are modified when ligand exchange occurs, and the pzc usually shifts to lower pH as surfaces become more acidic and therefore accept fewer protons at any one pH. The negative charge added to the surface

12

R. L. P A W

when ligand exchange takes place on goethite was -0.38 eq mol-' of silicate, -0.7 eq mol-I of selenite, and -1.0 eq mol-I of phosphate (Hingston et al., 1968b, 1972; Parfitt and Atkinson, 1976).

D. LIGAND EXCHANGE

Ligand exchange can also be used as a method of estimating the number of surface sites. Phosphate has been used for this purpose, since it is very strongly adsorbed, replaces a very large proportion of the reactive OH, and often has a well-defined adsorption maximum (Atkinson et al., 1974). Fluoride adsorption and the determination of OH- ions released during fluoride adsorption has recently been used on a quantitative basis as a method for estimating reactive hydrous oxides in soils, and it may be possible to develop this method further so that specific sites can be identified (Perrott er al., 1976a,b). IV. Adsorption Mechanisms

A. GOETHITE (a-Fe00H)

Synthetic goethite can be prepared with a very well defined crystal surface. The predominant (001) face consists of rows of one-, two-, and three-coordinated OH (A, C, and B types, respectively) separated from the next three rows by a groove where oxide ions are exposed (Figs. 3 and 6) (Atkinson, 1969; Russell et al., 1974). Parfht et al. (1976) showed that a high-surface-area preparation of goethite had 410 pmol g-' of A-, B-, and C-type OH and C-type oxide ions exposed on the (100) face. The A-type OH were the only groups involved in ligand exchange, but the B- and C-type OH could form hydrogen bonds with adsorbing ligands. The (010) face was shown to be made up of 220pmol g-'.of Lewis acid sites and 220pmol g-' of two coordinated (C-type) OH ions. The surface area of this goethite preparation was calculated to be 90 d 8'. The mechanism of phosphate adsorption on goethite has been studied in more detail than has any other similar reaction. Atkinson et al. (1972) showed that the rate of exchange of 32Pon phosphated goethite was relatively slow, suggesting the formation of a binuclear bridging Fe OP(0) ,O * Fe surface complex rather than a monodentate Fe*OP(O), complex. This mechanism is consistent with the strong adsorption that has been observed in adsorption studies (Atkinson, 1969; Yates and Healy, 1975) and with the observation that phosphate could not be desorbed from goethite by washing at low pH (Hingston et al., 1974). Infrared studies have provided direct evidence for the formation of a bridging complex on goethite over the whole range of surface coverage (Atkinson et al.,

ANION ADSORPTION BY SOILS

13

FIG. 6. Ideal structure of goethite (a-FeOOH) showing surface OH (white), A-type OH (gray), and Lewis acid sites (black).

1974; P d i t t er af., 1976; P d i t t and Atkinson, 1976; Parftt and Russell, 1977), and it has been shown that the evacuated bridging complex is present as (FeOhPOOH rather than as (FeOkPOO- (Russell et al., 1975; P d i t t et al., 1976). Russell et al. (1974) showed that phosphate replaced A-type OH, and they suggested that the POH group formed a hydrogen bond to surface C'-type F e . 0 groups in the grooves on the (100) face (Russell et af., 1975) (Fig. 7). The evacuated bridging complex appears to retain a proton even at high pH (Parfht et al., 1976). Recent infrared and potentiometric titration results with goethite in suspension have shown that the bridging complex is ionized at high pH and protonated at low pH (Parfitt and Atkinson, 1976). The pH of net zero charge depends on the level of adsorbed phosphate. At half-coverage (100 pmol g-' phosphate) this pH is 5.1, compared with 8.1 for nonphosphated goethite in 0.01 M NaC1. The equations for phosphate adsorption at pH 3.6, 5.1, and 8.1 are

+

100

HPO:

+

-

FeOIOOLeo

p-O

-I

+ 100 OH- + 100 H 2 0

14

R. L. PARFITT

FIG. 7. Model of goethite with HPO, adsorbed on (100) face.

Hingston et al. (1968a, 1971, 1972, 1974) studied the adsorption of SO:-, YSiOL, H,POr, Moq-', S e a - , H,AsO;, and F on goethite and gibbsite and showed that these anions were selectively adsorbed in the presence of Cl-. This indicated that specific adsorption was taking place. It was suggested that these anions were adsorbed on goethite and gibbsite by ligand exchange with surface OH or OH: groups. Anions of fully dissociated acids are adsorbed if the surface carries a positive charge; thus, S 4 - is adsorbed only on the acid side of the pzc. However, anions of incompletely dissociated acids can also be adsorbed on the alkaline side of the pzc, since they can provide a proton, which is needed for removal of a surface OH at the adsorption site. Maximum adsorption occurs at a pH close to the pK of the acid, where the surface potential and the concentration of the adsorbing hydrolyzable ion are optimal (Bowden et al., 1974). Both C1- and NO; are adsorbed only at low pH when the surface is positively charged. This is consistent with chemical data showing that OH- and H,O are more strongly attracted to Fe3+ and A P than are NO,- and Cl-. When HNO, and HCl are dried onto goethite and evacuated, it appears that ligand exchange can occur (Parfitt and Russell, 1977). P d i t t and Russell (1977) examined the spectra of surface OH groups of goethite in the presence of a range of adsorbed anions. The experiments showed that sulfate and selenite could replace all A-type OH, suggesting that binuclear complexes were formed. This was confirmed by the observation that at half-

ANION ADSORPTION BY SOILS

15

coverage the remaining A-type OH hydrogen bonds were lengthened by an amount that depended on the anion oxygen-oxygen distance. This conclusion is consistent with (a) the strong adsorption observed for selenite and sulfate on iron surfaces (Aylmoreetal., 1967; Hingstonetaf., 1968b, 1971), ( 6)theobservation that selenite cannot be desorbed from goethite (Hingston et al., 1974), and (c) an adsorption maximum of about 200 pmol g-', giving one anion per two A-type FeeOH. Parfitt and Smart (1977, 1978) examined the S-0 stretching spectrum of sulfate adsorbed on iron oxides and confirmed that sulfate formed binuclear bridging complexes. A similar spectrum was obtained on a wet film of sulfate and goethite, suggesting that the complex is present not only on drying but also in suspension (R. L. Parfitt, unpublished results). However, Yates and Healy (1975) compared the rate and extent of sulfate adsorption with phosphate adsorption at pH 6.15 and suggested that sulfate was not involved in ligand exchange on goethite. Borate, molybdate, and silicate are adsorbed on goethite by ligand exchange (Hingston er al., 1972), and infrared spectra show that A-type OH are replaced during the reaction (Pditt and Russell, 1977). Silicic acid behaves as a weak monobasic acid (pK = 9.6); thus, only one goethite OH can be replaced by silicate. The surface complex may be in the form Fe.OSi(OH),. Boric acid is a Lewis acid that accepts OH- (pK = 9.0), and the reaction with goethite probably gives Fe.OH.B(OH),. Hingston et al. (1974) and Bowden et al. (1974) showed that fluoride is adsorbed on goethite by a ligand exchange reaction. More recently Parfitt et a f . (1976) found that only A-type OH were exchanged, and the B- and C-type OH were inert to fluoride. This is consistent with an isotherm maximum near 400 pmol g-' for fluoride adsorption on a high-surface-area goethite (Hingston et al., 1974). Clean preparations of goethite adsorb atmospheric carbon dioxide to give a surface carbonate species (Russell et al., 1975). However, most anions, except for NO;, are adsorbed more strongly on goethite and block the adsorption sites. The halogens Br- and I- show adsorption behavior similar to that of Cl- . On air drying HCl, HBr, or HI with goethite, some ligand exchange with A-type OH takes place, but some HCl, HBr, and HI is also adsorbed by hydrogen bonding (Parfitt and Russell, 1977). In work with organic ligands Watson et a f . (1973) suggested that 2,4-D was weakly adsorbed on goethite by ligand exchange. P d i t t et al. (1977a) showed that benzoate was also weakly adsorbed, with one carboxylate oxygen replacing one A-type OH and the other carboxylate oxygen keyed into the surface groove so that the aromatic ring is at a high angle to the (100) face. Appelt et al. (1975a) showed that p-OH benzoate, salicylate, and phthalate were more strongly adsorbed than was benzoate. Low levels of oxalate are strongly adsorbed on goethite in the binuclear form

16

R. L. PARFIlT

(Fe * 00CC00 * Fe). At higher surface coverage oxalate is more weakly adsorbed and is in the monodentate form (Parfitt et al., 1977a). The adsorption of fulvic acid and humic acid on iron oxides has been studied by a number of workers (Greenland, 1965). Recently it has been shown that both fulvic acid and humic acid are strongly adsorbed on goethite by ligand exchange. The carboxylate groups replace several A-type OH, giving multiple points of contact. Additional mechanisms of adsorption include hydrogen bonds and entropy effects. Van der Waals bonding did not appear to contribute significantly to the adsorption (Parfitt et al., 1977~).

B . HEMATITE ( o l - F ~ O 3 )

Although the oxygen within hematite crystals is present as oxide, the ideal surface is composed entirely of hydroxide ions in one and two coordination (Parfitt et al., 1975). However, Atkinson et al. (1967) suggested that the actual degree of order on the hematite surface depended on the method of preparation. Most studies have been carried out with hematite that is prepared by hydrolysis of ferric nitrate solutions under reflux conditions. Such preparations usually contain a small amount of goethite as a separate phase. Some goethite may also be present as a surface coating on hematite, but differences between the infrared spectra for phosphated goethite and hematite suggest that the hematite surface is different from the goethite surface. An infrared study of phosphate adsorbed by drying on hematite gave results that were consistent with an ordered hematite surface, (Parfitt et al., 1975), but Breeuwsma and Lyklema (1971), using potentiometric titration, DTG, and N2 adsorption data, concluded that the surface was porous to cations, N2,and water, but not to anions. It is likely that hematite suspensions have a coating of amorphous iron hydroxide, which becomes more crystalline on drying (Atkinson et al., 1967; Breeuwsma and Lyklema, 1971, 1973). Jurinak (1966) found that surface OH groups on hematite heated to 500°C were regenerated by water vapor adsorption and that each OH regenerated occupied 0.22 n d . Jurinak (1966) and Parfitt et al. (1975) found that one phosphate ion was adsorbed also on each 0.22 n d of surface. Jurinak (1966) also found that phosphated hematite had one surface OH per 0.125 n d , which suggested that two POH groups now occupied one FeOH site (that is, the phosphate was monodentate Fe - 0 .PO(OHX, with two OH groups exposed). However, Parftt et al. (1975), on the basis of infrared spectra, suggested that phosphate was adsorbed in the bridging form. Breeuwsma and Lyklema (1973) used a hematite which they considered was slightly porous to cations, and they concluded that phosphate replaced O&+ groups at low pH and OH at high pH. Kuo and Lotse (1974) investigated the

ANION ADSORPTION BY SOILS

17

kinetics of adsorption and desorption of phosphate and found that the adsorption process required a very low activation energy. Sulfate adsorption has been studied by Jurinak (1966), Aylmore ef al. (1967), and Breeuwsma and Lyklema (1973); the results were consistent with ligand exchange. Jurinak (1966) suggested that sulfate was adsorbed in the monodentate form, but infrared results indicated that the bridging complex was formed (Parfitt and Smart, 1978). Molybdate adsorption is more complex, and paramolybdate probably forms on the surface at high concentrations (Reyes and Jurinak, 1967). Microcalorimetry showed that the surface energy of hematite was lower after anion adsorption (Jurinak and Burau, 1967).

C. OTHER IRON OXIDES

The crystal structure of lepidocrocite (7-FeOOH) is given in diagrammatic form by Wells (1962). The ideal surface consists of rows of one-, two-, and three-coordinated OH ions. The crystal structure of a akaganeite @I-FeOOH)consists of multiple octahedral chains joined up along their lengths by sharing comers. It probably has rows of OH ions in one, two, and three coordination exposed at the surface (Gallagher, 1970; Parfitt ef al., 1975). Infrared spectroscopy has shown that both phosphate and sulfate are adsorbed as binuclear bridging complexes on lepidocrocite and akaganeite (Parfitt et al., 1975; Parfitt and Smart, 1978).

D. GIBBSITE AND OTHER ALUMINUM SURFACES

The mechanism of anion adsorption on aluminum hydroxides is less well understood than that on iron oxides because the surfaces are less well defined. However, synthetic gibbsite can be prepared in a very well crystallized form (Russell et al., 1974). The crystal structure of gibbsite is given by Bragg and Claringbull (1965). Synthetic gibbsite consists of well-ordered hexagonal crystals, and, although the (001) face predominates, the edge faces contain the reactive sites (Parfitt et al., 1977b). In the ideal structure each A13+ ion exposed on the edge faces is coordinated to one H,O and one OH ion, while each OH on the (001) face is coordinated to two A13+ ions below the surface layer. Russell et al. (1974) found that five different types of surface OH on the (001) face could be detected by infrared spectroscopy. None of these surface OH groups exchanged with phosphate or oxalate (Parfitt et al., 1977b). Alvarez et al. (1976), using laser Raman spectroscopy, observed four bands,

18

R. L. P A R F m

at frequenciesclose to the infrared frequencies of bulk OH. Although the gibbsite had a low surface area, it was suggested that they were surface OH, since the intensity varied with anion adsorption. Muljadi et al. (1966a,b,c) suggested that phosphate adsorption on gibbsite from dilute phosphate solutions took place on the edge faces, and entropy factors were a very significant driving force in the reaction. They indicated that ligand exchange occurred and that phosphate was adsorbed in a monodentate form. However, later isotopic exchange work by Kyle et al. (1975) showed that phosphate was probably adsorbed as a bridging complex. Parfitt et al. (1977b) studied the adsorption of phosphate, oxalate, and benzoate on a synthetic gibbsite that had about 60pmol g-' Al.(OH)(H,O) exposed on the edge faces. The adsorption isotherms showed that 25 pmol g-' phosphate and 21 pmol g-' oxalate were strongly adsorbed on this preparation; for phosphate the adsorption maximum occurred at 70 pmol 8'. Infrared data showed that up to 80 pmol g-' oxalate was adsorbed by ligand exchange with Al. This supports earlier conclusions that the edge Al*(OH)H,O groups react with phosphate and oxalate and suggests that the complexes probably are in a binuclear or bidentate form. No reaction with the (001) face Al*OH*AIgroups was observed, since the five infrared bands due to these surface OH were unchanged, as were the four bands due to OH within the crystal. Muljadi ef al. (1966a) and Kyle et al. (1975) showed that gibbsite adsorbed more than 200 pmol g-' phosphate at high solution concentrations, but their preparations may have included some less-crystalline but very reactive phase. At high concentrations at pH 5 , phosphate adsorption continued to increase, and some concomitant potassium adsorption occurred at the higher concentrations. Muljadi et al. (1966a) suggested that this adsorption occurred on the lesscrystalline phase. Pditt et al. (1977b) found the plateau was at 70 pmol g-' in a well-crystallized gibbsite, and thus the crystallinity of gibbsite is important in controlling the amount of phosphate adsorbed. Helyar et al. (1976a,b) studied the kinetics of adsorption and desorption of phosphate on a commercial synthetic gibbsite and found that the initial rapid adsorption was followed by a slow reaction. More phosphate is adsorbed in the presence of Ca ions than in the presence of Na, K, or Mg, and it was postulated that two phosphate ions on the (001) face formed a complex with one Ca ion, which allowed increased phosphate adsorption. However, this seems unlikely, since infrared results show that phosphate is not adsorbed on the (001) face, and Ca causes increased phosphate adsorption on other oxides and soils (Ryden and Syers, 1975b; R. L. Parfitt,unpublished results). It also seems likely that the commercial gibbsite contained a small amount of high-surface-area amorphous material, since the calculated surface area is much less than the measured surface area.

ANION ADSORPTION BY SOILS

19

At very high concentrations of phosphate, precipitation or growth of a new crystal phase probably takes place (Bache, 1964; Muljadi et al., 1966a). Hingston et al. (1972, 1974) determined adsorption envelopes for sulfate, selenite, molybdate, and silicate on gibbsite and concluded that the results were consistent with ligand exchange reactions. Boehmite (7-A100H) has a structure similar to that of lepidocrocite, and pseudoboehmite is a less-crystalline form of boehmite. Aylmore et al. (1967) showed that sulfate was strongly adsorbed on pseudoboehmite at pH 4.6, and little sulfate could be desorbed. When phosphate is adsorbed on mixed aluminum hydroxides, OH ions are released and surface positive charge is decreased (Rajan et al., 1974; Rajan, 1975a, 1976). Interpretation of these data is difficult, since both the phosphate and the aluminum hydroxide can accept or release protons. Rajan (1976) suggested that, at pH 4, H,POr was adsorbed initially on Al.OH,+, sites and with increasing phosphate coverage Al. OH sites reacted to form monodentate complexes, A1 * H,PO,". At high phosphate concentrations the phosphate reacted with surface A1 * OH * A1 groups. Chen et al. (1973a,b) studied phosphate adsorption on a-alumina and found that 15 pmol g-' was strongly adsorbed. The adsorption envelopes had a maximum at pH 4, and phosphate adsorption was decreased by the presence of chelating anions. The rapid phosphate adsorption reaction was followed by a slow reaction when hexagonal crystals were formed. Van Riemsdijk et al. (1975, 1977) also observed the growth of hexagonal crystals with aluminum hydroxide and x-ray data and suggested that they were crystals of sterrettite. In a study using y-A&O,, Huang (1975a) also found that maximum adsorption occurred near pH 4 with high levels of phosphate but shifted to higher pH with low levels of phosphate. The specific chemical energy of adsorption was estimated to be -16 kl mol-I. At high phosphate concentrations the reaction is complicated, since surfaces containing aluminum react to form new phases such as taranakite (Wada, 1959; Taylor et al . , 1965; Tamimi et al., 1968). It has been suggested that when A1 occupies cation exchange sites it is present both as A P and as a basic cation with an empirical formula Al,(OHX+ (Brown and Newmann, 1973). Muljadi et al. (1966b) have shown that aluminum in this form is able to react strongly with phosphate, and it is likely that exchangeable aluminum is a site for ligand exchange. Rich (1968) has reviewed the literature on the formation of hydroxyaluminum species. It appears that interlayer hydroxyaluminum does not take part in anion exchange reactions in the interlayer surface region of expansible layer silicates (Huang, 1975b). Colombera et al. (1971) showed that hydroxyaluminum species could form on illite surfaces; Greenland (1971) gave them the name outlayers and

20

R. L. PARlTlT

suggested that reactive aluminum in soils was in this form and probably is involved in ligand exchange reactions.

E. AMORPHOUS HYDROXIDES Amorphous iron and aluminum hydroxides have less well defined surfaces than the crystalline hydrous oxides. Femhydrite, amorphous ferric hydroxide, consists of spherical particles, 10-20 nm in diameter, with a large surface area (100-300 m2 g-') and a defective hematite structure where some 0 ions are replaced by water and some Fe positions are vacant (Schwertmann et al., 1974). Amorphous aluminum hydroxide is unstable and rapidly crystallizes to pseudoboehmite and bayerite. Reactions that have been studied include adsorption with silicic acid (Beckwith and Reeve, 1963; Hingston and Raupach, 1967), borate (McPhail et al., 1972; Sims and Bingham, 1968a), phosphate (De, 1961; Hsu and Rennie, 1962; Bache, 1964; Hasan and Pollard, 1966; Ryden and Syers, 1975a), iodide (Whitehead, 1974), arsenate (Anderson et al., 1976), and molybdate (Jones, 1957; Reisenauer et al., 1962), and the results are consistent with ligand exchange. Ryden and Syers (1975a) suggested equations for phosphate adsorption at different surface coverage, but pH was not controlled in these experiments. Parfitt et al. (1975) and Parfitt and Smart (1978) have shown that phosphate and sulfate are adsorbed on amorphous Fe(OH),, and both form a binuclear bridging complex. Allophane has been defined as a naturally occurring hydrous aluminosilicateof varying composition yet with short range order, Si-0-A1 bonds, and a distinct DTA trace (Wada and Harward, 1974). Allophane particles are probably spherical, with a diameter of about 5 nm and a structure consisting of a glass-like aluminosilicate core with an outer surface of aluminum surrounded by an octahedral arrangement of water and OH- ions. Some SiOH groups may also be exposed at the surface. F8+ ions are often found in association with allophanes, and reactive OH and H,O ligands are probably associated with the iron as well as the aluminum. The negative charge of an allophane measured by Na+ adsorption at (pH 7) was 135 meq g-' , and the pH of zero charge varied from pH 7 to lower values with different allophanic material (Wada and Harward, 1974). Ghosh and Battacharyya (1930) and Cloos et al. (1968) studied the adsorption of phosphate on synthetic silica aluminas and found that adsorption increased as the aluminum content increased. It was suggested that adsorption took place on positively charged sites and with OH groups on surface hydroxyaluminum cations.

ANION ADSORPTION BY SOILS

21

Rajan (1975a,b,c) and Rajan and Perrott (1975) showed that low concentrations of phosphate were adsorbed by ligand exchange on silica aluminas and soil allophanes. Some adsorbed sulfate, and silicate was displaced in addition to OH ions and H,O. At higher concentrations hydroxyaluminum polymers were disrupted, and structural silicate was displaced by phosphate but not by selenite (Rajan and Watkinson, 1976). Inoue and Wada (1968, 1971a,b) found that the adsorption of humic material on allophane, imogolite, and montmorillonite followed a Langmuir curve. Allophane adsorbed the largest amount, and it was concluded that adsorption was by ligand exchange of carboxylate groups with the coordination shells of A1 atoms and by van der Waals bonding. The structure of imogolite has been determined by Cradwick et al. (1972). The external surface of the tubes has a face similar to the gibbsite (001) face. Phosphate adsorption probably can occur on this face as well as on sites at the ends of the tubes where broken bonds occur. Other sites within the tubes contain Al-OH and Si. OH groups, and it is unlikely that anion adsorption occurs in this region (Parfitt et al., 1974). P d i t t et al. (1974, 1977b) suggested that phosphate and oxalate were adsorbed on imogolite by ligand exchange on the external surfaces of the tubes and at the end of tubes. However, the adsorption was weaker than on gibbsite or allophane.

F. CLAY MINERALS Some clay minerals have a pH-dependent charge which occurs at the edges of the crystals where Al.(OH)H,O groups are exposed. The Al*OHgroups are the sites that accept a proton at low pH to become AlaOH; (Schofield, 1949; Schofield and Samson, 1953; Bolland et al., 1976). Muljadiet al. (1966a) found that the positive charge on a high-surface-area kaolinite was 0.95 meq per 100 g at pH 3. At low solution concentrations phosphate is adsorbed on some clay mineral surfaces (Low and Black, 1950; Kuo and Lotse, 1972), but at high phosphate concentrations precipitation occurred, resulting in the formation of new crystalline phases such as taranakite (Kittrick and Jackson, 1954, 1955, 1956; Wada, 1959). The mechanism of adsorption is by exchange of phosphate with AI-OH groups on the edge sites of clay minerals (Kelley and Midgley, 1943; Low and Black, 1950; Mehlich, 1964; Pissarides et al., 1968). Muljadi et al. (1966a,b) showed that phosphate adsorption on K-kaolinite occurred on the edges of the crystals, and each phosphate ion occupied 0.28-

22

R. L. P A m

0.41 d . Each Al-(OH)H20exposed on the edges occupies 0.33 n d , suggesting that one phosphate ion is adsorbed on each A1 ion. Kafkafi et al. (1967) suggested that, since two adjacent Al*OHwere 0.296 nm apart, some phosphate cou€dbe fixed on kaolinite as a binuclear complex. However, the major part of the phosphate was exchangeable and was thought to occur in a monodentate form. Kuo and Lotse (1972) suggested that phosphate exchanged with Al*&O groups on kaolinite rather than AlmOH, since (a) adsorption increased with decrease in pH, and (6) no release of OH was observed. These effects can now be explained by considering surface OH; groups. When exchangeable A1 i s present in kaolinite, approximately half of the A1 is able to adsorb phosphate (Muljadi et al., 1966b). It is possible that only one of the two forms of A1 described by Brown and Newmann (1973) is reactive. This is also consistent with earlier observations (Coleman, 1944, 1945; Haseman et al., 1950; Russell and Low, 1954; Hemwall, 1957b; Coleman et al., 1960; HSU, 1965, 1968; Hall and Baker, 1971). Pissarides et al. (1968) showed that the exchangeable cations influenced the amount of phosphate that could be adsorbed on edge sites of clay minerals, and on Na-montmorillonite there was negative adsorption owing to diffuse doublelayer effects. Parfitt (1972) also found that negative adsorption occurred r - ~ Na-montmorillonite with uronic acid at pH 6, but positive adsorption took place at low pH or if Al was present on the exchange sites. When aluminum and iron hydroxyl species are present on mica surfaces, phosphate and sulfate adsorption are greatly increased (Rankin and Wilson, 1969; Langdon et al., 1973; Perrott et af., 1974a). It was suggested that phosphate reacted initially by adsorption on A1 and Fe sites, and then this was followed by a rearrangement reaction. Kodama and Singh (1972) and Kodama and Webber (1975) found that phosphate and sulfate could be incorporated into montmonllonite interlayers. However, the reaction involved a precipitation reaction with aluminum, giving AlPO4nHzO and A~(OHX.S(SO~)O.,S. Hudcova (1970) also studied the adsorption of phosphate on clay minerals and found that, although kaolinite adsorbed most phosphate, the adsorption energy was greatest on illite. Schell and Jordan (1959) showed that montmorillonite adsorbed more phosphate and sulfate than did halloysite or kaolinite. When silica was adsorbed on kaolinite, equal amounts of phosphate were desorbed, which suggested that adsorption occurred on similar sites (Kafkafi and Bar-Yosef, 1969). Maximum silica adsorption occurred near the pK value of the silicic acid (Bar-Yosef et af., 1969). The surface area, the surface aluminum and iron, the pH, and the exchangeable cations are the major factors influencing phosphate adsorption on clay minerals, and they explain the differences between clay minerals (Edzwald et al.,

ANION ADSOWION BY SOILS

23

1976). Results of Frost and Griffin (1977) suggest that these factors also control the extent of selenite and arsenate adsorption. Aylmore et al. (1967) found that sulfate was adsorbed by kaolinite, and they suggested that adsorption occurred by ligand exchange on edge sites. Initially sulfate was strongly adsorbed, but at higher supernatant concentration the adsorption was reversible with respect to concentration. At maximum adsorption one sulfate ion would be adsorbed on 0.67 n d and 1.33 n d for the two kaolinites studied, assuming an edge area of 4 d g-' (Muljadi et al., 1966a). This represents lower surface coverage than with phosphate. Bower and Hatcher (1967) studied the adsorption of fluoride on clay minerals and found that more fluoride was adsorbed on kaolinite and halloysite than on montmorillonite and vermiculite. In two studies of borate adsorption on clay minerals, Hingston (1964) and Sims and Bingham (1967) found that maximum adsorption occurred at pH values of 9-10. Borate retention was largely attributed to hydroxyiron and hydroxyaluminum inpurities in the clay minerals. Couch and Grim (1968) showed that borate adsorption on illite consisted in a rapid reaction and a slow adsorption process. They suggested that the former was due to B(OH)L adsorption on edge sites and the latter to diffusion of boron into tetrahedral sites. The results of Jasmund and Lindner (1973) support these conclusions. The mechanisms of adsorption of organic anions on clay minerals have been reviewed by Greenland (1965, 1971) and Mortland (1970).

G . CALCITE (CaC03)

Phosphate adsorption on calcite surfaces can be described by a Langmuir equation (Cole et al., 1953; Kuo and Lotse, 1972; Holford and Mattingly, 1975b). The reaction involves three steps: (a) chemisorption of phosphate accompanied by heterogeneous formation of nuclei of amorphous calcium phosphate; (b) a slow transformation of these nuclei into crystalline calcium phosphate; and ( c ) crystal growth of calcium phosphate (Stumm and Leckie, 1971; Griffin and Jurinak, 1973, 1974). The calcium phosphate species which is nucleated depends on the initial phosphate concentration. At low phosphate concentrations Griffin and Jurinak (1974) found that hydroxyapatite was formed, although Amer and Ramy (1971), using solubility measurement and isotopic exchange, suggested that octacalcium phosphate was formed from phosphate concentrations between 1.1 and 1.7pg ml-' . Lahav and Bolt (1963) showed that the calcite surface was modified by dissolved components from soil solution, suggesting that calcite in soil will have different surface properties from pure calcite. This has been discussed in more detail by Mattingly (1975).

R. L. PARFI’IT

24

V. Identification of Adsorption Sites in Soils

A. SURFACE IRON AND ALUMINUM

The reactive sites for anion adsorption in pure systems are the singly coordinated Al-OH and Fe-OH groups, which are exposed at surfaces. These groups are present at the edges of clay minerals as well as on the surfaces of hydrous oxides, and therefore they are present in most soils (Mott, 1970). The nature and distribution of the reactive iron and aluminum components in soils have been described elsewhere (Oades, 1963; Mitchell et al., 1964; Rich, 1968; Coulter, 1969; Greenland, 1971; Wada and Harward, 1974; Jones and Uehara, 1973). The OH sites in two-coordinated Al-(OH).Al do not usually take part in ligand exchange reactions in pure systems, although they can form hydrogen bonds. The Lewis acid sites Al*OHz and Fe.OHz also occur on the edges of minerals. Under certain conditions they can react with Lewis bases such as ammonia to give Fe-NH, and Al-NH,, although under soil conditions water is held more strongly than ammonia. At high pH these sites become negatively charged: AI.OH,

+ O K + A I . O K + H,O

The sites that adsorb protons at low pH are probably the one-coordinated A1 * OH and Fe * OH groups, which give A1 * O&+ and Fe * OH: . On some oxides and oxyhydroxides FeO groups may also be exposed at the surface, and they may become protonated (FeOH+) at low pH. Several workers have used Schofield’s (1949) method of chloride adsorption to measure the positive sites on soils (Deshpandeel al., 1964; Tweneboah et al., 1967; Moshi et al., 1974). Others have measured the charge characteristics of soils by potentiometric titration (van Raij and Peech, 1972; Espinoza et al., 1975; El-Swaify and Sayegh, 1975; Gallez et al., 1976). However, some sites will not be detected by these methods if they are blocked by other adsorbed anions (Deshpande et al., 1968). Fieldes and Perrott (1966) have used fluoride exchange as a test for allophane, and Brydon and Day (1970) showed that this reaction also occurs with other amorphous soil material. The test is probably not specific for identifying ligand exchange sites in soil, since Al-OH.A1 and Si-OH groups react with fluoride in the pH range 6-7 where this reaction is carried out (Perrott et al., 1976a). However, tests with fluoride do give an indication of the amount of poorly ordered material present in soils. If Fee OH and Ale OH sites already hold organic anions, fluoride must compete with these anions for the sites, and therefore tests with fluoride are not suitable for surface soils (Perrott et al., 1976a). Recent results suggest that fluoride exchange at pH 8 may be useful in estimating ligand exchange sites (Perrott et al., 1976b). Many workers have correlated extractable iron and aluminum in soils with

ANION ADSORF’TION BY SOILS

25

anion adsorption data. Tamm’s acid oxalate reagent has been widely used to extract iron and aluminum from soils (Tamm, 1922; Schwertmann, 1964; Schwertmann et al., 1968; Daly and Binnie, 1974; Juo et al., 1974). Landa and Gast (1973) have shown that amorphous Fe(0Hh was extracted by this reagent but goethite was not dissolved. When used on soil, Tamm’s reagent is thought to cause dissolution of amorphous iron and aluminum compounds. The reaction with iron is largely a photochemical reaction that requires ultraviolet light (Schwertmann, 1964), but aluminum ions are brought into solution as oxalate complexes. Exchangeable aluminum, AI*OB+ions, and A1 at edge sites are probably dissolved in addition to amorphous aluminum hydroxides and amorphous aluminosilicates. The exact nature of amorphous or disordered material is not well understood, but such material has been found in measurable amounts in volcanic ash soils, poorly drained soils, tropical soils, and podzols (Mitchell et af., 1964; Wada and Harward, 1974). Buffered dithionite solutions have been used to reduce free iron oxides, which can then be extracted in citrate or acid solutions. These reagents will dissolve crystalline iron oxides in addition to the amorphous material dissolved by Tamm’s acid oxalate. Thus, dithionite extracts give no indication of the surface Fe-OH, since the iron oxides are completely dissolved. Dithionite is not completely specific for extraction of iron from soil, since aluminum and silicon are also brought into solution (Habibullah et af., 1972; Juo et al., 1974). It is doubtful if iron and aluminum can be separated completely, since soil goethites contain some aluminum, which substitutes for ferric ions in the structure (Nomsh and Taylor, 1961). Therefore, both iron and alunimum are brought into solution during dissolution of soil goethite. Surface coatings of iron and aluminum hydroxides can be formed on the external surfaces of clay minerals (e.g., Greenland, 1971; Colombera et al., 1971), and these substances have been shown to adsorb anions (Sims and Bingham, 1968b; Langdon et al., 1973; Perrott et al., 1974a,b; Huang, 1975b). Sree Ramulu et al. (1967) and Huang (1975b) have shown that similar material in 2: I clay interlayers is not active in anion adsorption. Tweneboah et al. (1967) suggested that aluminum coatings could be extracted with 0.5 M CaCI, at pH 1.5; however, a small amount of iron and silicon is also extracted with this reagent. Dithionite citrate bicarbonate solution has also been used to remove coatings from clays, but silicon and aluminum as well as iron are dissolved (e.g., Roth et al., 1969), so the exact nature of the iron compounds is uncertain. B. ORGANOMETALLIC COMPLEXES

Phosphate can react with metal ions such as cobalt to form monodentate or bidentate complexes in the presence of other organic ligands-for example,

26

R. L. PARFTlT

Co(en)P04 and Co(N&kP04 (Lincoln and Stranks, 1968). Phosphato-iron-III and aluminum complexes form in solution only at low pH (Bohn and Peech, 1969), but humic acid containing ferric ions is able to hold P in solution at higher pH (Weir and Soper, 1963). Humic acid and fulvic acid form complexes with aluminum as well as ferric ions (Schnitzer and Skinner, 1964; Schnitzer, 1969). Aleksandrova (1954) reported that part of the aluminum that reacted with humic acid was exchangeable and could adsorb phosphate and other anions (Appelt et al., 1975b). Although iron is strongly complexed by humic acids, Fokin and Sinkha (1970) showed that phosphate can be adsorbed by the complex, part of the phosphate being isotopically exchangeable at pH 4. Phosphate was adsorbed more strongly by an ironfulvic acid complex. Iron and aluminum components of soil organic matter are also important in the adsorption of anionic surfactants (alkylate sulfonates) by soils (Krishna Murti et al., 1966).

C. EXTRACTION OF PHOSPHATE

Chang and Jackson (1957) developed an extraction procedure that they claimed was able to separate the phosphate held by aluminum, iron, and calcium. In their procedure 0.5 M NaF was used to dissolve aluminum from soils, thus releasing phosphate held by the aluminum. However, some phosphate held by iron and calcium is also released in the process, and some of the aluminumbound phosphate is readsorbed on other sites (Bromfield, 1967, 1970). Then 0.1 M NaOH was used to displace phosphate held by ferric ions, but some aluminosilicates will be dissolved by this treatment, and phosphate substituting for silicate will also be released. Calcium phosphates are dissolved in a final treatment with 0.5 M sulfuric acid. Because of the uncertainty of the method, results obtained with the Chang and Jackson procedure should be treated with caution. VI. Adsorption by Soils

A. PHOSPHATE

Phosphate adsorption by soils has been the subject of extensive reviews (Dean, 1949; Wild, 1950b; Hemwall, 1957a; Smith, 1965; Larsen, 1967; Ryden ef al., 1973). Most reviewers have dealt with the precipitation mechanism and the adsorption mechanism of phosphate “fixation. ” Some papers suggest that, in acid soils, phosphate is associated with hydrous oxides of iron and aluminum, and it is unlikely that discrete crystalline iron and aluminum phosphates persist in

ANION ADSORITION BY SOILS

27

soils (e.g., Bache, 1963, 1964). However, in the immediate vicinity of phosphate fertilizer particles, there are local conditions of low pH and high phosphate concentration, which may cause dissolution of clays and reprecipitation of phosphates. Later work suggests that basic aluminum phosphates may form in acid soils even at low phosphate concentrations (White and Taylor, 1977; van Riemsdijk et al., 1975, 1977). In neutral and calcareous soils calcium phosphates are formed, and, if calcite is present, hydroxyapatite and calcium phosphates are adsorbed on the CaCO, surface. 1 , Adsorption Sites

Phosphate adsorption by soils is usually determined by shaking the soil with phosphate solutions in an indifferent electrolyte for a given time. The phosphate remaining in solution is measured, and the phosphate adsorbed can be calculated. The adsorption isotherm is given by a plot of adsorbed phosphate against phosphate remaining in solution. This procedure has been used by many workers to measure the phosphate adsorption capacity of soils (e.g., Fox et al., 1969; Barrow, 1970; Bache and Williams, 1971; Rajan and Fox, 1972; Anderson et al., 1974; Gebhardt and Coleman, 1974~). Many workers, often using a single point on the isotherm, have correlated the phosphate adsorption capacity with other soil factors. Most results show that phosphate adsorption is better correlated with extractable aluminum than with iron (Williams et al., 1958; Saunders, 1965; Fassbender, 1969; Harter, 1969; Syers er al., 1971; John, 1972; Udo and Uzu, 1972; Leal and Velloso, 1973; Lopez-Hernandez and Burnham, 1974a; Evans and Smillie, 1976). However, some results show that either aluminum (Bromfield, 1965; Schwertmann and Knittel, 1973) or iron alone (Myszka and Janowska, 1973) is correlated with phosphate adsorption. Other workers have found a correlation with organic matter (Saunders, 1965; Myszka and Janowska, 1973; Leal and Velloso, 1973; Harter, 1969; Fassbender, 1969; John, 1972; Lopez-Hernandez and Burnham, 1974a), pH or clay content (Udo and Uzu, 1972; Schwertmann and Knittel, 1973), or calcium carbonate (Kacar, 1967). Phosphate adsorption can also be correlated with exchangeable aluminum in soils (Franklin and Reisenauer, 1960; Syers et al., 1971; Udo and Uzu, 1972), although Fitter and Sutton (1975) found this correlation only in soils with pH <5. At pH >5 the correlation was with exchangeable calcium. This agrees with the results on pure systems containing exchangeable aluminum, which show that phosphate does react with aluminum held on cation exchange sites. Wild (1950a, 1953) and Thorup and Mehlich (1961) showed that other exchangeable cations were important in affecting phosphate adsorption. The order of decreasing effect was A1 > Ca > Mg > K > Na = N h .

28

R. L. PARFITT

Many uncertainties are associated with this type of work. The phosphate adsorption capacity will vary with shaking time, the indifferent electrolyte, the initial phosphate concentration, and the solid-to-solution ratio for each soil (Rajan and Fox, 1972; Ryden and Syers, 1975b; Hope and Syers, 1976). However, Ryden and Syers (1975b) suggested that ionic strength and different cations affected only the rate at which equilibrium was attained. The phosphate adsorption will also increase with a decrease in pH if sodium or potassium phosphate is used (Obihara and Russel, 1972; Parfitt, 1977), since a lower pH will give the hydrous oxides more positive charge (Hingston et al., 1972; Bowden et al., 1974). Phosphate adsorption on synthetic hydrous oxides such as goethite, alumina, and gibbsite shows that most of the adsorption is complete within several hours. At concentrations of less than 0.005 pmol cm-3 (0.15 pg ~ m - ~ phosphate ), is adsorbed very strongly by surface OH groups to give binuclear or bidentate complexes. It seems likely that the same reaction will occur in soils wherever there are Al.(OH)&O or pairs of surface FeOH separated by about 0.3 nm (Parfitt, 1977; Ryden et al., 1977b). This reaction probably explains the correlation between rapid phosphate adsorption and extractable aluminum and iron in soils. Complete correlation is not possible, since some of the iron and aluminum that is extracted will also be inaccessible to phosphate ions, or in the forms FeOHFe, FeOHFe, and AlOHAl, which do not react with phosphate at low equilibrium concentrations. If crystalline iron oxides are not present, the best measure of the amounts of surface iron and aluminum are probably the methods based on Tamm’s acid oxalate extractant. For soils with large amounts of crystalline iron oxides, dithionite may be a more suitable extractant, although it will give an overestimate of surface aluminum and iron. Taylor and Schwertmann (1974) have shown that hematite and goethite are sinks for phosphate in fermginous soil concretions, and the ratio of P to Fe depends on weathering conditions and mode of genesis. In one Australian soil the sites for anion adsorption were shown to occur mainly on goethite particles (Fordham and Nomsh, 1974). Several workers have investigated phosphate adsorption on soils after extraction of iron and aluminum. The extraction procedure is important because reagents such as oxalate or citrate will block the remaining adsorption sites (Nagarajah et al., 1970). Interpretation of the results is difficult because removal of iron and aluminum sites can also cause dispersion of clay particles, thus giving an increased surface area for phosphate adsorption (Habibullah et al., 1972). Therefore it is not surprising that phosphate adsorption is increased after extraction with some soils and decreased in others (Coleman, 1944, 1945; Russell and Low, 1954; Bromfield, 1964, 1965; Hudcova and Kovarova, 1969; Fox et al., 1971; Galindo et al., 1971; Syerser al., 1971; Habibullahetal., 1972; Moshi et al., 1974). The significant correlations obtained between soil organic matter and phosphate adsorption suggest that some phosphate is adsorbed by the iron or

ANION ADSORPTION BY SOILS

29

aluminum ions, which are also chelated by large organic molecules in soils such as humic acid and fulvic acid (Fokin and Sinkha, 1970; Williams, 1960). Weir and Soper (1963) found that, although phosphate in this form is held against exchange by an anionic resin, part of the phosphate is isotopically exchangeable and available to plants. However, Fox and Kamprath (1971) showed that phosphate is weakly held on organic soils and can be removed by leaching. Thus, phosphate can be adsorbed at different energy levels by ferric or aluminum ions, which are held by organic matter but which are accessible to phosphate in solution. Soil organic matter can also block sites on iron and aluminum hydrous oxides and reduce phosphate adsorption by soil (Hashimoto and Takayama, 1971; Moshi et al., 1974). Attempts to remove organic matter with hydrogen peroxide results in the formation of oxalate, which blocks more sites and further reduces phosphate adsorption (Hudcova and Kavarova, 1969). 2 . Langmuir Isotherms Many workers have determined phosphate adsorption isotherms on soils and then have attempted to fit the results to a Langmuir or Freundlich equation (Fried and Shapiro, 1956; Olsen and Watanabe, 1957; Woodruff and Kamprath, 1965; du Plessis and Burger, 1966; Rennie and McKercher, 1959; Weir, 1972; Karim et al., 1973; Leal and Velloso, 1973; Schwertmann i d Knittel, 1973; Fitter and Sutton, 1975; Ballaux and Peaslee, 1975). Straight lines are obtained when the results from a limited concentration range are plotted according to the Langmuir equation. In some cases the data can best be fitted with two straight lines, and this has been taken to indicate two different phosphate adsorption sites (Shapiro and Fried, 1959; Syers et al., 1973; Karim et al., 1973; Juo and Maduakor, 1974; Rajan and Fox, 1975). Holford et al. (1974) used a Langmuir two-surface equation and obtained quite good agreement with experimental data. In calcareous soils the high-energy phosphate-adsorbing surface was correlated with free iron oxides and the low-energy surface was correlated with organic matter and the surface area of calcium carbonate (Holford and Mattingly, 1975a). Isotherms for the adsorption of phosphate by soils, over a large concentration range, may be described by a series of Langmuir equations. Ryden et al. (1977a,b) used five Langmuir equations, which then were reduced to three equations by successive approximations, thus dividing the isotherms into three regions. The conclusions were similar to those of Muljadi et al. (1966a), who also invoked three types of adsorption region. The nature of adsorption in Regions I and I1 is largely chemical, whereas more physical adsorption may occur in Region 111. It was suggested that OH,+exchanged with phosphate in Region I, and OH exchanged in Region II. However, the results of Rajan (1976) and Parfitt and Atkinson (1976) suggest that both OH 2' and OH participate in an exchange reaction with phosphate in Regions I and 11, with more OH,+being ex-

30

R. L. PARFITT

changed initially. If pH is not controlled, then more OH will be exchanged as the pH increases. Ryden et al. (1977a,b) have suggested that adsorption in Region I11 is more physical than chemical. However, this conclusion was based on Langmuir isotherms of adsorption, kinetics, and charge relationships in situations where pH was not controlled. Since adsorption at constant ionic strength in Region I11 was not completely reversible, this weak adsorption may be due to ligand exchange on a nearly saturated surface where the surface charge is much reduced. In other words, the mechanism of adsorption in all regions or for the whole isotherm may be essentially the same. Nevertheless, phosphate can be readily desorbed from “Region 111,” and this is obviously important for plant growth (Ryden and Syers, 1977). Results with goethite, which has only one site where phosphate adsorption occurs, show that the Langmuir equation does not apply throughout the whole concentration range because the sites are not isolated and the surface charge changes with surface coverage (Atkinson, 1969; Bowden et al., 1974). The equations developed by Bowden et al. (1973, 1977) give much better agreement with the experimental data, since the charges on the surface and on the anion are taken into account. Therefore conclusions, based on Langmuir equations, suggesting that there are two or three sites of phosphate adsorption must be treated with caution. Since the slope of an isotherm is an index of adsorption energy, it can be used to compare the performance of different soils with respect to phosphate adsorption. Bache and Williams (1971) used the Temkin equation, which takes into account the decrease in adsorption energy with surface coverage. The plot of phosphate adsorbed against log (equilibrium concentration) was linear over a larger concentration range as compared with the Langmuir plot. They also found that the slope of this curve at c = lW4 M was correlated with x , which was determined from a single point on the isotherm where 150 mg P was added per 100 g soil. They suggested that this single-point determination could be used as a simple method of describing the phosphate sorption isotherm. Gunary (1970) showed that inclusion of a square-root term in the Freundlich equation gave a better fit with the data, but there was no theoretical basis for this. Very few workers have measured the surface areas of soils used for phosphate adsorption experiments. Habibullah et al. (1972) and Ryden and Syers (1975b) used nitrogen adsorption to determine surface areas, although the area occupied by each phosphate ion was not calculated. Olsen and Watanabe (1957) used ethylene glycol surface areas and found that each phosphate ion occupied 22 n d for an acid soil and 5.2 n d for a calcareous soil. This is a less dense surface coverage compared with one phosphate per 0.66 n d on goethite, 0.22 nrnZ on hematite, 0.33 n d on lepidocrocite, and 0.45 nm2 on Fe(OHh gel for each phosphate ion ( P d i t t et al., 1975). Some tropical volcanic ash soils adsorb phosphate up to 200 pmol g-’ and

ANION ADSORPTION BY SOILS

31

oxisols can adsorb up to 50 pmol g-' (Rajan and Fox, 1972; Fox, 1974; Gebhardt and Coleman, 1974c; Parftt, 1977), which is similar to the amounts adsorbed by synthetic hydroxides. This suggests that soil allophane and soil iron oxides have large surface areas. Phosphate retention on allophane soils increases with the degree of weathering (Saunders, 1965; Fox, 1974), probably because of the increased aluminum content of weathered allophane (Wada and Harward, 1974). Blanchar and Hossner (1969) studied the adsorption of polyphosphates by some corn belt soils. They found that trimetaphosphate was not adsorbed, but tripolyphosphate and pyrophosphate adsorption was higher than orthophosphate adsorption.

3 . Ligand Exchange Reactions Kolthoff (1936) and Kelley and Midgley (1943) suggested that phosphate could exchange with OH- on an edge Al. OH; this type of reaction is referred to as a ligand exchange reaction. Recent evidence for ligand exchange in soils comes from studies of competitive adsorption of anions, adsorption isotherms, and change in adsorption at different pH values (Obihara and Russell, 1972; Rajan and Fox, 1975; Parfitt, 1977). Ligand exchange reactions in soils involve competition between different anions in the soil for adsorption sites (Rajan and Fox, 1975). The most abundant anions naturally present are probably the organic anions, bicarbonate, nitrate, silicate, sulfate, phosphate, and hydroxyl. Rajan and Fox (1975) found that phosphate displaced sulfate and silicate during ligand exchange, but at high phosphate concentrations structural silicate was displaced. Nagarajah et al. (1968, 1970) studied the competitive adsorption and desorption of organic acids and phosphate on gibbsite, goethite, and kaolinite. They found that phosphate adsorption was reduced considerably by polybasic acids, the effect being more marked with the aluminum surfaces. Polygalacturonic acid, a component of root exudates, was also quite effective in reducing phosphate adsorption. Fulvic acid and humic acid react strongly with hydrous oxides (Greenland, 1971; Parfitt ef al., 1977c), and they can reduce phosphate adsorption on soils (Leaver and Russell, 1957; Manojlovic, 1965; Bhat and Bouyer, 1968; Hashimoto and Takayama, 1971; Weir, 1972; Moshi et al., 1974). Hingston et al. (1971) found that selenite and arsenate partly reduced phosphate adsorption on goethite. These and other results lead to the conclusion that, although phosphate is very strongly adsorbed by most soils, it can be partly displaced by the anions Ass-, SeG- HCQ-, OH-, and some polybasic organic anions (Deb and Datta, 1967; LeFleur and Craddock, 1967; Barrow, 1970; Syers et al., 1971; Nagarajah et al., 1968, 1970; Kinjo and Pratt, 1971b; Gebhardt and Coleman, 1974c; Hingston et al., 1974; Lopez-Hernandez, 1974). When some soils are shaken with distilled water some phosphate is desorbed

32

R. L. PARFITT

into solution (White and Beckett, 1964), but when phosphate is added adsorption occurs. Ryden et al. (1972) found that adsorbed phosphate could be desorbed from an A horizon, but it was probably readsorbed in the B horizon. In soils developed on silica sands, phosphate is often lost by leaching, since the phosphate reacts largely with the soil organic matter (Mattingly, 1965; Fox and Kamprath, 1971; Humphreys and Pritchett, 1971; Ballard and Fiskell, 1974). Silicate has been applied to some tropical soils in an attempt both to make adsorbed phosphate more available and to reduce phosphate adsorption (Roy et al., 1971). Obihara and Russell (1972) and Russell (1973) have dealt with this in some detail. They concluded that silicate, which is adsorbed more strongly at high pH, may increase phosphate availability, particularly near pH 7. However, Kafkafi and Giskin (1970) showed that silica was desorbed by soils when phosphate fertilizer was added, which indicates that phosphate is more strongly adsorbed than silicate. Laboratory experiments have shown that sulfate is also desorbed when phosphate is adsorbed onto soils, suggesting that the same sites are active in adsorbing ligands other than phosphate (Rajan and Fox, 1975). Use is made of desorption reactions in chemical analysis of soils for available phosphate. The soils are shaken for short periods with a small volume of extracting solution. Many of the extractants contain an anion that, if present in the correct concentration, can desorb phosphate from soils. Such extractants include 0.5 M sodium bicarbonate, acid fluoride solutions, acetic acid, and citric acid. Evans and Syers (1971) showed that, although citrate and bicarbonate desorbed phosphate from the face of a soil crumb, subsequently some phosphate was redistributed within the crumb. Beckwith (1965) developed a method based on adsorption isotherms that predicted the amount of phosphate fertilizer a soil would require to give an adequate level of phosphate in solution. The phosphate required to give 0.2 pg cmF3 (ppm) in solution after adsorption was assumed to be the amount of phosphate that was required for good plant growth in some Australian soils. Ozanne and Shaw (1967, 1968) have used 0.3 pg cm-3 for pastures in Western Australia. Fox et al. (1974) has found that the equilibrium concentrations required to give 95% of maximum yield were 0.4 pg cm-3 for lettuce, 0.1 pg cm-3 for sweet potato, and 0.06 pg cm-3 for corn in Hawaiian soils. The amount of phosphate required to give these equilibrium concentrations in solution varied greatly, with weathered volcanic ash soils needing very large amounts of phosphate, and alluvial soils needing small amounts (Fox et al., 1968; Fox and Kamprath, 1970). Jones and Benson ( 1975) found that a value of 0.13 p g was required for sweet corn on a high-phosphorus-fixing soil. Singh and Jones (1977) have shown that phosphate desorption increases with temperature in the range 12"30°C, and lettuce required lower concentrations of phosphate in soil solution at higher temperatures.

ANION ADSORPTION BY SOILS

33

Phosphate adsorption decreases as pH increases if NaCl is used as the indifferent electrolyte (Hingston et al., 1972; Obihara and Russell, 1972; Parfitt, 1977). Adsorption can also be reduced by adding lime to acid soils to raise the pH (Woodruff and Kamprath, 1965; Lopez-Hernandez and Burnham, 1974b). However, Reeve and Sumner (1970) and Lucas and Blue (1972), using limed and unlimed soils from the field, showed that liming did not reduce phosphate retention in some tropical soils. Mokwunye (1975) found similar results using buffer solutions at different pH and suggested that hydroxyaluminum material was activated at pH above 5 and provided sites for phosphate adsorption. Recent results indicate that adsorption on goethite is less dependent on pH if CaCI, is used as the electrolyte instead of NaCl, although bridging phosphate complexes are formed in both systems (R. L. Parfitt, unpublished data). The work of White and Taylor (1977) suggests that systems containing aluminum and calcium behave in a more complicated manner. Several workers have noted that, after phosphate is adsorbed on soils, the cation exchange capacity is increased (Mehlich, 1961; Schalscha et al., 1972, 1974b; Mekaru and Uehara, 1972; Sawhney, 1974; Juo and Maduakor, 1974; Ryden and Syers, 1975a, 1976; El-Swaify and Sayegh, 1975). Parfitt and Atkinson (1976) indicated that this was because of phosphate blocking positively charged sites as well as the adsorbed phosphate itself carrying a negative charge at higher pH values. 4 . Slow Reactions of Phosphate in Soil

Evidence from model systems suggests that ligand exchange reactions should occur rapidly between exposed Al*OH and FeeOH groups and phosphate in solution, and indeed there is an initial rapid uptake of phosphate by soils (Low and Black, 1950; Haseman et al., 1950; Hsu, 1964; Evans and Syers, 1971; Vanderdeelen et al., 1973). However, this rapid adsorption is followed by a period when slow adsorption occurs (Haseman et al., 1950; Low and Black, 1950; Hsu, 1964; du Plessis and Burger, 1966). Russell (1973) and Kuo and Lotse (1974) indicated that the reaction was a diffusion-controlled process. Phosphate that is added to soil is initially exchangeable with 32P-labeledphosphate solutions, indicating that all the phosphate is exposed. With time the amount drops, until about 40% remains exchangeable (Talibudeen, 1958; Mattingly and Talibudeen, 1961; Johnston and Poulton, 1977), which suggests that some of the phosphate is no longer exposed and possibly is held within the precipitates. Larsen et al. (1965) showed that half the phosphate that was applied as fertilizer became nonlabile within one to three years on most British soils. Munns and Fox (1976) found that, after 50-200 days, 30-50% of added phosphate remained labile in tropical soils and thus should be available for plant growth.

34

R. L. PARFITT

This slow reaction may be due to the precipitation of phosphates (Chen et al., 1973b; van Riemsdijk et al., 1975, 1977), or to penetration of the surface by phosphate ions (Holford and Mattingly, 1976), or to diffusion into pores. It is unlikely that variscite (AlP04.2H20)and strengite (FePO4.2H2O) are present in soils (Ryden et al., 1973), but at high phosphate concentrations and at low pH, clays react to form taranakite, (NH4,K)3A15H,(P04)8* 18H20 (Kittrick and Jackson, 1954, 1955). Although these conditions do prevail close to phosphate fertilizer granules, taranakite has been found only in soils treated with saturated fertilizer solutions. Bell and Black (1970) have listed other crystalline phosphates that have been identified in soils under these conditions. However, Norrish (1968) and Adams et al. (1973) have identified the plumbogummite minerals, gorceixite [BaA13(P04),(OH)5H20] and crandallite [CaA13(P04)2(0H)5 H,O], in soils and have suggested that they can be formed as a soil develops. Sawhney (1973) found some silt-size grains in soils that contained phosphate together with Al, Fe, Si, and some Ca. Barrow (1973a, 1974a,b,c) and Barrow and Shaw (1974, 1975a,b) studied the slow reaction between phosphate and soils and found that the rate was temperature-dependent but was not greatly affected by differences between soils or by a range of water contents. This suggested that the reaction through solution was not rate-limiting or, possibly, was not involved at all. The proportion of phosphate that was immobilized by the slow reaction as measured by arsenate displacement, plant uptake, and isotopic exchange was independent of the level of application. Much of the phosphate blocked the initial adsorption sites but in a form not readily exchangeable with labeled phosphate. It was suggested that the slow reaction was due to phosphate changing from a monodentate form to a bridging form. This conclusion is not consistent with the observations that pure iron oxides rapidly form the bridging complex, but the postulated reaction may occur with some aluminum hydroxide surfaces (Kafkafi et al., 1967). Several authors have used Chang and Jackson’s (1957) method in an attempt to follow the reactions of phosphate with time, and results suggest that phosphate that is initially “Al-bound” (NaF-extractable P) migrates to the “Fe-bound” fraction (NaOH-extractable P) (e.g., Hubbard and Walmsley, 1974; Smith, 1965). For calcareous soils Probert and Larsen (1972) suggested that the slow reaction involved a crystallization or recrystallization reaction. B. ARSENATE

The arsenate ion and the phosphate ion are chemically alike; thus, the adsorption behavior of arsenate on hydrous oxides is similar to phosphate adsorption (Hingston et al., 1968a, 1971).

ANION ADSORPTION BY SOILS

35

Fordham and Nomsh (1974) showed that arsenate and phosphate were both retained in a Western Australian soil by goethite particles rather than by iron in a more dispersed form. Several workers using less direct methods have suggested that arsenate adsorption by soils is controlled largely by the hydrous oxides of iron and aluminum (Holobrady et al., 1969; Holobrady and Galba 1970; Jacobs et al., 1970). Galba (1972) showed that arsenate adsorption decreased with pH, and Woolson et al. (1973) found that arsenate could be desorbed from soils by leaching with phosphate, which indicates that arsenate, like phosphate, is adsorbed in soils by a ligand exchange mechanism.

C. MOLYBDATE

Molybdate is adsorbed on goethite and gibbsite by a ligand exchange reaction (Hingston et al., 1972), which suggests that molybdate will react with exposed FeOH and AlOH groups. In soils, adsorption increases from low values at pH to a maximum at pH 4 (Jones, 1957; Reisenauer et al., 1962; Catani et al., 1970), and adsorbed molybdate can be released after treatment with dithionite or oxalate (Jones, 1956, 1957; Reisenauer et al., 1962; Trobisch and Schilling, 1963; Smith and Leeper, 1969; Cheng and Ouellette, 1973), which is consistent with ligand exchange on iron and aluminum surfaces. Similar results have been obtained with volcanic ash soils (Theng, 1971; Gonzalez et al., 1974). Barrow (1970, 1972) determined adsorption isotherms for molybdate on soils and found that molybdate adsorption on different soils paralleled phosphate and sulfate adsorption on the same soils. The adsorption of molybdate by soils is similar to the adsorption of phosphate in many respects. Initially the molybdate is rapidly adsorbed from solution, but with time a slow reaction takes place independent of the water content of the soil. The product of this reaction cannot be displaced with hydroxide solutions (Smith and Leeper, 1969; Barrow, 1973b; Barrow and Shaw, 1974); thus, the slow reaction may be due to reorganization of molybdate on surfaces or to polymerization of molybdate, which normally occurs at low pH. Molybdate can be desorbed from soils by phosphate or sulfate (Stout et al., 1951; Barrow, 1973b). Desorption with phosphate increased with pH. Phosphate was more effective than hydroxide at pH 7, but at pH above 9 hydroxide alone was nearly as efficient as phosphate (Barrow, 1973b). Phosphate also reduced molybdate adsorption from solution, but sulfate had no effect (Gorlach et al., 1969). The effects with phosphate decreased with time, which shows that molybdate is more strongly adsorbed after initial adsorption.

36

R. L. PARFI’IT

D. SELENITE The selenite (Se03*-’ anion is more stable in soils than selenate (Se042-), which is rapidly leached or reduced to selenite. Selenite is strongly adsorbed by ligand exchange on goethite (Hingston et al., 1968b, 1971, 1974), where it probably forms a bridging binuclear complex (Parfitt and Russell, 1977; Parfitt and Smart, 1977). Cary et al. (1967) also found that selenium is immobilized by sesquioxides in acid soils and later showed that selenium concentration in soil solution is governed primarily by a femc oxide-selenite adsorption complex, which forms rapidly when selenite is added to soils (Geering et al., 1968; Cary and Allaway, 1969). However, Levesque (1974a,b) found that selenite was also associated with aluminum and organic matter in Canadian podzols, and Jones and Belling (1967) showed that selenite was retained by calcareous soils. Brown and Carter (1969) found that selenite leaching was increased by additions of sulfate, suggesting that both ions are adsorbed on the same sites. Selenite adsorption by New Zealand soils was related to the degree of weathering and the allophane content of these soils (John et al., 1976).

E. SULFATE

Reviews by Freney ef al. (1962) and Harward and Reisenauer (1966) have included sections on the adsorption of sulfate by soils. Many soils retain sulfate, particularly soils with large amounts of hydrous oxides of iron and aluminum. Thus, weathered tropical soils and volcanic ash soils retain sulfate strongly. Adsorption isotherms for sulfate adsorption on soils have been determined by Chao et al. (1962), Hasan et al. (1970), Barrow (1972), Haque and Walmsley (1973), and others. At low solution concentration, the isotherms have been described by the Langmuir or Freundlich equations (Harward and Reisenauer, 1966; Bornemisza and Llanos, 1967; Hasan et al., 1970). Hingston et al. (1972) showed that sulfate adsorption on goethite and gibbsite decreased with increase in pH up to 8, beyond which no adsorption occurred; similar results are found for soils (Harward and Reisenauer, 1966; Gebhardt and Coleman, 1974b; Scott, 1976). Haque and Walmsley (1974a) and Barrow (1967) have shown that sulfate adsorption is correlated with extractable aluminum rather than extractable iron, although both iron oxide and hydrous aluminum surfaces strongly adsorb sulfate (Aylmore et al., 1967). Scott (1976) suggested that sulfate adsorption at low levels depended on active iron rather than active aluminum in Scottish soils, but aluminum was more important near to the saturation level. Sanders and Tinker

ANION ADSORPTION BY SOILS

37

(1975) suggested that hematite was responsible for sulfate adsorption in an Oxford soil. Volcanic ash soils usually adsorb considerable amounts of sulfate, probably because of the presence of allophane and other hydrous oxides (Ayers and Hagihara, 1953; Fox et al., 1971; Mekaru, 1969; Haque and Walmsley, 1973, 1974b; Gebhardt and Coleman, 1974b). However, Hogg and Toxopeus (1966) and Fox (1974) have shown that younger allophane soils retain little sulfate against leaching, whereas the older allophane soils retain sulfate strongly. This suggests that either there are additional sites in older soils owing to the increased aluminum levels, or the sites are more accessible. Losses of sulfate by leaching have been reported by a number of investigations, which were reviewed by Harward and Reisenauer (1966). Leaching is more significant in soils that are low in hydrous oxides of iron and aluminum, particularly in A horizons. Swoboda and Thomas (1965) showed that sulfate is leached even in red-yellow podzolic soils, which have significant amounts of iron oxides, if large volumes of water are used. Leaching also can occur if positive sites are blocked by organic ligands (for example, in highly organic soils), since the sulfate has a lower binding constant than polycarboxylic acids (Haque and Walmsley, 1974b). Thus, Gillman (1974) found more phosphateextractable sulfate in lower horizons where the pH of zero charge was higher and where there were more positive sites. Harward and Reisenaur (1966) have reviewed the papers dealing with mechanism of adsorption. The most likely mechanism of ligand exchange is the replacement of M OH: or M * OH groups by sulfate ions, and Bornemesza and Llanos (1967) have shown that OH ions are released during sulfate adsorption. P d i t t and Russell (1977) and P d i t t and Smart (1977) showed that sulfate is adsorbed as the binuclear bridging complex Fe*OS(OO)O*Feon goethite, and recent work shows that the same complex is formed on all iron oxides (Parfitt and Smart, 1978). The data of Gallez et al. (1976), which showed that the pH of zero charge for soils shifts to higher pH when sulfate is adsorbed, are consistent with the formation of a binuclear bridging complex. The ligand exchange mechanism accounts for the rapid reaction of sulfate with soils. This may be followed by a slow reaction, which Chang and Thomas (1963) suggested was due to rupture of bridging A1 * OH A1 and A1 * 0 A1 groups followed by adsorption. Sulfate is adsorbed by soils less strongly than phosphate (Hasan et al., 1970; Haque and Walmsley, 1973), and phosphate solutions are used to extract sulfate in soil tests for sulfur (Chaoer al., 1962; Fox et al., 1964; Barrow, 1967; Peverill et al., 1975). It is likely that the same sites are involved in adsorption in soils (Scott, 1976) as has been shown for goethite ( P d itt and Russell, 1977). The order of adsorption for different anions is phosphate > molybdate > sulfate >

-

-

R. L. PARFITT

38

chloride > nitrate (Ayers and Hagihara, 1953; Fieldes and Schofield, 1960; Singh and Kanehiro, 1969; Kinjo and Pratt, 1971b; Barrow, 1972; Gebhardt and Coleman, 1974b).

F. BORIC ACID Boron is probably present in soil solution as boric acid, H3BG, a weak monobasic acid, which acts not as a proton donor but as a Lewis acid, which accepts OH. B(OH),

+ H20= B(OH);

t H+

pK

=

9.0

Boric acid has been shown to react with goethite, possibly by accepting OH from FeOH groups (Parfitt and Russell, 1977). At higher concentrations boric acid fmns polymers, and the acidity increases. 3B(OHh = B&(OH)L

+ H+ + 2 & 0

pK = 6.84

Illite adsorbs more boron than kaolinite or montmorillonite clays (Fleet, 1965; Hingston, 1964), and Couch and Grim (1968) suggested that B(0H); was held at the edges of illite crystals, while some boron slowly diffused into the tetrahedral sites. Maximum adsorption on soils and soil materials is observed at pH 9 close to the pK as predicted by Hingston ef af. (1972) for ligand exchange, which suggests that boron adsorption is similar to a ligand exchange reaction (Hingston, 1964; Sims and Bingham, 1967, 1968a,b; Okazaki and Chao, 1968; Bingham et af., 1971; Metwally ef af., 1974). This is consistent with the observation that hydrous oxides of iron and aluminum adsorb boric acid (Sims and Bingham, 1968a; McPhail et af., 1972; Metwally ef af., 1974; El-Damaty et af., 1974). Other workers have shown that boric acid adsorption is correlated with extractable aluminum (Harada and Tamai, 1968; Hatcher ef af., 1967) and organic matter (Gupta, 1968). Russell (1973) suggested that boric acid is also held by humic colloids in soils, since carboxylic acids can condense with boric acid. This may explain the correlation of adsorption with organic matter content. Volcanic ash soils adsorbed large amounts of boric acid; the adsorption was correlated with allophane but not with free iron oxides or organic matter (Schalscha ef al., 1973). Boron adsorption follows a Langmuir isotherm over a limited concentration range (Hatcher and Bower, 1958; Biggar and Fireman, 1960; Hingston, 1964; Singh, 1964; Okazaki and Chao, 1968; Bingham et al., 1971; El-Damaty et al., 1974); Hatcher and Bower (1958) and Singh (1964) suggested that multisite adsorption was occurring.

ANION ADSORPTION BY SOILS

39

In a study of the desorption of boron from soil, Griffin and Burau (1974) concluded that boron was held on magnesium sites as well as on hydroxyiron and hydroxyaluminum surfaces. Rhoades et al. (1970) showed that boron is adsorbed by hydroxymagnesium [Mg(OHk] clusters; they suggested that these clusters are important in controlling boron adsorption in arid soils. Leaching experiments suggest that some boron is dissolved from soils, but part of the boron remains even after prolonged leaching (Reeve et al., 1955; Rhoades et al., 1970). G . SILICIC ACID

Silicon is present in soil solution as silicic acid, Si(OH),. The solubility of silicic acid in pure systems is constant in the pH range 2-9, but in soils it decreases with increase in pH (Russell, 1973). Silicic acid is known to be adsorbed in certain soils by hydrous iron and aluminum oxides (Beckwith and Reeve, 1963, 1964; McKeague and Cline, 1963a,b; Jones and Handreck, 1965, 1967; Wada and Inoue, 1974). Adsorption increased with>pHup to 9, which equals the pK for silicic acid dissociation: Si(OH), = H3SiOc

+ H+

Thus, the amount of silicic acid in soil solution can be explained by adsorption on iron and aluminum surfaces (Miller, 1967;McKeague and Cline, 1963a;Beckwith and Reeve, 1964). Maximum adsorption in soils occurred at pH 9 (McKeague and Cline, 1963b; Obihara and Russell, 1972), which suggested that ligand exchange reactions were involved. Obihara and Russell (1972) found that silicate adsorption followed the Langmuir equation, while Wada and Inoue (1974), for volcanic ash soils, used a Freundlich equation at higher silicate concentrations. Silicate adsorption is decreased by the presence of phosphate (Ohihara and Russell, 1972; Kafkafi and Giskin, 1970) and by humus (Wada and Inoue, 1974), which suggests that the same sites are active in adsorption. H. FLUORIDE

The fluoride ion reacts with goethite by ligand exchange with the onecoordinated OH group (Hingston et al., 1972, 1974; Parfitt et al., 1976; Parfitt and Russell, 1977). With gibbsite a large number of OH groups are replaced, suggesting that A1 * OH * A1 as well as A1 * OH groups can exchange with fluoride. Bower and Hatcher (1967) showed that fluoride adsorption followed a Langmuir equation and was accompanied by release of OH. Gibbsite, [Al(OH)J, halloysite, and kaolinite adsorbed more fluoride than goethite, montmorillonite, and vermiculite.

40

R. L. P M l T

Fieldes and Perrott (1966) used the release of OH ions by fluoride as a field test for allophane, but Brydon and Day (1970) showed that soils containing aluminum soluble in Tamm’s acid oxalate solution also reacted in the same way. Perrott et al. (1976a) developed a laboratory method whereby OH released by fluoride could be used as an indicator of the amount of disordered material in subsoils.

I. HALIDES

Chloride adsorption has been used to measure the positive charge of soils (Schofield, 1949). Gebhardt and Coleman (1974a) found that andepts adsorbed up to 6 meq Cl- per 100 g at pH 6 and up to 32 meq per 100 g at pH 3.8. Adsorbed Cl- was exchangeable with NQ- and could be desorbed by washing with water. Smith and Davis (1974) found that bromide was adsorbed in only one of the soils studied; the other soils exhibited anion exclusion properties with bromide. Iodide is adsorbed by soils as well as by iron and aluminum hydroxides (Whitehead, 1973, 1974; Seleznev and Tyuryukanov, 1970). Adsorption increased with concentration until a plateau was reached in the isotherm. Maximum adsorption occurred at low pH. The halides can be adsorbed in small amounts on goethite by ligand exchange (Parfitt and Russell, 1977), but in soils they are probably adsorbed by electrostatic attraction to M*OHZ sites, which occur at low pH.

J . NITRATE

Nitrate is weakly adsorbed on goethite and gibbsite by electrostatic attraction (Hingston et al., 1972), but ligand exchange does occur in evacuated systems at low pH (Parfiitt and Russell, 1977). In most cases nitrate is leached quite readily from soils (e.g., Smith and Davis, 1974) and is held more weakly than chloride, sulfate, or phosphate (Kinjo and Pratt, 1971a,b; Singh and Kanehiro, 1969). However, soils that have positive sites are able to prwent rapid leaching of nitrate (van Raij and Camargo, 1974; Wild, 1972; Jones, 1975; B!ack and Waring, 1976). Volcanic ash soils retain nitrate more strongly than other soils presumably because of the presence of many positive sites on allophane (Singh and Kanehiro, 1969; Kinjo et af ., 1971; Schalscha et al., 1974a; Espinoza et af., 1975). Kinjo and Pratt (1971a) found that adsorption followed the Langmuir isotherm and increased with decreasing pH to pH 3.5.

ANION ADSORPTION BY SOILS

41

VII. Summary and Conclusions

The literature covering anion adsorption by soils and soil materials leads to the following conclusions: (1) Surface Al. OH and FeaOH groups are the important sites for the adsorption of anions. The amount of adsorption is controlled by the number of these sites that are exposed at surfaces, and therefore soils that contain large amounts of high-surface-area hydrous iron and aluminum oxides will be extremely efficient in adsorbing anions. (2) Anion adsorption involves an electrostatic interaction as well as some chemical interaction between the surface and the ion. The Langmuir model is incomplete in describing this adsorption, because it takes no account of charge. The adsorption of anions is dependent on pH, with maximum adsorption usually occumng for fully dissociated ions at low pH where the surface becomes positively charged, owing to protonation of surface M.OH groups. Maximum adsorption of anions of incompletely dissociated acids occurs at a pH value close to the pK of the acid. (3) The order of adsorption by a soil is probably phosphate > arsenate > selenite = molybdate > sulfate = fluoride > chloride > nitrate. The more strongly adsorbed ions will react with M * OH and M *OHgroups in a ligand exchange reaction where the anion becomes coordinated to the metal ion. For phosphate and sulfate it is likely that binuclear bridging complexes [Fe-OP(O0)O-Feand Fe*OS(OO)O.Fe] are formed on iron oxide surfaces. (4) Anion adsorption reactions in soil are complicated by competition for adsorption sites from other anions, including carboxylates, and also by the presence of cations such as calcium and aluminum. These reactions require further study under controlled conditions if anion adsorption in soils is to be more fully understood. It has become clear that there are many similarities between the adsorption reactions of different anions, and results obtained with one anion are an indication of what may happen with another anion. It is hoped that the ideas and conclusions that have emerged will lead to a better understanding of the factors controlling anion availability in soils.

ACKNOWLEDGMENTS I am grateful to Drs. R. J . Atkinson, G.J. Churchman, R. J . Furkert, and B . K. Theng and to Mr. A. J . Metson for helpful criticism and advice in the preparation of this manuscript.

42

R. L. PARFITT REFE!REN CE S

Adams, J. A., Howarth, D. T., and Campbell, A. S. 1973. J. Soil Sci. 24, 215-223. Aleksandrova, L. N. 1954. Pochvovodenie 1, 14-29. Aivarez. R.. Cramer, R. E.. and Silva, J. A. 1976. Soil Sci. SOC.Am. J . 40, 317-319. Amer, F., and Ramy, A. 1971. J. Soil Sci. 22, 267-274. Anderson, G., Williams, E. G., and Moir, J. 0. 1974. J . Soil Sci. 25, 51-62. Anderson, M. A., Ferguson, J. F., and Gavis, J. 1976. J. Colloid Interface Sci. 54, 391-399. Appelt, H., Coleman, N. T., and Pratt, P. F. 1975a. Soil Sci. SOC.Am., Proc. 39, 623627. Appelt, H., Coleman, N. T., and Pratt, P. F. 1975b. Soil Sci. SOC.Am., Proc. 39, 628-630. Atkinson, R. J. 1%9. Ph.D. Thesis, University of Western Australia, Perth. Atkinson,, R. J., Posner, A. M., and Quirk, J. P. 1967. J. Phys. Chem. 71, 550-558. Atkinson, R. J . , Posner, A. M., and Quirk, J. P. 1972. J. Inorg. Nucl. Chem. 34, 2201-221 1. Atkinson, R. J., Parfitt, R. L., and Smart, R.St.C. 1974. J. Chem. Soc., Faraday Trans. I 70, 1472-1479. Ayers, A. S., and Hagihara, H. H. 1953. SoilSci. 75, 1-17. Aylmore, L. A. G., Karim, M., and Quirk, J. P. 1967. SoilSci. 103, 10-15. Bache, B. W. 1963. J. Soil Sci. 14, 113-123. Bache, B. W. 1964. J. Soil Sci. 15, 110-116. Bache, B. W., and Williams, E. G. 1971. J. SoilSci. 22, 289-301. Ballard, R., and Fiskell, J. G. A. 1974. Soil Sci. SOC.Am., Proc. 38, 250-255. Ballaux, J . C., and Peaslee, D. E. 1975. Soil Sci. SOC.Am., Proc. 39, 275-278. Barrow, N. J . 1967. SoilSci. 104, 342-349. Barrow, N. J . 1970. SoilSci. 109, 282-288. Barrow, N. J. 1972. Soil Sci. 113, 175-180. Barrow, N. J . 1973a. Aust. J . Soil Res. 11, 57-63. Barrow, N. J . 1973b. SoilSci. 116, 423-431. Barrow, N. J . 1974a. SoilSci. 117, 28-33. Barrow, N. J. 1974b. Soil Sci. 118. 82-89. Barrow, N . 1. 1974c. Soil Sci. 118, 380-386. Barrow, N. J., and Shaw, T. C. 1974. Commun. Soil Sci. Plant Anal. 5, 355-364. Barrow, N. J . , and Shaw, T. C. 1975a. SoilSci. 119, 167-177. Barrow, N. J . , and Shaw, T. C. 1975b. SoilSci. 119, 190-197. Bar-Yosef, B., Kafkaf, U., and Lahav, N. 1969. Soil Sci. SOC.Am., Proc. 33, 672-677. Beckwith, R. S. 1965. Aust. J . Exp. Agric. Anim. Husb. 5, 52-58. Beckwith, R. S., and Reeve, R. 1963. Aust. J . Soil Res. 1, 157-168. Beckwith, R. S., and Reeve, R. 1964. Aust. J. Soil Res. 2, 33-45. Bell, L. C., and Black, C. A. 1970. Soil Sci. SOC.Am., Proc. 34, 735-740. Bhat, K. K. S., and Bouyer, S. 1968. I n “Isotopes and Radiation in Soil Organic Matter Studies,” pp. 299-313. IAEA, Vienna. Biggar, J. W., and Fireman, M. 1960. Soil Sci. SOC.Am., Proc. 24, 1 15-120. Bingham, F. T . , Page, A. L., Coleman, N. T., and Flach, K . 1971. Soil Sci. SOC. Am., Proc. 35, 546-550. Black, A. S., and Waring, S. A. 1976. Aust. J. Soil Res. 14, 181-196. Blanchar, R. W., and Hossner, L. R. 1969. Soil Sci. SOC.Am., Proc. 33, 622-625. Bohn, H. L., and Peech, M. 1969. Soil Sci. SOC.Am., Proc. 33, 873-876. Bolland, M. D. A., Posner, A. M., and Quirk, J. P. 1976. Aust. J. Soil Res. 14, 197-216. Bornemisza, E., and Llanos, R. 1967. Soil Sci. SOC.Am., Proc. 31, 356-360. Bowden, J . W., Bolland, M. D. A., Posner, A. M., and Quirk, J. P. 1973. Nature (London) Phys. Sci. 245, 81-82.

ANION ADSORPTION BY SOILS

43

Bowden, J. W., Posner, A. M., and Quirk, J. P. 1974. Trans. Inr. Congr. Soil Sci.. lOrh, 1974 Vol. 11, pp. 29-36. Bowden, J. W., Posner, A. M., and Quirk, J. P. 1977. Ausr. J . Soil Res. 15, 121-136. Bower, C. A., and Hatcher, J . T. 1967. Soil Sci. 103, 151-154. Bragg, W. L., and Claringbull, G. F. 1965. “The Crystalline State,” Vol IV, p. 118. Bell, London. Breeuwsma, A,, and Lyklema, J. 1971. Discuss. Faraday Soc. 52, 324-333. Breeuwsma, A , , and Lyklema, J. 1973. J . Colloid Inrerface Sci. 43, 437448. Bromfield, S. M. 1964. Narure (London) 201, 321-322. Bromfield, S. M. 1965. Ausr. J . Soil Res. 3, 31-49. Bromfield, S. M. 1967. Ausr. J . Soil Res. 5, 225-234. Bromfield, S. M. 1970. Soil Sci. 109, 388-390. Brown, G., and Newmann, A. C. D. 1973. J. Soil Sci. 24, 339-353. Brown, M. J . , and Carter, D. L. 1969. Soil Sci. Soc. Am., Proc. 33, 563-565. Brydon, J. E., and Day, J. H. 1970. Can. J . Soil Sci. 50, 35-41. Cary, E. E., and Allaway, W. H. 1969. Soil Sci. SOC. Am., Proc. 33, 571-574. Cary, E. E., Wieczorek, G. A., and Allaway, W. H. 1967. Soil Sci. Soc. Am., Proc. 31, 21-26. Catani, R. A., Alcarde, J. C., and Furlani, P. R. 1970. An. Esc. Super. Agric. “Luiz de Queiroc” Univ. Sad Paulo 27, 223-233. Chang, M. L., and Thomas, G. W. 1963. Soil Sci. SOC. Am., Proc. 27, 281-283. Chang, S. C., and Jackson, M. L. 1957. SoilSci. 84, 133-144. Chao, T. T. Hanvard, M. E., and Fang, S. C. 1962. Soil Sci. SOC. Am., Proc. 26, 234-237. Chen, R. Y . S., Butler, J. N., and Stumm, W. 1973a. J . Colloid Inrerjke Sci. 43, 421-4136, Chen, R. Y . S . , Butler, J. N., and Stumm, W. 1973b. Environ. Sci. Technol. 7, 327-332. Chenge, B. T., and Ouellette, G. J. 1973. Soils Ferr. 36, 207-215. Cloos, P. A., Herbillion, A., and Echeverria, J. 1968. Trans. Inr. Congr. Soil Sci., 9rh, 1968 Vol. 11, pp. 733-743. Cole, C. V., Olsen, S. R., and Scott, C. 0. 1953. Soil Sci. SOC. Am., Proc. 17,352-356. Coleman, N. T., Thorup, J . T., and Jackson, W. A. 1960. Soil Sci. 90, 1-7. Coleman, R. 1944. Soil Sci. 58, 71-77. Coleman, R. 1945. Soil Sci. Soc. Am., Proc. 9, 72-75. Colombera, P. M., Posner, A. M., and Quirk, J. P. 1971. J. Soil Sci. 22, 119-128. Couch, E. L., and Grim, R. E. 1968. Clays Clay Miner. 16, 249-255. Coulter, B. S. 1969. Soils F e n . 32, 215-223. Cradwick, P. D. G., Farmer, V. C., Russell, J. D., Masson, C. R., Wada, K., and Yoshinaga, N. 1972. Nature (London), Phys. Sci. 240, 187-189. Daly, B. K.,and Binnie, H. J. 1974. Commun. Soil Sci. Plant Anal. 5, 507-514. De, S. K . 1961. Kolloid-2. 179, 134-140. Dean, L. A. 1949. Adv. Agron. 1, 391-411. Deb, D. L., and Datta, N. P. 1967. Plant Soil 26, 432-444. Deshpande, J. L., Greenland. D. J., and Quirk, J. P. 1964. Trans. Inr. Congr. SoilSci., Bth, I964 Vol. 111, pp. 1213-1225. Deshpande, J. L., Greenland, D. J., and Quirk, J. P. 1968. J. Soil Sci. 19, 108-122. du Plessis, S. F., and Burger, R. du. T. 1966. S. Afr. J . Agric. Sci. 9, 117-126. Edzwald, J. K.,Toensing, D. C., and Leung, M.C.-Y. 1976. Environ. Sci. Technol. 10, 485-490. El-Damaty, A. H., Metwally, A. L., and Yousry, M. 1974. Agrokem. Talajtan 23, 71-82. El-Swaify, A,, and Sayegh, A. H. 1975. Soil Sci. 120, 49-56. Espinoza, W., Gast, R. G., and Adams, R. S.,Jr. 1975. Soil Sci. Soc. Am., Proc., 39, 842-846. Evans, J., and Smillie, G. W. 1976. Ir. J. Agric. Res. 15, 65-73. Evans, T. D., and Syers, I . K. 1971. Soil Sci. SOC. Am., Proc. 35, 906-909. Fassbender, H. W . 1969. Turrialba 19, 497-505.

44

R.

L. PARFITT

Fieldes, M., and Perrott, K. W. 1966. N.Z. J . Sci. 9, 623-629. Fieldes, M., and Schofield, R. K. 1960. N.Z. J . Sci. 3, 563-579. Fitter, A. H., and Sutton, C. D. 1975. J . Soil Sci. 26, 241-246. Fleet, M. E. L. 1965. Clay Miner. Bull. 6, 3-16. Fokin, A. D., and Sinkha, M. K. 1970. Izv. Tirniryazevsk. S-kh. Akad. 2, 149-153. Fordham, A. W., and Nonish, K. 1974. Ausr. J. SoilRes. 12, 165-172. Fox, R. L. 1974. Trop. Agric. 51, 200-210. Fox, R. L., and Kamprath, E. J. 1970. Soil Sci. SOC.Am., Proc. 34, 902-907. Fox, R. L., and Kamprath, E. J. 1971. Soil Sci. SOC.Am., Proc. 35, 154-156. Fox, R. L., Olsen, R. A., and Rhodes, J. F. 1964. Soil Sci. Soc. Am., Proc. 28, 243-246. Fox, R. L., Plucknett, D. L., and Whitney, A. S. 1968. Trans. In!. Congr. Soil Sci. 9rh. 1968 Vol. 11, pp. 301-310. Fox, R. L., Hasan, S. M., and Jones, R. C. 1971. Int. Symp. SoilFertil. Eval., Proc., 1971 Vol. 1, pp. 857-864. Fox, R. L., Nishimoto, R. K., Thompson, J. R., and de la Pena, R. S. 1974. Trans. Inr. Congr. Soil Sci., IOrh, 1974 Vol. 4 , pp. 232-236. Franklin, W. T., and Reisenauer, H. M. 1960. Soil Sci. 90, 192-200. Freney, J. R., Barrow, N. J., and Spencer, K. 1962. Planr Soil 17, 295-308. Fried, M., and Shapiro, R. E. 1956. Soil Sci. SOC.Am., Proc. 20, 471-475. Frost, R. R., and Griffin, R. A. 1977. Soil Sci. Soc. Am. J . 41, 53-57. Galba, J. 1972. Pol’nohospodarsmo 18, 1055-1061. Galindo, G. G., Olguin, C., and Schalscha, E. B. 1971. Geoderma 7, 225-232. Gallagher, K . J. 1970. Nature (London) 226, 1225-1227. Gallez, A., Juo, A. S. R., and Herbillon, A. J. 1976. Soil Sci. SOC.Am. J . 40, 601-608. Gebhardt, H., and Coleman, N. T. 1974a. Soil Sci. Soc. Am., Proc. 38, 255-259. Gebhardt, H., and Coleman, N. T. 1974b. Soil Sci. Soc. Am., Proc. 38, 259-262. Gebhardt, H., and Coleman, N. T. 1974c. Soil Sci. Soc. Am., Proc. 38, 263-265. Geering, H. R., Cary, E. E., Jones, L. H. P., and Allaway, W. H. 1968. Soil Sci. Soc. Am., Proc. 32, 3 5 4 0 . Ghosh, J. C., and Battacharyya, P. B. 1930. Soil Sci. 26, 31 1-322. Giles, C. H., MacEwan, T. H., Nakhwa, S. N., and Smith, D. 1960.J. Chem. Soc. pp. 3973-3993. Gillman, G. P. 1974. Aust. J. Soil Res. 12, 173-176. Gonzalez, R . B., Appelt, H., Schalscha. E. B., and Bingham, F. T. 1974. SoilSci. SOC.Am., Proc. 38, 903-906. Gorlach, E., Gorlach. K., and Compata, A. 1969. Agrochimica 8, 506-512. Graham, D. 1953. J. Phys. Chem. 57, 665-669. Greenland, D. J. 1965. Soils Fert. 28, 415-425. Greenland, D. J . 1971. Soil Sci. 111, 34-41. Griffin, R. A., and Burau, R. G. 1974. Soil Sci. Soc. Am., Proc. 38, 892-896. Griffin, R. A., and Jurinak, J. J. 1973. SoilSci. Soc. Am., Proc. 37, 847-850. Griffin, R. A., and Jurinak, J. J. 1974. Soil Sci. SOC.Am.. Proc. 38, 75-79. Gunary, D. 1970. J. Soil Sci. 21, 72-77. Gupta, U. C. 1968. Soil Sci. Soc. Am., Proc. 32, 45-48. Habibullah, A. K. M., Lewis, D. G., and Greenland, D. J. 1972. Trans. Commun. V and VI Inr. SOC. Soil Sci. pp. 81-92. Hair, M. L. 1967. “Infrared Spectroscopy in Surface Chemistry.” Arnold, London. Hall, J. K., and Baker, D. E. 1971. Soil Sci. Soc. Am.. Proc. 35, 876-881. Haque, I., and Walmsley, D. 1973. Geoderma 9, 269-278. Haque, I . , and Walmsley, D. 1974a. Trop. Agric. 51, 253-263. Haque, I . , and Walmsley, D. 1974b. Planr Soil 40, 145-152. Harada, T., and Tamai, M. 1968. Soil Sci. Planr Nurr. (Tokyo) 14, 215-224.

ANION ADSORPTION BY SOILS

45

Harter, R. D. 1969. Soil Sci. Soc. Am. Proc. 33, 630-634. Hanvard, M. E., and Reisenauer, H. M. 1966. Soil Sci. 101, 326-335. Hasan, K. A,, and Pollard, A. G. 1966. Pak. J . Soil Sci. 2, 1-9. Hasan, S. M., Fox, R. L., and Boyd, C. C. 1970. Soil Sci. Soc. Am., Proc. 34, 897-901. Haseman, J . F., Brown, E. H., and Whitt, C. D. 1950. Soil Sci. 70, 257-271. Hashimoto, Y., and Takayama, H. 1971. J . Sci. Soil Manure 42, 3 7 4 3 . Hatcher, J. T., and Bower, C. A. 1958. Soil Sci. 85, 319-323. Hatcher, J. T., Bower, C. A., and Clarke, Id. 1967. Soil Sci. 104, 422426. Helyar, K. R., Munns, D. N., and Burau, R. G . 1976a. J . Soil Sci. 27, 307-314. Helyar, K. R., Munns, D. N., and Burau, R. G. 1976b. J . Soil Sci. 27, 315-323. Hemwall, J. B. 1957a. Adv. Agron. 9, 95-112. Hemwell, J . B. 1957b. Soil Sci. 83, 101-108. Hingston, F. J. 1964. Aust. J. Soil Res. 2, 83-95. Hingston, J . F., and Raupach, M. 1967. Aust. J . Soil Res. 5 , 295-309. Hingston, F. J., Posner, A. M., and Quirk, J. P. 1968a. Adv. Chem. Ser. 70, 82-90. Hingston, F. J.. Atkinson. R. J., Posner, A. M.. and Quirk, J . P. 1968b. Trans. Congr. SoilSci. 9th, 1968 Vol. I , pp. 669-678. Hingston, F. J., Posner, A. M., and Quirk, J. P. 1971. Discuss. Faraday Soc. 52, 334-342. Hingston, F. J., Posner, A. M., and Quirk, J . P. 1972. J . Soil Sci. 23, 177-193. Hingston, F. J., Posner, A. M., and Quirk, J . P. 1974. J. Soil Sci. 25, 16-26. Hogg, D. E., and Toxopeus, M. R. J . 1966. N . Z . J . Agric. Res. 9, 93-97. Holford, I. C. R.. and Mattingly, G. E. G. 1975a. J . Soil Sci. 26, 407-417. Holford, 1. C. R., and Mattingly, G. E. G. 1975b. Geoderma, 13, 257-264. Holford, I. C. R., and Mattingly, G. E. G. 1976. Plant Soil 44, 219-229. Holford, I. C. R., Wedderburn, R. W . M., and Mattingly, G. E. G. 1974. J . Soil Sci. 25, 242-255. Holobrady, K . , and Galba, J . 1970. Pol'nohospodarsrvo 16, 575-581, Holobrady, K., Galba, J., and Chrenekova, E. 1969. Pol'nohospodarsrvo 15, 956-963. Hope, G. D., and Syers, J. K. 1976. J . Soil Sci. 27, 301-306. Hsu, P. H. 1964. Soil Sci. Soc. Am., Proc. 28, 474478. Hsu, P. H. 1965. Soil Sci. 99, 398-402. Hsu, P. H. 1968. Adv. Chem. Ser. 73, 1 15-127. Hsu,P. H., and Rennie, D. A. 1962. Can. J . Soil Sci. 42, 197-209. Huang, C. P. 1975a. J . Colloid Interface Sci. 53, 178-186. Huang, P. M. 1975b. Soil Sci. Soc. Am., Proc. 39, 271-274. Hubbard, E. A., and Walrnsley, D. 1974. Trop. Agric. 51, 361-369. Hudcova, 0. 1970. Ved. Pr. Vyzk. Ustavu Rastl. Vyroby Praze-Ruzyni 16, 181-186, Hudcova, 0.. and Kovarova, B. 1969. Rostl. Vyroba 15, 1065-1073. Humphreys, F. R., and Pritchett. W. L. 1971. Soil Sci. Soc. Am., Proc. 35, 495-500. Inoue, T., and Wada. K. 1968. Trans. Int. Congr. Soil Sci.. 9th, 1968 Vol. 3 pp. 289-298. Inoue, T., and Wada, K. 1971a. Clay Sci. 4, 61-70. Inoue, T., and Wada, K. 1971b. Clay Sci. 4, 71-86. Jacobs, L. W., Syers, J . K., and Keeney, D. R. 1970. Soil Sci. Soc. Am., Proc. 34, 750-754. Jasmund, K., and Lindner, B. 1973. Proc. Int. Clay Conf., 1972 pp. 399413. John, M. K. 1972. Commun. Soil Sci. Plant Anal. 3, 197-205. John, M. K., Saunders, W. M. H., and Watkinson, .I.H . 1976. N . Z . J . Agric. Res. 19, 143-151. Johnston, A. E., and Poulton, P. R. 1977. Rothamsted Exp. Stn. Rep., 1976 Part 2, pp. 53-85. Jones, G. B., and Belling, G. B. 1967. Aust. J . Agric. Res. 18, 733-740. Jones, J. P., and Benson, J. A. 1975. Commun. Soil Sci. Plant Anal. 6, 465-477. Jones, L. H. P. 1956. Science 123, I 116. Jones, L. H. P. 1957. J. Soil Sci. 8 , 313-317. I

46

R. L. PARFI’IT

Jones, L. H. P., and Handreck, K. A. 1965. Plant Soil 23, 79-96. Jones, L. H. P., and Handreck, K. A. 1967. Adv. Agron. 19, 107-150. Jones, M. J. 1975. Trop. Agric. (Trinidad) 52, 1-10, Jones, R. C., and Uehara, G. 1973. Soil Sci. SOC.Am., Proc. 38, 792-798. Juo, A. S. R., and Maduakor, H. P. 1974. Commun. in Soil Sci. Planr Anal. 5, 479-499. Juo, A. S. R., Moormann, F. R., and Maduakor, H. P. 1974. Geoderma 11, 167-179. Jurinak, J. J. 1966. Soil Sci. SOC.Am., Proc. 30, 559-562. Jurinak, J. J., and Burau, R. G. 1967. Soil Sci. SOC. Am., Proc. 31, 732-736. Kacar, B. 1967. Ankara Univ. Ziraat Fak. Yayin. 17, 215-234. Kafkafi, U., and Bar-Yosef, B. 1969. Proc. Inr. Clay Conf., 3rd. 1969 Vol. 1, p p . 691-696. K a f k d , U., and Giskin, M. 1970. Is. J . Chem. 8, 373-381. Kafkafi, U., Posner, A. M., and Quirk, J. P. 1967. Soil Sci. SOC.Am., Proc. 31, 348-352. Karim, M., Ahmed, F., and Islam, A. 1973. Geoderma 9, 221-227. Kelley, J. B., and Midgley, A. R. 1943. Soil Sci. 55, 167-176. Kinjo, T., and Pratt, P. F. 1971a. Soil Sci. SOC.Am., Proc. 35, 722-725. Kinjo, T.. and Pratt, P. F. 1971b. Soil Sci. SOC.Am., Proc. 35, 725-728. Kinjo, T., Pratt, P. F.,and Page, A. L. 1971. Soil Sci. SOC.Am., Proc. 35, 728-732. Kittrick, J. A., and Jackson, M. L. 1954. Science 120, 508-509. Kittrick, J. A., and Jackson, M. L. 1955. Soil Sci. SOC.Am., Proc. 19, 292-295. Kittrick, J. A., and Jackson, M. L. 1956. J . Soil Sci. 7, 81-89. Kodama, H., and Singh, S. S. 1972. Can. J. Soil Sci. 52, 209-218. Kodama, H., and Webber, M. D. 1975. Can. J. SoilSci. 55, 225-233. Kolthoff, I. M. 1936. J . Phys. Chem. 40, 1027-1040. Krishna Murti, G. S. R., Volk, V. V., and Jackson, M. L. 1966. Soil Sci. SOC.Am., Proc. 30, 685-688. Kuo, S., and Lotse, E. G. 1972. Soil Sci. SOC. Am., Proc. 36, 725-729. Kuo, S., and Lotse, E. G. 1974. Soil Sci. 116, 400406. Kyle, 1. H., Posner, A. M., and Quirk, J. P. 1975. J . Soil Sci. 26, 3 2 4 3 . LaFleur, K. S., and Craddock, G. R. 1967. Soil Sci. SOC.Am., Proc. 31, 324-327. Lahav, N., and Bolt, G. H. 1963. Nature (London) 200, 1343-1344. Landa, E. R., and Gast, R. G. 1973. Clays Clay Miner. 21, 121-130. Langdon, A. G., Perrott, K. W., and Wilson, A. T. 1973. J . Colloid Interface Sci. 44, 486494. Larsen, S. 1967. Adv. Agron. 19, 151-210. Larsen, S., Gunary, D., and Sutton, C. D. 1965. J . Soil Sci. 16, 141-148. Leal, J. R., and Velloso, A. C. X. 1975. Pesqui. Agropecu. Bras.. Ser. Agron. 8, 81-88. Leaver, J. P., and Russell, E. W. 1957. J . Soil Sci. 8, 113-126. Levesque. M. 1974a. Can. J . Soil Sci. 54, 63-68. Levesque, M. 1974b. Can. J . Soil Sci. 54, 205-214. Lincoln, S. F., and Stranks, D. R. 1968. Ausr. J . Chem. 21, 37-57. Little, L. 1966. “Infrared Spectra of Adsorbed Species.” Academic Press, New York. Lopez-Hernandez, D. L. 1974. Commun. Soil Sci. Planr Anal. 5, 145-154. Lopez-Hernandez, I. D., and Burnham, C. P. 1974a. J . Soil Sci. 25, 196-206. Lopez-Hernandez, I. D., and Burnham, C. P. 1974b. J . Soil Sci. 25, 207-216. Low, P. F., and Black, C. A. 1950. Soil Sci. 70, 273-290. Lucas, L. N., and Blue, W. G. 1972. Trop. Agric. (Trinidad) 49, 287-295. McKeague, J. A., and Cline, M. G. 1963a. Can. J. Soil Sci. 43, 83-96. McKeague, J. A., and Cline, M. G. 1963b. Adv. Agron. 15, 339-396. McPhail, M., Page, A. L., and Bingham, F. T. 1972. Soil Sci. SOC.Am., Proc. 36, 510-514. Manojlovic, S. 1965. Zemljiste Biljka 14, 25-35. Mattingly, G. E. G. 1965. Rep. For. Res. Comm., London, 1965 p p . 93-96.

ANION ADSORPTION BY SOILS

47

Mattingly, G. E. G. 1975. SoilSci. 119, 369-375. Mattingly, G. E. G., and Talibudeen, 0. 1961. Rothamsted Exp. Stn. Rep.. 1960 pp. 246-265. Mehlich, A. 1961. Trans. Inr. Congr. Soil Sci., 7th 1960 Vol. 11, pp. 292-302. Mehlich, A. 1964. Soil Sci. Soc. Am., Proc. 28, 492496. Mekaru, T. 1969. M.S.Thesis, University of Hawaii, Honolulu. Mekaru, T., and Uehara, G. 1972. Soil Sci. SOC.Am., Proc. 36, 296-300. Metwally, A. I., El-Damaty, A. H.,and Yousry, M. 1974. Agrokem. Talajfan 23, 59-70. Miller, R. W. 1967. Soil Sci. SOC.Am., Proc. 31, 46-50. Mitchell, D. D., Farmer, V. C., and McHardy, W. 1. 1964. Adv. Agron. 16, 327-383. Mokwunye, U. 1975. Soil Sci. SOC. Am., Proc. 39, 1100-1 102. Mortland, M. M. 1970. Adv. Agron. 22, 75-117. Moshi, A. O., Wild, A,, and Greenland, D. J. 1974. Geoderma 11, 275-285. Mon, C. J. B. 1970. SCI Monogr. 37, 40-53. Muljadi, D., Posner, A. M., and Quirk, J. P. 1966a. J . Soil Sci. 17, 212-229. Muljadi, D., Posner, A. M., and Quirk, J. P. 1966b. J . Soil Sci. 17, 230-237. Muljadi, D., Posner, A. M., and Quirk, J. P. 1966c. J. Soil Sci. 17, 238-247. Munns, D. N., and Fox, R. L. 1976. Soil Sci. SOC.Am. J . 40, 46-51. Myszka, A., and Janowska, M. 1973. Pol. J . Soil Sci. 6, 27-35. Nagarajah, S . , Posner, A. M., and Quirk, J. P. 1968. Soil Sci. Soc. Am., Proc. 32, 507-510. Nagarajah, S., Posner, A. M., and Quirk, J. P. 1970. Nature (London) 228, 83-85. Nonish, K. 1968. Trans. Inr. Congr. Soil Sci. 9th. 1968 Vol. 2, pp. 713-723. Nonish, K . , and Taylor, R. M. 1961. J . Soil Sci. 12, 294-306. Oades, J. M. 1963. Soils Fert. 26, 69-80. Obihara, C. H., and Russell, E. W. 1972. J . SoilSci. 23, 105-117. Okazaki, E., and Chao, T. T. 1968. Soil Sci. 105, 255-259. Olsen, S. R., and Watanabe, F. S. 1957. Soil Sci. SOC.Am., Proc. 21, 144-149. Ozanne, P. G., and Shaw, T. C. 1967. Ausr. J . Agric. Res. 18, 601-612. Ozanne, P. G., and Shaw, T. C. 1968. Trans. Int. Congr. SoilSci., 9th. 1968 Vol. 2, pp. 273-280. Partitt, R. L. 1972. Soil Sci. 113, 417421. Parfitt, R. L. 1977. Soil Sci. SOC.Am. J . 41, 1064-1067. Parfitt, R. L., and Atkinson, R. J. 1976. Nature (London) 264, 740-742. Parfitt, R. L.,and Russell, J. D. 1977. J. Soil Sci. 28, 297-305. Parftt, R. L., and Smart, R. St. C. 1977. J. Chem. Soc., Faraday Trans. 173, 796-802. Parfitt, R. L.,and Smart, R. St. C. 1978. Soil Sci. SOC.Am. J. 42, 48-50. Parftt, R. L., Thomas, A. D., Atkinson, R. J., and Smart, R. St. C. 1974. Clays Clay Miner. 22, 455456. Parfitt, R. L., Atkinson, R. J., and Smart, R. St. C. 1975. Soil Sci. Soc. Am., Proc. 39, 837-841. Parftt, R. L., Russell, J. D., and Farmer, V. C. 1976. J. Chem. Soc.. Faraday Trans. 172, 1082- 1087. Parfitt, R. L., Fanner, V. C., and Russell, J. D. 1977a. J . Soil Sci. 28, 29-39. Parfitt, R. L., Fraser, A. R., Russell, J. D., and Farmer, V. C. 1977b. J . Soil Sci. 28, 4 0 4 7 . Parftt, R. L., Fraser, A. R., and Fanner, V. C. 1977c. J. Soil Sci. 28, 289-296. Perrott, K. W., Langdon, A. G., and Wilson, A. T. 1974a. Geoderma 12, 223-231. Perrott, K. W., Langdon, A. G., and Wilson, A. T. 1974b. J . Colloid Inrerjiace Sci. 48, 10-19. Perrott, K. W., Smith, B. F. L., and lnkson, R. H. E. 1976a. J . Soil Sci. 27, 58-67. Perrott. K. W., Smith, B. F. L.,and Mitchell, B. D. 1976b. J. Soil Sci. 27, 348-356. Peverill, K. T., Briner, G. P., and Douglas, L. A. 1975. Ausr. J . Soil Res. 13, 69-76. Pissarides, A., Steward, J. W. B., and Rennie, D. A. 1968. Can. J . SoilSci. 48, 151-157. Probert, M. E.. and Larsen, S. 1972. J. Soil Sci. 23, 76-81. Rajan, S. S . S. 1975a. Nature (London) 253, 434436.

48

R. L. PARFITT

Rajan, S. S. S. 1975b. N.Z.J. Sci. 18, 93-101. Rajan, S. S. S. 1975b. J . Soil Sci. 26, 250-256. Rajan, S. S. S. 1976. Nature (London) 262, 45-46. Rajan, S. S. S.,and Fox, R. L. 1972. Commun. in Soil Sci. Plant Anal. 3, 493-504. Rajan, S. S. S., and Fox, R. L. 1975. Soil Sci. Soc. Am., Proc. 39, 846-851. Rajan, S. S. S.,and Perrott, K. W. 1975. J. Soil Sci. 26, 257-266. Rajan, S. S. S.,and Watkinson, J. H. 1976. Soil Sci. SOC. Am. J . 40, 51-54. Rajan, S. S. S., Perrott, K. W., and Saunders, W. M. H. 1974. J. Soil Sci. 25, 438-447. Rankin, P. C., and Wilson, A. T. 1969. J. Colloid Interface Sci. 30, 277-283. Reeve, N. G., and Sumner, M. E. 1970. Soil Sci. SOC.Am., Proc. 34, 263-267. Reeve, R. C., Pillsbury, A. F., and Wilcox, L. V. 1955. Hilgardia 24, 69-91. Reisenauer, H.M., Tabilch, A. A., and Stout, R. R. 1962. Soil Sci. Soc. Am., Proc. 26, 23-27. Rennie, D. A., and McKercher, R. B. 1959. Can. J . Soil Sci. 39, 64-75. Reyes, E. D., and Jurinak, J. J. 1967. Soil Sci. Soc. Am., Proc. 31, 637-641. Rhoades, J . D., Ingvalson, R. D., and Hatcher, J. T. 1970. Soil Sci. SOC. Am., Proc. 34, 871-875. Rich, C. I. 1968. Clays Clay Miner. 16, 15-30. Roth, C. B . , Jackson, M. L., and Syers, J. K., 1969. Clays Clay Miner. 17, 253-264. Roy, A. C . , Ali, M. Y.,Fox, R. L., and Silva, J. A. 1971. I n t . Symp. Soil Fertil. Eval., Proc., Ist, 1971 VOI. 1, pp. 757-765. Russell, E. W. 1973. “Soil Conditions and Plant Growth.” Longmans, Green, New York. Russell, G. C., and Low, P. F. 1954. Soil Sci. SOC. Am., Proc. 18, 22-25. Russell, J. D. 1974. In “The Infrared Spectra of Minerals” (V. C. Farmer, ed.), pp. 11-25. Mineral. SOC.,London. Russell, J. D., Partitt, R. L., Fraser, A. R., and Farmer, V. C. 1974. Nature (London) 248, 220-22 1. Russell, J. D., Paterson, E., Fraser, A. R., and Farmer, V. C. 1975. J . Chem. Sor., Faraday Trans. I71, 1623-1630. Ryden, J . C., and Syers, J. K . 1975a. Nature (London) 255, 51-53. Ryden, J. C., and Syers, J. K . 1975b. J . Soil Sci. 26, 395-406. Ryden, J. C . , and Syers, J. K. 1976. Soil Sci. Soc. Am. J . 40, 845-846. Ryden, J. C., and Syers, J. K . 1977. Soil Sci. 123, 353-361. Ryden, J. C . , Syers, J. K., and Hanis, R. F. 1972. J. Environ. Qual. 1, 430-434. Ryden, J. C., Syers, J. K., and Hanis, R. F. 1973. Adv. Agron. 25, 1-45. Ryden, J. C., Syers, J. K., and McLaughlin, J. R. 1977a. J. Soil Sci. 28, 62-71. Ryden, J. C., McLaughlin, J. R., and Syers, J. K. 1977b. J. Soil Sci. 28, 72-92. Sanders, F. E., and Tinker, P. B. H. 1975. Geoderma 13, 317-324. Saunders, W. M. H. 1965. N.Z.J.Agric. Res. 8, 30-57. Sawhney, B. L. 1973. Soil Sci. SOC.Am., Proc. 37, 658-660. Sawhney, B . L. 1974. Soil Sci. SOC. Am., Proc. 38, 159-160. Schalscha, E. B . , Pratt, P. F., Kinjo, T., and Amar, J . 1972. Soil Sci. Soc. Am., Proc. 36, 912-914. Schalscha, E. B., Bingham, F. T., Galindo, G. G., and Galvan, H. P. 1973. Soil Sci. 116, 70-76. Schalscha, E. B., Pratt, P. F., and Dornecq, T. C. 1974a. Soil Sci. Soc. Am., Proc. 38, 44-45. Schalscha, E. B., Pratt, P. F., and Soto, D. 1974b. Soil Sci. Soc. Am., Proc. 38, 539-540. Schell, W. R., and Jordan, J. V. 1959. Plant Soil 10, 303-318. Schnitzer, M. 1969. Soil Sci. SOC.Am., Proc. 33, 75-81. Schnitzer, M., and Skinner, S. M. 1964. Soil Sci. 98, 197-203. Schofield, R. K. 1949. J. Soil Sci. 1, 1-8. Schofield, R. K . , and Samson, R. R. 1953. Clay Miner. Bull. 2, 45-51. Schwertmann, U. 1964. Z . Pfanzenernahr., Dueng., Bodenkd. 105, 194-202. Schwertmann, U . , and Knittel, H . 1973.2. Pfanzenernahr., Dueng. Bodenkd. 134, 43-52.

ANION ADSORPTION BY SOILS

49

Schwertmann, U., Fischer, W. R., and Papendorf, H. 1968. Trans. fnr. Congr. Soil Sci., 9rh, 1968 Vol. 1, pp. 645-655. Schwertmann, U., Fischer, W. R., andTaylor, R. M. 1974. Trans. fnr. Congr. Soil Sci., IOrh, 1974 Vol. 6, pp. 237-249. Scott, N. M. 1976. J. Sci. Food Agric. 27, 367-372. Seleznev, Yu M., and Tyuryukanov, A. N. 1970. Pochvovedenie 10, 26-31. Shapiro, R. E., and Fried M. 1959. Soil Sci. SOC. Am., Proc. 23, 195-198. Sims, J. R., and Bingham, F. T. 1967. Soil Sci. SOC.Am., Proc. 31, 728-732. Sims, J. R., and Bingham, F. T. 1968a. Soil Sci. SOC. Am., Proc. 32, 364-369. Sims, J. R., and Bingham, F. T. 1968b. Soil Sci. SOC.Am., Proc. 32, 369-373. Singh, B. B., and Jones, J . P. 1977. Plant Soil 46, 31-44. Singh, B. R., and Kanehiro, Y. 1969. Soil Sci. SOC.Am., Proc. 33, 681-683. Singh, S. S. 1964. Soil Sci. 98, 383-387. Smith, A. N. 1965. J. Aust. fnsr. Agric. Sci. 31, 110-126. Smith, B. H., and Leeper, G. W. 1969. J. Soil Sci. 20, 246-254. Smith, S. J., and Davis, R. J. 1974.1. Environ. Qual. 3, 152-155. Sree Ramulu, U.S., Pratt, P. F., and Page, A. L. 1967. Soil Sci. SOC.Am., Proc. 31, 193-196. Stout, P. R., Meagher, W. R., Pearson, G. A., and Johnson, C. M. 1951. Plant Soil 3, 51-87. Stumm, W., and Leckie, J. 0. 1971. Pror. Int. Conf. Water Pollur. Res., 5th, 1970 pp. 1-26. Swoboda, A. R., and Thomas, G.W. 1965. Soil Sci. SOC. Am., Proc. 29, 540-544. Syers, J . K., Evans, T. D., Williams, J . D. H., and Murdoch, J . T. 1971. Soil Sci. 112, 267-275. Syers, J. K., Browman, M. G.,Smillie, G.W. and Corey, R. B. 1973.Soil Sci. SOC.Am., Proc. 37, 358-363. Talibudeen, 0. 1958. J. Soil Sci. 9, 120-129. Tamimi, Y. N., Kanehiro, Y.,and Sherman, G. D. 1968. Soil Sci. 105,434-439. Tamm, 0. 1922. Medd. Statens Skogsfoersoeksanstalt 19, 387-404. Taylor, A. W., Gurney, E. L., and Frazier, A. W. 1965. Soil Sci. SOC. Am. Proc. 29, 317-320. Taylor, R. M., and Schwertmann, U. 1974. Aust. J. Soil Res. 12, 133-146. Theng, B. K. G. 1971. N.Z.J. Sci. 14, 1040-1056. Thorup, R. M., and Mehlich, A. 1961. SoilSci. 91, 38-43. Trobisch, S., and Schilling, G. 1963. Chem. d. Erde 23, 91-103. Tweneboah, C. K., Greenland, D. J., and Oades, J. M. 1967. Ausr. J. Soil Res. 5, 247-261. Udo, E. J., and Uzu, F. 0. 1972. Soil Sci. SOC. Am., Proc. 36, 879-883. Vanderdeelen, J., lnes Pino, N., and Baert, L. 1973. Turrialba 23, 291-296. van Raij, B., and Camargo, de 0. A. 1974. Trans. Inr. Congr. Soil Sci., IOrh, 1974 Vol. 2, pp. 384-39 I . van Raij, B., and Peech, M. 1972. Soil Sci. Soc. Am., Proc. 36, 587-593. van Riemsdijk, W. H., Westrate, F. A., and Bolt, G.H. 1975. Nature (London) 257, 473-474. van Riemsdijk, W. H., Weststrate, F. A,, and Beek, J . 1977. J. Environ. Qual. 6 , 26-29. Wada, K. 1959. Soil Sci. 87, 325-330. Wada, K., and Harward, M. E. 1974. Adv. Agron. 26, 21 1-260. Wada, K., and Inoue, A. 1974. Soil Sci. Plant Nurr. 20, 5-15. Watson, J . R., Posner, A. M., and Quirk, J. P. 1973. J . Soil Sci. 24, 503-5 11. Weir, C. C. 1972. Trop. Agric. (Trinidad) 49, 89-96. Weir, C. C., and Soper, R. J . 1963. Can. J. Soil Sci. 43, 393-399. Wells, A. F. 1962. “Structural Inorganic Chemistry.” Oxford Univ. Press (Clarendon), London and New York. White, R. E., and Beckett, P. H.T. 1964. Plant Soil 20, 1-15. White, R. E., and Taylor, A. W. 1977. J. Soil Sci. 28, 48-61. Whitehead, D. C. 1973. J. Sci. Food Agric. 24, 547-556.

50

R. L. PARFITT

Whitehead, D. C. 1974. J . Sci. Food Agric. 25, 73-79. Wild, A. 1950a. Trans. Int. Congr. Soil Sci.. 41h. 1950 Vol. I , pp. 146-149. Wild, A. 1950b. J . Soil Sci. 1, 221-238. Wild, A. 1953. J . Soil Sci. 4, 72-85. Wild, A. 1972. J . Soil Sci. 23, 315-324. Williams, E. G . 1961. Trans. Inr. Congr. Soil Sci.. 7rh, 1960 Vol. 3, pp. 604-611. Williams, E. G . , Scott, N. M . , and McDonald, M. J . 1958. J . Sci. Food Agric. 9, 551-559. Woodruff, J . R., and Kamprath, E. J. 1965. Soil Sci. Soc. Am., Proc. 29, 148-150. Woolson, E. A . , Axley, J . H . , and Keamey, P. C. 1973. Soil Sci. SOC.Am.. Proc. 37, 254-259. Yates, D. E., and Healy, T.W. 1975. J . Colloid Inretface Sci. 52, 222-228. Yates, D. E., Levine, S., and Healy, T.W. 1914. J . Chem. Soc., Faraday Trans. I 70, 1807-1818.

ADVANCES IN AGRONOMY, VOL. 30

COLD HARDINESS AND FREEZING INJURY OF AGRONOMIC CROPS Peter L. Steponkus Department of Agronomy, Cornell University, Ithaca, New York

I. Introduction ............ ........... .. . .. . .. . A. Winter B. Cold Hardiness ...................................................... 11. Characterization of the Freezing Process and Freezing Injury A. The Freezing Process.. . . . . . , . . . . . B. Factors Affecting the Freezing Process . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

111. Environmental Factors Affecting Cold Hardiness

. .. . . . . . .. . . .. .. . . . . . . . . . . ... .

Repercussions of Freezing on the D. Manifestations of Freezing Injury 111. Environmental Factors Affecting Cold C.

............................. ................................. ...................... ....................

IV. Effect of Developmental Stage on Cold ss . . . . . . . . . . . . . V. Physiological and Biochemical Aspects A. Biochemical Alterations from a D B. Biochemical Alterations from an Environmental Perspective . C. Biochemical Alterations from a Stress Avoidance Perspective D. Biochemical Alterations from a Stress Tolerance Perspective VI. Screening and Stress Procedure VII. A. Summary and Conclusions Acclimation Procedures. . . . . ............. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References ..... . . . . . . ., . . . . . . . . B. Freezing Procedures.. . . . . . . . . . . . . . .

51 51 53 54 55 56 60 62 65 67 68 70 71 73 75 76 80 86 88 89 90 91 92 93

I. Introduction

A. WINTER HARDINESS

Winter hardiness of cereal grains and perennial forage crops is of considerable concern to agronomists in cold northern temperate regions of the world. Reductions in grain yield are incurred not only as a direct result of winter damage to fall-seeded crops but also as a result of limiting the areas where such crops can be 'Department of Agronomy Series Paper No. 1225. 51 Copyright @ 1978 by Academic Press, Inc. All rights of reproduction in any form reserved. ISBN-0- 12-000730.4

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sown, as the alternative is to use spring-sown cultivars, which are generally less productive (Salmon, 1917a; Hill and Salmon, 1927; Warnes et al., 1971). In addition, winter hardiness is a prime factor limiting perennation of forage crops grown in northern regions. A stand reduction of 25% or more is considered to be sufficient deterioration to warrant replanting (Heinrichs, 1973). As a result, winter hardiness of agronomic crops has been the subject of considerable investigation, and development of varieties with improved winter hardiness for northward expansion is of primary concern (Warnes and Johnson, 1972b). In spite of these efforts, however, the introduction of new cultivars that possess increased winter hardiness has not always been so successful (Grafius, 1974). Although Grafius (1974) concludes that present methods are inadequate for increasing winter hardiness, it might be more appropriate to consider that the primary objective to increase winter hardiness per se is too broad an undertaking. Winter hardiness implies avoidance of or tolerance to all the cumulative effects of winter that a plant encounters-including freezing, heaving, smothering, desiccation, and diseases (Salmon, 1917b). The combined effects of climatic, soil, plant, and cultural factors interact to determine the degree of injury incurred by a crop following the rigors of winter. Soil factors, such as compaction or waterholding capacity, may accentuate or diminish the influence of several climatic factors, including temperature and precipitation. Conversely, climatic conditions, such as the amplitude of diurnal temperature fluctuations or snow cover, may mitigate soil factors. Cultural practices and previous climatic conditions may influence the plant’s resistance, which has considerable diversity within a species, to the stresses imposed on it by the combined climatic and soil factors. Plant resistance may take the form of certain physiological or morphological adaptations that allow the plant either to tolerate or to avoid the imposed stresses. Tolerance and avoidance mechanisms may reside at either the whole plant, tissue, or cellular level. Thus, the undertaking to increase winter hardiness is indeed a rather ambitious objective, and one that is probably insurmountable if approached in its entirety. In addition to the various factors that affect cold hardiness, numerous logistical difficulties are encountered in assessing winter hardiness. The usual approach is to subject the plants to the rigors of winter in a field situation. Such a situation lacks any control over the severity of the stresses imposed on the plants and also lacks any degree of consistency (Hill and Salmon, 1927). In this respect, Levitt (1956) has indicated that winter conditions that result in differential survival occur only once every ten years. Salmon (1933) indicates that between 1917 and 1933, in the location of the experiment, no winter was severe enough to distinguish between relatively hardy and less hardy varieties of wheat. Thus, it is often necessary to grow material for many years and in several locations in order to maximize the probability of achieving the desired degree of injury (Andrews, 1958). The need to delineate the various components of winter hardiness and to devise appropriate stress conditions for each is evident.

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B. COLD HARDINESS Of all the factors relating to the winter hardiness complex, cold hardiness, the ability to withstand low freezing temperatures, is of paramount importance. In most winter-wheat-producing areas, temperature is the single most important factor limiting plant survival (Johnson et al., 1970). In an evaluation of the survival of wheat varieties grown at nearly thirty experiment stations in the Great Plains for several decades, direct freezing injury appeared to be the principal cause of killing (Quisenberry, 1938). Heifer and Kline (1960) indicated that soil temperatures below -6°C at a 2.5-cm depth caused significant winter killing of winter oats. The ability of plants to withstand low temperatures is a latent trait, which exhibits an annual periodicity. It is only through the interaction of appropriate environmental cues and the genetic potential of a species that an increase in cold hardiness is manifested. Therefore, of prime concern are the environmental factors that affect the annual process of cold acclimation and, of equal significance, the annual process of deacclimation. Although the usual approach has been to question what alterations are occurring in the tissue in response to the environmental cues, attention should be directed first to understanding what conditions or stresses the plant is expected to avoid or tolerate during the freezing process. Thus, before an attempt is made to assess what biochemical or physiological alterations are causally related to the acclimation process, knowledge of what constitutes freezing damage is essential. It is well established that the order of cold hardiness is rye > wheat > barley > oats, but it is not known whether these differences are due to differences in the tolerance of freezing stresses or to differences in the freezing stresses that arise in the different species during freezing. Questions of why freezing to - 18°C allows for survival whereas freezing to -20°C results in death are not adequately answered. What changes in the cellular environment are effected by this slight decrease in temperature so that survival is now precluded? The answers to these questions are needed to assess accurately the significance of biochemical changes occumng during cold acclimation in order to determine which are causally related to the ability to withstand freezing stresses. Much of the research directed toward an understanding of the mechanism of cold acclimation has centered on the analysis of various cellular constituents in plants that have been subjected to acclimating conditions. This wealth of information cannot be fully appreciated, however, because of a lack of understanding of what constitutes freezing injury. Unfortunately, the basic premise of such correlative investigations is that an increase (or decrease) in a particular cellular constituent implies a causal relationship to cold hardiness. This rationale has even been extended to assuming that relative differences in cold hardiness between cultivars or even between species should be accompanied by corresponding increments in the particular constituent under investigation. However, this

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would hold true only if the investigator were fortunate enough to choose the one cellular constituent that was the rate-limiting step in the entire cold acclimation process. It is not too surprising that this approach frequently parallels current technology in laboratory methodology and instrumentation. Thus, in order to ultimately improve the winter hardiness of agronomic crops, we must first address the problem of cold hardiness. Fundamental to such an endeavor is the need to characterize the freezing stresses that are imposed on the plant tissue, to understand the repercussions of these stresses on the cellular environment and architecture, and to determine what constitutes freezing injury at the cellular and molecular level. Only when such informatiofi is available can the physiological and biochemical aspects of cold acclimation be fully elucidated. With such an approach, procedures for artificial acclimation, freezing, and assessment of subsequent viability will emerge for use in evaluation of germplasm in breeding programs and for formulation of appropriate cultural and management practices. Moreover, such information would provide direction for breeding programs and cultural practices rather than merely serving as a postmortem evaluation. It is within the above format that this review will be presented. II. Characterization of the Freezing Process and Freezing Injury

In recent years, several comprehensive reviews on the freezing process and resultant injury in plants have been written. These include the extremely comprehensive treatise by Levitt (1972); the reviews by Mazur (1969, 1970), with special emphasis on the physicochemical aspects of the freezing process; the review of Olien (1967a), which discusses freezing stresses that result from macro and micro redistribution patterns of water in relation to survival; the review of Heber and Santarius (1973), which places particular emphasis on the possible mechanisms of protection by various cellular constituents; and the review of Burke ef al. (1976) on freezing injury. For the purpose of this review, consideration of the physical and chemical events that occur during freezing, the ensuing changes in the cellular environment, and the repercussions on cellular structure and function are of prime concern. Current knowledge of the physicochemical aspects of the freezing process is quite extensive (Mazur, 1969, 1970; Olien, 1967a, 1977). In comparison, our knowledge of what constitutes freezing damage at the molecular level is rather deficient. Although numerous theories on the mechanism of freezing injury have been postulated, in 1969 Mazur considered them all to have deficiencies. Unfortunately, this still holds true. Contributing to this situation is the fact that the multiple stresses that arise during freezing are viewed simply as causing death, without any delineation of the numerous ways in which death can be effected. Even at the cellular level this deficiency prevails, and, instead of death, loss of

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semipermeability is the measure of damage. Such deficiencies in understanding what constitutes freezing damage have precluded an accurate assessment of the proposed mechanisms of injury and cold acclimation.

A.

THE FREEZING PROCESS

Freezing in plant tissues involves the redistribution of water with respect to both its physical state and its location. The freezing process and the resultant alterations in the plant can be studied at various levels of organization within the plant. However, regardless of the level of ultimate concern, the freezing process in an individual cell should be of immediate concern, and it is at the cellular level that an understanding of the freezing process must begin. Mazur (1969, 1970) has detailed the physicochemical events occurring during freezing. In summary, when intact plants, tissues, cells, or isolated organelles are subjected to temperatures that are decreasing below the freezing point of water, the water both in the cell and in the extracellular surroundingswill initially supercool. Because the extracellular solution has a lower solute concentration and more effective ice nucleators, initial ice formation will occur extracellularly. Generally at temperatures above - lOT, subsequent nucleation of the intracellular water is prevented by the plasma membrane. As the vapor pressure of the extracellular ice-water mixture is less than that of the intracellular water, a vapor pressure gradient results. Vapor pressure equilibrium can be achieved either by the efflux of water out of the cell to the extracellular ice, which results in cellular dehydration, or by intracellular ice formation. The manner in which equilibrium is achieved depends on the rate at which the cells are cooled in relation to the permeability of the plasma membrane and the surface-area-to-volumeratio. The temperature of the external ice will establish the lower value of the vapor pressure gradient, and hence will be responsible for water to be removed from the cell to achieve equilibrium. However, the actual amount that is removed will depend on the initial osmolality of the intracellular solution. Whether this amount of water will be removed depends on the membrane permeability and the surface area available for efflux. If the flux is not adequate, the cells will equilibrate by intracellular ice formation-which is generally considered to be lethal (Levitt, 1972). However, under the freezing rates normally encountered in nature, the cells will equilibrate by extracellular ice formation. It should be emphasized that, even though ice formation occurs at only a few degrees below O'C, liquid water still remains. In dilute solutions the entire system will eventually be composed of ice, and the solutes will precipitate (Mazur, 1969). This point is referred to as the eutectic point of the solution. Eutectic points are usually not observed in complex systems such as cells, and a small fraction of water will remain unfrozen even at low temperatures (Heber and Santarius, 1973). This point is very important in

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considering the ways in which freezing can affect cellular structure. If thermal equilibration is achieved and is followed by vapor pressure equilibrium, transitions are still occurring within the frozen tissue. Recrystallization-the conversion of small or nonspherical crystals to large spherical crystals-will occur because of the higher surface free energy of the former. Although the above events are associated with the freezing process, injury is usually apparent after thawing. Although this can, in part, be due to the necessity of a thawed condition for manifestation of injury that was incurred during freezing to be visible, there are numerous reports that events during thawing may be injurious (Levitt, 1972). During thawing, the vapor pressure of the external ice-water solution rises, and a vapor pressure gradient will again be established. Equilibration requires the movement of water back into the cell. It is within this setting of freezing and thawing that questions arise as to how these various cellular environmental changes result in injury and how plants in an acclimated state can survive the freezing process.

B. FACTORS AFFECTING THE FREEZING PROCESS

The preceding discussion provides a general description of the freezing process that is widely used to consider the various stresses that a cell will be subjected to during freezing. There is general agreement that intracellular ice formation subjects the plant cells to mechanical stresses of ice, and extracellular ice formation subjects the cells to dehydration, which results in several subsequent stresses. Although there is no question that, under certain conditions, the two distinct types of freezing can occur as described, additional stresses can occur in intact plants composed of several different tissue types. These additional stresses can occur after the initial extracellular ice nucleation event but before equilibration is achieved. In these situations, several factors, both internal and external, can affect the freezing process and alter the stresses that arise in the cellular environment. Olien (1961, 1964, 1965) has indirectly studied the patterns of extracellular water content during freezing by observing the electrophoretic behavior of various charged dyes. Several patterns of fluctuation in extracellular water content during freezing have been observed and have been interpreted as indicative of different types of freezing stress. Following the initial event of extracellular ice formation, two types of freezing are inferred: equilibrium and non-equilibrium freezing. Olien (1977) considers the distinction between the two as being a function of the intensity of the freezing process-with intensity referring to the amount of energy required for ice crystal growth that acts in a specific time interval and region of tissue (Olien, 1973). Low-intensity freezing induces

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equilibrium water transitions, and high-intensity freezing results in nonequilibrium transitions. Nonequilibrium freezing involves a sudden drop in the content of liquid between protoplasts, during which time the amount of water frozen is not a function of temperature. This displacement from equilibrium is large, especially as freezing begins (Olien, 1967a). Depending on conditions in the tissue and the type of tissue, nonequilibrium freezing, which originates in the extracellular region, can result in two forms of stress. The sudden formation of ice can cause nucleation of the intracellular water and result in intracellular freezing as described previously. Alternatively, the nonequilibrium freezing energy can be dissipated by explosive formation of large ice masses along the cell walls, resulting in separation and disruption of the tissues (Olien, 1967a). Although both processes are nonequilibrium freezing events, the former results in intracellular ice formation, whereas the latter results in extracellular ice formation. Equilibrium freezing involves a continuous exponential decrease in liquid between protoplasts as temperature decreases and results in cell contraction due to dehydration. Thus, equilibrium freezing would describe the process of extracellular ice formation as outlined in the previous section. However, dehydration of the cell can occur either by having the extracellular ice and unfrozen water in contact with the cell surface, or it can be achieved through a vapor phase with the ice spatially separated from the cell surface (Olien, 1977). The energies of freezing and frost desiccation have been discussed by Olien (1971a). Adhesion stresses can also result from equilibrium freezing. Several factors determine whether equilibrium or nonequilibrium freezing will occur, and significant differences exist in the patterns of water transitions, ice structures, killing temperature, and injury (Olien, 1967a). These factors include the amount of supercooling, moisture content of the tissue, heat transfer, and tissue type. Although some factors can quantitatively affect the degree of stress and result in the degree of injury being a function of temperature, other factors can qualitatively affect the freezing process and produce a different type of stress, which is not a function of temperature. It is clear that Olien’s work demonstrates the importance of how one views the freezing process. Consideration of whether a given factor is affecting the freezing process is usually not done directly, and alterations in the freezing process are usually inferred from evaluation of the damage or injury incurred. Factors that have been shown to affect the degree of injury include duration and intensity of the cold, rate of freezing and thawing, degree of supercooling, and multiple freezing cycles; these factors relate to the physical parameters of the test environment. Other factors that affect the degree of injury include stage of growth or development, anatomical differences, moisture content, and growth habit; such factors relate to parameters of the test subject. In determining how or why these

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factors affect the degree of injury, concern should be directed to whether they alter the freezing process and resultant stresses, or whether they affect the sensitivity of the plant to the stresses. Such a distinction would be helpful in considering the process of cold acclimation, to be discussed in a subsequent section (Section V). However, for now it may be introduced by the question of whether cold acclimation involves an alteration in the freezing process and resulting stresses, or whether the tolerance or sensitivity of the plant is altered. It is clear from Olien's work that the former is a valid and documented possibility. With reference to factors that affect the freezing process, it is possible that the wellestablished and substantial differences in hardiness that exist in different plant organs (leaves versus roots) may be due to differences in the freezing stresses imposed on the tissues rather than strictly due to differences in "hardiness"-if hardiness is interpreted to mean tolerance (see Levitt, 1972). Therefore, careful consideration of the factors that affect the freezing process is warranted, especially in assessing what factors are causally related to the acclimation process. 1 . Moisture Content

Numerous reports by some of the earliest workers (Chandler, 1913; Schaffnit, 1910; Sinz, 1914) demonstrated that winter injury was greater with high levels of tissue moisture. Salmon (1917b) considered moisture content of plant tissue to be among the most important of internal factors that influence winter hardiness. Subsequently, alterations in moisture content were shown to occur during both cold acclimation (Newton, 1924; Gruentuch, 1935; Andrews et al., 1974a) and deacclimation (Laude, 1937; Gusta and Fowler, 1976). In the above studies, there was a high correlation between the degree of injury incurred and water content; however, it was not established as to whether this was due to an alteration in the freezing process or to some influence on the plants' tolerance. In 1964, Olien reported that decreasing the moisture content of barley leaves from 3.5 to 1.5 g H,O per gram dry weight decreased the lethal temperature from 25" to O"F, and the freezing point decreased from 30" to 25°F. In this and subsequent papers, Olien and co-workers (1965, 1974a, 1975; Olien and Marchetti, 1976) concluded that the lower moisture content was altering the freezing process from an injurious nonequilibrium pattern to a less-injurious equilibrium pattern. The killing temperature of acclimated barley is lowest (- 10" to -20°C) at 65% tissue moisture, increasing to 0°C when the tissue moisture approaches 80% (Olien, 1974b). In wheat, high moisture content resulted in LQ, values between - 12" and - 16°C; under low moisture content the LQ, values were between -15" and -23°C. Although Olien considers moisture content to alter the freezing stress rather dramatically, reduced moisture levels can also result in an increased solute concentration, which would influence the amount of water removed from the intracellular solution.

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2 . Rate of Cooling The rate of freezing and thawing is a primary factor that influences freezing injury. As previously discussed, the rate at which cooling occurs will determine the type of freezing (Mazur, 1969, 1970) or the intensity and type of stresses involved (Olien, 1967a). As early as 1917, Salmon (1917a) suggested that slow freezing decreases injury by preventing ice formation within the cells, giving the tissue an opportunity to dry out and permitting the protoplasm to adjust to the new conditions. From observations of the freezing of various cell types, Mazur (1969) surmises that slow cooling rates promote long exposures to solution effects-that is, exposure to critical concentrations of solute or to critical levels of dehydrationand faster rates increase the probability of intracellular freezing. Such interpretations are based on a wide range of cooling and thawing rates associated with the freeze preservation of cells and tissues. Although it is frequently observed in intact tissues that fast freezing rates increase injury (Sprague, 1955), it has not generally been observed that extremely slow rates are necessarily more injurious than intermediate rates. However, in very few instances has a sufficiently wide range of freezing rates been investigated in intact plants. Furthermore, it is also important to ascertain whether the fast rates of cooling that increase injury are actually experienced under natural conditions. For example, Sprague (1955) demonstrated that cold-acclimated ladino clover stolons and alfalfa roots and crowns were injured less when cooled slowly than when cooled rapidly. However, most significant was the fact that measured midwinter plant temperatures on clear days and nights approached those found to be lethal. In addition to the rate of cooling, the rate of thawing may also influence the degree of injury. Gusta and Fowler (1977) demonstrated that wheat plants thawed slowly (0.5"-2"C/hr) had an LDs0 of -18"C, whereas those thawed rapidly (2"-4"C/min) had an LQ, of - 15°C. Although the incidence of such a rapid thawing rate under natural conditions is extremely unlikely, this observation must be recognized in artificial freezing tests.

3 . Duration of Freezing Once thermal equilibration of the tissue with the ambient temperature occurs, vapor pressure equilibration will follow. Once vapor pressure is achieved during extracellular freezing, cellular dehydration should be maximal and further increases in injury should be minimal. However, numerous reports have demonstrated that the length of time the tissue is frozen can influence the degree of injury that results (Hudson and Brustkern, 1965; Greenham, 1966; Rammelt, 1972). Similarly, Gusta and Fowler (1977) report that at a given freezing temperature the duration between 0 and 1 hour had no effect on injury, but after

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24 hours the injury increased. One might question whether this was a manifestation of a longer period of time in the frozen condition or whether temperature and vapor pressure equilibration was not achieved after 1 hour. Pomeroy et al. (1975) have reported that the influence of duration of freezing on injury depends on whether the freezing temperature is near the lethal temperature. For instance, in wheat, survival was 100% at -6"C, regardless of the length of time frozen (1-120 Fours); at - 12'C, survival decreased from 100% after 12 hours; and at- 16"C,'survival decreased from 80% after 1 hour to 10% after 48 hours. If vapor pressure equilibration occurred, other stresses, such as grain growth, are contributing to injury. 4 . Supercooling

Siminovitch and Scarth (1 938) have shown that supercooling in both tender and hardy cells often results in intracellular freezing. When extensive supercooling occurred before ice inoculation, the degree of intracellular freezing was much more extensive in tender tissues than in hardy tissues. Olien (1964) considers supercooling to be more injurious because it promotes nonequilibrium freezing. Whereas Gusta and Fowler (1977) found that supercooling followed by freezing resulted in death at higher temperatures than when freezing was initiated at just below O'C, Andrews et al. (1974a) contend that, under conditions that induce supercooling, the cold hardiness is increased considerably. If supercooling occurs without freezing, it will be a very effective mechanism for avoiding freezing damage (Levitt, 1972). However, if freezing follows supercooling, the rate of freezing incurred by the tissue is much greater than the cooling rate of the ambient environment. Thus, the detrimental effects associated with supercooling are related to the extremely rapid rates of freezing and the resultant stresses that occur under such conditions. Although Nath and Fisher (1971) have shown that alfalfa will supercool 8'-9'C in artificial freezing tests, few studies report either the amount of supercooling or the resultant freezing rate the tissues are subjected to. Until such information is available, the degree of supercooling that can be tolerated remains to be resolved.

C. REPERCUSSIONS OF FREEZING ON THE CELLULAR ENVIRONMENT

The repercussions of the freezing process on the cellular environment of the cell and its components are numerous. These changes include the obvious decrease in temperature, the presence of ice crystals, and dehydration of the cell. There are several consequences of dehydration, which include a reduction in cell volume and surface area, an increase in concentration of solutes, precipitation of

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some salts resulting in pH changes, and removal of water of hydration of macromolecules. Mazur (1969, 1970) refers to these as solution effects and notes that all these repercussions occur as a monotonic function of temperature. There is general agreement that, under conditions of extracellular ice formation, decreases in temperature or the presence of ice crystals per se are not responsible for injury (Heber and Santarius, 1973), and that the process of cellular dehydration is the most disruptive and injurious repercussion of the freezing process (Mazur, 1970). However, dehydration results in a multitude of effects, and it is within this array that there is a great divergence in hypotheses on the mechanism of freezing damage. All the repercussions, either singularly or in various combinations, have served as the basis for mechanisms of freezing damage (see Mazur, 1969; Heber and Santarius, 1973). As mentioned before (Mazur, 1970), none is entirely satisfactory. It would appear that the major shortcoming of each lies in the attempt to explain all the manifestations of freezing. Since freezing results in a multitude of stresses, it is reasonable to assume that the overall mechanism of freezing injury is a composite of many of the hypotheses put forth and that they should not be considered as mutually exclusive.

I . Direct Effects of Temperature In general, direct effects of low temperature are not considered to be responsible for the damage incurred during freezing (Heber and Santarius, 1973). However, such conclusions can be prejudiced, because damage may result from numerous stresses, and one factor may mask or preclude manifestation by another. Generally, temperature has been deemed a minor component in studies comparing the survival of tissues in a supercooled state with those that have been frozen. However, there have been examples of how temperature can affect protein denaturation (Brandts, 1967). 2 . Ice Crystal Formation Aspects of mechanical damage and the incidence of physical abrasion of the cells have been reviewed extensively by other authors (Levitt, 1972; Heber and Santarius, 1973). Such physical damage is generally acknowledged to result from intracellular ice formation and is presumably the reason why this type of freezing is always lethal. Although the usual conclusion is that extracellular ice formation does not cause injury through physical damage of the ice crystals, Olien (1964) indicates that under certain conditions nonequilibrium freezing can result in the rapid formation of ice masses and large perfect crystals that can split the tissues and destroy cells. The structure of crystals forming between the protoplasts is considered to be very important in affecting injury. Masses of small or imperfect crystals cause little damage, but they may become more perfect and

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destructive as the temperature drops. The type of ice crystal formation may vary considerably in winter cereals, and certain cellular components can influence ice crystal formation (Olien, 1965). As early as 1906, Wiegand reported that ice formation may physically separate plant tissues.

3 . Cellular Dehydration There is general concensus that cellular dehydration is the primary cause of freezing damage. Dehydration results in multiple effects, as delineated earlier. At a given temperature, the extent of dehydration will be a function of the initial osmolality of the cell, since the temperature of the extracellular ice will determine the vapor pressure that must be achieved by removal of water. In cells with a higher osmotic concentration, less water will have to be removed to achieve vapor pressure equilibrium at a given temperature. The concentration of cellular solutes required to achieve vapor pressure has been invoked by many as the primary cause of freezing injury (see Mazur, 1970). The dehydration and resultant concentration of solutes may result in injury in a number of ways: Some indicate that the actual concentration of various toxic compounds is responsible, whereas others indicate that only the osmotic removal of water is important (see Mazur, 1970). Removal of water causes a reduction in cell size, which has been considered to be important, as it could lead to deformation of the plasma membrane. As early as 1940, Scarth et al. indicated that injury to the plasma membrane was related to plasmolysis and deplasmolysis. Wiest and Steponkus (1978) have shown that protoplasts that have been contracted in relatively high osmolalities and subsequently induced to expand by dilution of the osmoticum lyse before they regain their original size. Furthermore, the amount of injury to frozen and thawed protoplasts could be quantitatively accounted for by injury that occurs when the plasma membrane is osmotically induced to contract and expand. Both the extent and kinetics of injury in protoplasts exposed to a freeze-thaw cycle and in those subjected to osmotic manipulation are similar. These facts strongly suggest that injury to protoplasts during a freeze-thaw cycle is due to the same stresses of contraction and expansion that result from osmotic manipulation in the absence of ice. C. R. Olien (personal communication) has indicated that such an agreement is to be expected, because when isolated protoplasts are frozen in an aqueous medium, the major stress is due to desiccation by the osmotic removal of water.

D. MANIFESTATIONS OF FREEZING INJURY

The visual manifestations of freezing injury-a darkened, water-soaked, flaccid appearance-are very apparent immediately following thawing. The gross disruption of cellular architecture is evidenced by extremely leaky cellular mem-

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branes. It is unfortunate that the indications of freezing injury are so vivid, so sudden, and so easily measured by techniques such as the release of electrolytes (Dexter et a l . , 1932), because inquiries into the manifestations of freezing injury at a more fundamental level have been stifled. Although there is a general concensus that freezing injury results in the loss of semipermeability, this is, at best, a very broad generalization, as there are many ways in which the loss of semipermeability can be achieved.

I . Injury at the Tissue Level In considering cold hardiness in relation to plant morphology, it is generally agreed that the crown is the most vulnerable (Kneen and Blish, 1941), as survival of both cereal grains (Pauli, 1960) and forage crops (Jung and Larson, 1972) is dependent on the survival of regenerative and conductive tissues. Within the crown, three distinct regions can be distinguished on the basis of major differences in the tissue: the upper region, containing the apical meristem; the basal region, where large vascular elements of the mesocotyl and roots enter and continue toward the central transitional region; and lateral regions, where much finer vascular elements branch out from the central region to leaf sheaths (Olien, 1974b). Crown survival depends on the extent of injury in these three regions, and the type of freezing process that can occur varies among the regions (Olien, 1964). Generally, equilibrium freezing will occur in the upper region, unless the moisture content is excessively high, and nonequilibrium freezing is usual in the basal region, unless the moisture content is exceptionally low. The different types of freezing processes can occur simultaneously in the different regions. Even though the crown is the most critical for survival, Jung and Larson (1972) state that cold tolerance is usually greatest for crowns, intermediate for roots, and least for leaves. This statement is based on the decreased incidence of freezing temperatures in addition to actual tolerance. With respect to individual tissues of alfalfa, the stelar tissue of roots is considered more tolerant than cortical tissue, as the latter develops little cold tolerance (Jung and Larson, 1972). 2 . Injury at the Cellular Level In recent years, it has been commonly inferred that the primary cause of freezing injury is damage incurred by cellular membranes, especially the plasma membrane. Although freeze-induced membrane damage has received widespread attention since the late 1960’s, it is not an entirely new revelation (Levitt and Dear, 1970). As early as 1912, Maximov concluded that freezing injury was due to damage to the plasma membrane. A resurgence in the view pointing to the plasma membrane as the site of freezing injury was provided by

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Levitt and Scarth (1936a,b) and Siminovitch and Scarth (1938). In the ensuing years, these observations gradually lost their significance, as attention was diverted to soluble cytoplasmic components as the site of freezing injury. Fortunately, in the late 1960’s there was a renewed emphasis on cellular membranes as the site of freezing injury (Heber, 1967, 1968; Siminovitch et al., 1968; Mazur, 1969, 1970; Olien, 1967a; Heber et al., 1973; Levitt and Dear, 1970; Sakai and Yoshida, 1968). However, in spite of this renewed interest, characterization of membrane damage did not progress much further than the acknowledgment that freezing results in the loss of semipermeability. This is, at best, a very broad generalization, but it has served as the basis for evaluating the various effects of freezing and speculating on mechanisms of injury. Thus, all too frequently, the multiple stresses arising during freezing have been interpreted with respect to a single general type of strain-the loss of semipermeability. In the early 1960’s, interest in membranes was stimulated by studies of alterations in chloroplast membranes in relation to freezing injury (Heber and Santarius, 1964). Numerous papers by Heber and co-workers (Heber, 1967, 1968, 1970; Heber and Emst, 1967; Heber and Santarius, 1964, 1967, 1973; Heber et al., 1971, 1973; Santarius, 1971, 1973a,b; Santarius and Heber, 1970, 1972)provided considerable insight into the effects of freezing on the function of chloroplast membranes. Subsequently, Garber and Steponkus (1976a) and Steponkus et al. (1977) extended this work, providing information on the repercussions of freezing on chloroplast thylakoid structure and function at the molecular level. Heber (1967) attempted to localize the site of freezing injury and concluded that uncoupling of photophosphorylation was a result of altered permeability of membranes. A similar conclusion was reached by Uribe and Jagendorf (1968). However, Garber and Steponkus (1976a) demonstrated that the situation was considerably more complex-ven though their attention was restricted to the effects of freezing on photophosphorylation as measured by light-induced proton uptake (see Jagendorf, 1975). Following a slow freeze-thaw cycle, there were three lesions in light-induced proton uptake: loss of plastocyanin, a protein in the electron transport chain; loss of chloroplast coupling factor, the protein responsible for coupling ATP synthesis to electron transport; and loss of osmotic responsiveness. Delineation of the freeze-induced damage to light-induced proton uptake into three separate lesions clearly demonstrated the complexity of freezing on biological systems. If this system can be considered as a simplification of the situation that exists in comparison with intact cells, the dangers of making inferences regarding mechanisms of freezing injury from observations of survival are evident. The question of what constitutes plasma membrane damage at the molecular level remains to be answered, although several recent reports have addressed the question (Palta et al., 1977a,b; Steponkus and Wiest, 1978; Wiest and Stepon-

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kus, 1978). In these reports, questions of what constitutes plasma membrane damage is approached by studying the plasma membrane in siru in either tissue slices or isolated protoplasts. Whereas the work of Palta et al. (1977a,b) is concerned with alterations in plasma membrane permeability following sublethal injury, the work of Wiest and Steponkus (1978) is concerned with the damage resulting in rupture of the plasma membrane. As early as 1940, Scarth et al. indicated that injury to the plasma membrane occurred during deplasmolysis. Wiest and Steponkus (1978) determined that, on thawing, the degree of expansion that can be tolerated before lysis occurs is dependent on the degree of contraction incurred during the prior freeze-induced contraction. It was apparent that some membrane alteration occurred when the protoplasts were contracted, which subsequently limited the protoplast size that could be achieved on dilution. The contraction-inducedalteration in itself did not result in lysis, but affected the resilience of the plasma membrane. Furthermore, there was a critical increment in surface area that could be tolerated, which was independent of the degree of contraction. The fact that injury was correlated with the surface area expansion of the plasma membrane immediately suggests that injury is related to the disruption of intermolecular forces occumng in the plane tangent to the membrane surface. As lysis was correlated with an absolute increase in surface area, this implied that disruption of the membrane requires the same amount of work regardless of the surface area. This fact suggests that the work required for disruption of the plasma membrane is equal to the magnitude of the weakest intermolecular forces joining the membrane together and is constant. The preceding work demonstrates the nature of a specific lesion in the plasma membrane that develops as a result of a specific stress that occurs during extracellular freezing-desiccation by the osmotic removal of water (Olien, 1967a; see Section 11,C,3). Such a lesion could be wholly responsible for injury incurred in tender tissues at relatively high subfreezing temperatures when the majority of water is removed from the cells. However, other lesions would be more likely to appear in tissues that are injured at lower temperatures, where only a small fraction of the initial water content is remaining and can be removed by lowering the temperature. Elucidation of these lesions requires that the stresses be imposed in a singular fashion, which is sometimes difficult. However, such information on the nature of both the stress and the resultant lesion that occurs at any given time during freezing is needed in order to determine the mechanism by which plants acclimate. 111. Environmental Factors Affecting Cold Hardiness

Temperate-zone crop plants exhibit an annual periodicity in their tolerance of freezing temperatures; in the winter they are able to withstand freezing temperatures of -30°C or lower, but in the spring or summer they are susceptible to

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freezing temperatures and are easily killed by temperatures of -3” to -5°C. The increase in cold hardiness during the fall is referred to as cold acclimation, and the loss of hardiness in the spring is termed deacclimation. The cold hardiness of a given species is dependent on two factors: (a) the inherent or genetic capacity of the species to acclimate in order to withstand freezing temperatures, and (b) the conditioning or expression of this heritable capacity. Plants lacking the genetic capacity are considered unhardy orfrost-sensitive species; those that possess the genetic capacity but have not experienced the proper cues for its expression are considered to be in an unhardy Condition; and those that possess the genetic capacity and have received the proper environmentalcues are considered to be in a hardy condition. Heslop-Harrison (1969), in discussing how development and differentiation determine yield of economic plants, introduced the subject with the following eloquent statement: “What is incontestable is that development and differentiation are manifestations of gene function, so that the fundamental problem can at least be defined: it is to understand how gene action is governed in ontogeny so as to give an orderly expression to the potentialities attained during the evolutionary history of a species, producing an organism that is harmoniously coordinated both within itself and with the environment. The process of cold acclimation and the development of cold hardiness of a species is a prime example of the interaction between a plant and its environment as outlined in this statement. The problems of cold hardiness that are now confronting agronomists concerned with world food production are due to the fact that man, out of necessity, is disturbing the “orderly expression” of, “the potentialities attained during the evolutionary history of a species,” so that at times the organism is no longer “harmoniously coordinated. . . with the environment. It is from this perspective that the problems of cold hardiness and the environmental cues that influence cold acclimation should be viewed. When one is considering how plants respond to the environmental cues, it must not be assumed that all plants should respond similarly to the same cues. Thus, what are considered to be “proper,” “optimum,” or “necessary” environmental cues for one species may vary considerably for different cultivars or ecotypes within that species. It is within this context that the great diversity of reports in the literature should be viewed. Furthermore, although the environmental cues serve to synchronize plant development with the environment, the plant’s responsiveness has taken centuries to evolve; and freezing injury in cultivated species can result from any factor that disrupts this synchrony. Some varieties may not be responsive to the surrounding environmental cues or may not respond rapidly enough; some may not develop a sufficient degree of hardiness; and some may deacclimate too rapidly. Each of these factors may arise because individual varieties are being introduced into areas that are vastly or even slightly different from their natural habitat, where centuries of selection pressures have evolved those individuals most closely and appropriately ”

”

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synchronized with the prevailing environment. Although it is the burden of the breeder to work within these confines, it is the responsibility of physiologists to provide understanding and direction for the new horizons in improving cold hardiness of a species. Cold hardiness may be influenced by radiation, temperature, photoperiod, precipitation, and stage of development of the plant, with different optimum conditions for different species and cultivars. Suneson and Peltier (1938) characterized the seasonal progression of cold hardiness of winter wheat in relation to environmental factors during a 6-year period. Initially, high daily temperature maxima in conjunction with high radiation and shortened photoperiods were conducive to increased hardiness. At this time, xeric conditions favored acclimation. Subsequently, exposure to sustained low temperatures resulted in maximum hardiness, but the actual level was dependent on the preceding stage. Finally, a decrease in hardiness was associated with the warmer temperatures of spring. In considering aspects of the environment that are conducive to acclimation, this interplay and progression must be kept in mind in regard to the effects of temperature, light, and moisture.

A. TEMPERATURE

Temperature is the key environmental parameter for synchronizing a plant's capacity to withstand freezing temperatures with the prevailing ambient temperatures (Olien, 1967a; Paulsen, 1968; Svec and Hodges, 1972a; Gusta and Fowler, 1976). Low, above-freezing temperatures are conducive to an increase in hardiness in the fall, and warm temperatures are responsible for the decrease in the spring. Generally, it is considered that most plants will acclimate as temperatures are gradually lowered below 10°C (Alden and Hermann, 1971). For instance, winter cereals are considered to be in a tender state if plants have been growing at a temperature above 1O"C, with optimal temperatures for acclimation near 3°C (Olien, 1967a). Maximum cold acclimation of alfalfa and other perennial legumes develops about the time the soil freezes (Hodgson, 1964). However, during acclimation the progressive decline in temperatures from the relatively high temperatures in early fall, followed by the low, above-freezing temperatures in late fall and early winter, followed by freezing temperatures in winter, is extremely important in the acclimation process. Each stage has a distinctive role in the overall process of acclimation with respect both to succeeding stages and to the influence of other environmental factors. This is an important point to remember in attempting to define precisely the role of temperature in the acclimation process. In cereal grains, noticeable increases in hardiness occur in a few days at 3°C with the maximum occumng in about 3 weeks (Olien, 1964). Longer periods at

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above-freezing temperatures result in a gradual loss of hardiness, even under apparently optimum conditions of nutrition and light (Andrews, 1958; Roberts and Grant, 1968), a factor alluded to by Molisch in 1897. However, if after the hardening period the plants are maintained at temperatures slightly below freezing, hardiness will be retained (Olien, 1967a). Similarly, Andrews er af. (1974b) found that diurnal freezing did not significantly increase maximum hardiness but reduced the rate of loss of hardiness after the maximum had been attained. This fact would probably account for the report of a specific freezing temperature requirement for hardening of winter wheat seedlings (Siminovitch er al., 1967). In this case, seedlings grown in the light at 2°C increased in hardiness after transfer to -3°C in the dark for 2 weeks. However, the comparison was made with seedlings maintained at 2°C for 8 weeks, during which time hardiness may have been declining. On this basis, one would have to question whether there are two separate phases of acclimation-one at above-freezing temperatures and one below, as was claimed (Siminovitch er af., 1967). The importance of the progression of temperatures can be supported by the fact that Pomeroy er af. (1975) found that high levels of hardiness can be rapidly induced in 4-6 days in wheat if the hardening temperatures are preceded by warm temperatures. Previous reports (Pomeroy and Fowler, 1973; Andrews et af., 1974b) showed that 6-8 weeks at 2"-4°C were required for maximum hardiness.

B . LIGHT

Many authors, from the very earliest workers to the most contemporary, have considered light to be a major factor influencing cold acclimation. In 1899, Toporkov (cited by Vasil'yev, 1961) concluded that intense light is one of the major factors promoting the development of resistance to low temperatures, and in 1974, Andrews er al. (1974b) indicated that levels of cold hardiness in winter wheat plants are directly associated with the length and intensity of daily light exposure. Although the involvement of light in the cold acclimation process has endured the test of time, reports in the literature appear, at times, to be conflicting. For instance, Dexter (1933a,b) is often cited to support the concept that winter annuals are incapable of cold acclimation in the absence of light, but Tysdal (1933) found that light intensity was important only when it reached a minimum so that it weakened the plant. Andrews (1958) states that, in germinating seeds, hardiness can be induced in the dark. In this instance, the apparent differences in reports regarding the requisite for light can be attributed to the stage of development the plants are in at the time of acclimation. Thus, in germinating seeds the endosperm is a source of energy, so that acclimation can occur in the dark, but in older seedlings the endosperm is no longer an effective source of reserves, and there is a light dependency. Even Dexter (1933a,b)

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concluded that the role of light was only to act as a source of photosynthate, and in plants such as alfalfa, which have large reserves, cold hardiness can increase in the dark. Rather conclusive evidence that light per se is not a requirement of the acclimation process is supported by the numerous reports that the light requirement can be replaced by incubation on sugar solutions (Tumanov and Trunova, 1963; Steponkus and Lanphear, 1967b). Clarification of the point that light functions to provide a source of photosynthates still leaves an additional area of conflict with respect to whether the photosynthates produced are merely a source of respiratory substrates enabling the acclimation process to proceed or whether in fact a portion of the photosynthates results directly in increased hardiness. This point will be addressed in a subsequent section (Section V). Steponkus and Lanphear (1968) interpret the low light saturation of the acclimation response to be due to the fact that the requirements of the cold acclimation process are only a small proportion of the total mount of the photosynthates produced. Similarly, Hiinsel (1972) indicates that the endosperm might, under certain conditions, exert a decisive influence on the degree of frost resistance and on seedling survival. In young seedlings, light-dependent processes, as well as mobilization of endosperm reserves, are important for optimal hardening, and light can compensate for the grain effect more effectively with respect to hardening than with respect to dry matter production. A second area of apparent conflict in the literature in regard to the role of light in the acclimation process relates to whether light functions in a photoperiodic role in addition to a photosynthetic role. It is commonly accepted that short photoperiods stimulate acclimation, partly because of the annual decline in photoperiod that is coincident with the time of natural acclimation, but also because of reports that some species fail to acclimate under long photoperiods (Hodgson and Bula, 1956). However, Trunova (1965) reports that hardiness of winter wheat increases more rapidly under long light exposures (16-24 hours) than under short light exposure (8-12 hours). Paulsen (1968) also reported that winter wheat hardened to the greatest extent under a long photoperiod and a decreasing temperature, and Rimpau (1958) observed a direct correlation between length of the critical photoperiod and freezing tolerance in wheat. Paulsen (1968) suggested that low light intensities under artificial conditions may be the reason for reports that long photoperiods favor acclimation, whereas under field conditions short photoperiods promote hardiness. Such an explanation is only partially correct; the distinction should be based on whether the species or cultivar in question is photoperiodically responsive in relation to growth cessation or induction of dormancy in those species with a true physiological rest period. Although Andrews (1960b) reported an apparent photoperiodic response of wheat, the results are difficult to interpret, owing to a temperature interaction resulting from the increased light duration. More frequently, the reports indicate that short photoperiods are not required for acclimation of cereal grains

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(Trunova, 1965; Paulsen, 1968; Rimpau, 1958), but short photoperiods are required for acclimation of certain perennials such as alfalfa (Bula ef al., 1956; Hodgson, 1964; Hodgson and Bula, 1956). This difference may be due to the selection for photoperiodic insensitivity in winter cereal grains, which may be of questionable value (Johnson et ul., 1970). According to Young and Feltner (1966), winter annuals have no permanent period of dormancy, and growth processes cease only on exposure to low temperatures. A photoperiodic stimulation of cold acclimation in photoperiodically responsive cultivars underlines the statement made by Heslop-Harrison (1969) in regard to the synchronization of the plant with its environment and the fact that it is dependent on the potentials attained during the evolutionary history of the species. Thus, Hodgson and Bula (1956) found that hardy but southern ecotypes of sweet clover (Melilotus spp.) failed to develop maximum hardiness in Alaska, even though they were exposed to normally acclimating temperatures. Similarly, Bula et al. (1956) found that northern ecotypes of alfalfa developed resistance earlier under a 12-hour photoperiod and at a faster rate than southern ecotypes. Medicagofalcata, a far-northern ecotype, developed cold resistance equally well under long, normal, or shortened photoperiods;M. sativa, cultivars Moapa and Caliverde, failed to develop any appreciable degree of hardiness under any photoperiod, whereas M . sativa cv. Ranger increased in hardiness in response to shortened photoperiods. Thus, in Alaska cold resistance must be developed by mid-October, and hardening must occur under photoperiods of 15 hours (midAugust) to 11 hours (early October). It would appear that both southern ecotypes and M. falcatu are photoperiodically insensitive, but the latter can become acclimated under any photoperiod, whereas in the southern ecotypes appreciable acclimation does not occur. Only in the intermediate temperature varieties such as Ranger was photoperiod instrumental in synchronizing the plant with the environment. Thus, in the case of perennial forage species, photoperiodic stimulation of acclimation influences the hardiness of plants with respect to the timing of the onset of acclimation, and the genetic potential for cold acclimation is achieved only after exposure to the photoperiod to which a cultivar is adapted (Hodgson, 1964). Thus, in these species photoperiod may be as important as temperature in influencing cold acclimation.

C . MOISTURE

Conflicting reports exist for the role of moisture in hardiness. In regard to soil moisture, Salmon (1933) and Tysdal(l933) indicated that soil moisture acts as a buffer against sudden temperature changes. However, Gruentuch (1935) specifically pointed to high soil moisture as a factor reducing the degree of plant hardening. Earlier, Newton (1924) found that a reduction in available water content within

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the plant was the most important quantitative change associated with hardiness. Not only is decreased moisture content associated with increased survival, but Gusta and Fowler (1976) concluded that in dehardening studies there was a high positive correlation between cold survival and water content of crowns. However, the greatest increase in water content in both artificially and naturally acclimated crowns occurred during the first 3 days of dehardening and then became constant or decreased slowly, whereas deacclimation proceeded almost linearly for 15 days. Metcalf et al. (1970) found that a slight change in moisture content of winter cereal crowns had a significant effect on the lowest temperature that plants could survive. Although other environmental parameters affect the hardiness of the plants through their interaction with the hardening process and the development of tolerance to the stresses of freezing, Olien (1964) and Suneson and Peltier (1934a,b) consider that changing moisture content greatly affects the freezing process. Thus, whereas light and temperature effects on acclimation are probably mediated through the development of resistance, moisture content directly affects the stresses that the plant must withstand. IV. Effect of Developmental Stage on Cold Hardiness

Given that several factors affect the freezing process and resultant stresses and that several environmental factors alter the plant’s resistance to these stresses, the plant must be viewed as the integrator of these opposing series of events. The effectiveness of the integration will determine the incidence of injury. The stage of development can influence both the stresses incurred and the resistance acquired. Plant age, or, more properly, the stage of development, appears to have a profound effect on the plant’s capacity for both acclimation and maintenance of hardiness. However, many studies that have attempted to elucidate these aspects have been confounded with other factors. Field studies in which the effect of sowing date is considered in relation either to hardiness at different times during the winter (Andrews ef al., 1960) or to overall winter survival (Roberts and Grant, 1968) confound stage of development with the duration of the acclimation period. Nevertheless, interesting observations have been made from such studies that cannot be explained by differences in the duration of the acclimation period. For instance, Roberts and Grant (1968) observed that relatively old plants, which had been growing 11 weeks or more before growth cessation, experienced more winter injury than did plants that were seeded at a later date. Similar results were obtained when cold hardiness, rather than winter hardiness, was determined (Andrews et a!., 1960). Injury to plants grown for 16 weeks in the fall before exposure to a freezing temperature was greater than injury to younger plants. No

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satisfactory explanation for this decreased hardiness of mature plants has been proposed. Many controlled experiments have been performed by sowing dry or recently imbibed seeds directly at acclimating temperatures and determining hardiness as a function of time (Andrews et al., 1974a). Prior to imbibition, a dry seed is capable of surviving exposure to -196°C. This hardiness decreases during 5 days at 2°C or 24 hours at 24°C (Andrews et al., 1974a). This early minimum in seedling hardiness may be due to an imbibition-induced alteration of the freezing process or to an effect of the initiation of growth processes in the seed, or to both. An influence of the former would be through increased water content. An influence of the latter appears to occur in the case of dormoats. Andrews and Burrows (1974) have observed that field survival of a dormoat crop, treated so as to induce secondary dormancy, survived the winter better than an untreated crop. Although the seeds of the former group had obviously become imbibed during the fall, as evidenced by the ability of the untreated seeds to germinate, the secondary dormancy prevented germination and thus allowed the crop to survive the rigors of winter. Following the imbibitiodgermination-induceddecline in hardiness is a rather steady increase in hardiness of cereals grown at low temperatures for about 3-6 weeks (Andrews et al., 1974b). The exact stage of development at which this maximum occurs, as well as its duration, is dependent on the specific variety (Roberts and Grant, 1968) and can be used to distinguish genetic differences between varieties (Andrews, 1958). Klages (1926a,b) demonstrated that young winter wheat seedlings exhibited the greatest cold acclimation potential before achieving the three- to four-leaf stage. Suneson and Peltier (1934b) and Peltier and Kiesselbach (1934) reported similar results in seedlings of oats, barley, and wheat. However, Roberts and Grant (1968) reported a maximum in winter hardiness of winter wheat at the four- to six-leaf stage of plants grown in the dark. Similarly, maximum hardiness was observed in the four- to six-leaf stage in rye (Andrews, 1960b) and barley (Dantuma and Andrews, 1960). When seedlings are grown in the dark, maximum hardiness is achieved when the coleoptiles reach 45-55 mm in length (Andrews, 1960a). In general, hardiness of various legumes is minimal when they are forming the first pair of permanent leaves (Steinbauer, 1926) and subsequently increases with age up to 60 days (Peltier and Tysdal, 1932). However, although this is true for alfalfa and red clover, Tysdal and Pieters (1934) found that hardiness of lespedeza decreases after the two-leaf stage. Thus, lespedeza cultivars were distinctly hardier than red clover or alfalfa in the unhardened cotyledonary stage, whereas in the hardened cotyledonary stage the reverse was true. In cereals, the second decline in hardiness has been attributed to the exhaustion of endosperm reserves (Suneson and Peltier, 1934a,b; Peltier and Kiesselbach, 1934). Suneson and Peltier (1934b) observed that the youngest seedlings exhib-

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ited the greatest cold acclimation potential, and seedlings in the transition stage between endosperm dependence and tillering exhibited the least potential. Others attribute the loss of hardiness to the completion of the vernalization process (Andrews, 1960a). However, Voblikova (1965) cited several reports indicating that vernalization was completed in 45-60 days, whereas cold hardiness was maintained for several months. However, hardiness determinations were made at 2-month intervals, and thus he was unable to determine precisely the time at which the decline in hardiness began. Vasil'yev (1961) conducted a series of enlightening studies to determine the effect of vernalization on tissue hardiness. Seeds are capable of completing vernalization when held at 0°C for 40-50 days, depending on the variety. Oneweek-old seedlings grown from vernalized seeds were found to be less injured by exposure to - 10" to -12°C than were seedlings of the same age grown from nonvernalized seeds. On the other hand, when the hardiness of plants in the tillering stage was compared, it was observed that plants grown from vernalized seeds were more susceptible to freezing temperatures than were plants grown from nonvernalized seeds. Vasil'yev (1961) concluded that the vernalization process per se does not affect tissue hardiness but, rather, that vernalization affects the growth rate of the plants. The development of plants grown from vernalized seeds appeared to be slower initially than that of nonvernalized plants. However, at about the four-leaf stage, the growth rate of vernalized plants was much higher than that of nonvernalized plants. Thus, the possibility exists that this increase in the growth rate is the primary cause for the decline in hardiness-perhaps by depleting the already diminishing endosperm reserves. Further evidence to support this view comes from observations that plants held continuously at -4°C for 22 weeks after exposure to 2"-5"C for 12 weeks retained a high degree of hardiness, even though vernalization had been completed (Voblikova, 1965). The possibility exists that vernalization predisposes plants to a more rapid exhaustion of endosperm reserves and in this way has an indirect effect on plant hardiness. However, a rigorous attempt to demonstrate conclusively the cause of this second decline in the cold hardiness of winter cereals has yet to be made, and some reports indicate that the decline in hardiness may not be associated with decreases in stored sugars (Tsenov, 1972). V. Physiological and Biochemical Aspects of Cold Acclimation

The majority of research concerned with cold hardiness of higher plants has dealt with the biochemical changes that occur during the period of cold acclimation. It would not be too great an exaggeration to state that almost all cellular constituents have, at one time or another, been analyzed with respect to a possible involvement in the cold acclimation process. In spite of the extensive amount

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of work and the overwhelming number of publications in this area, there is little agreement on the significance of the measured changes-a fact that has been cited by several review authors (Smith, 1968; Mazur, 1970; Alden and Hermann, 1971; Levitt, 1972; Heber and Santarius, 1973). Several factors have contributed to the dilemma that one of the most extensively studied areas of cold hardiness is the least understood. First, in much of the work there is a prevailing attitude that a single compound is responsible for cold hardiness and serves as a basis for the innumerable correlative studies. Associated with this attitude is the concept that, the greater the quantitative increase (or decrease) in a given compound, the more likely it is responsible for cold hardiness. In many instances, the correlation coefficient between hardiness and a cellular component in either a series of different cultivars or different species, or at different times of the year, has served as justification for the inclusion or exclusion of a particular component in the cold acclimation process. One must be very cautious of such reasoning, for only if the particular compound were the product of the rate-limiting step in the entire cold acclimation process would such a correlation exist. Second, there tends to be the assumption that freezing injury is the result of the same stress either in all plants or, more important, within the same plant at different stages of acclimation. Although the work of Olien (1967a) has shown evidence to the contrary, such an attitude is derived from the delineation of the various stresses that occur during freezing (see Levitt, 1972). Too often it is inferred that different types of freezing stresses are separate and distinct events that are mutually exclusive in a given plant. Rather, it would be more appropriate to view the stresses that arise during freezing as a sequential series of events. They may be envisioned as successive stress barriers, and survival depends on the successful and sequential avoidance or tolerance of each individual stress barrier. Hence, cold acclimation can be envisioned to involve a sequential series of alterations that would allow each stress barrier to be overcome, rather than one particular alteration being responsible for the total increase in hardiness. With such a view, it is easy to understand why numerous biochemical and physiological changes may be associated with the cold acclimation process, rather than one single biochemical event. Although little would be gained from yet another cataloguing of these reports, the significance of the various physiological and biochemical alterations can be assessed from various perspectives. Are the changes associated with other alterations in growth and development that coincide with cold acclimation and depend on some of the same environmental cues as cold acclimation? Are the changes merely occurring in response to the prevailing environment without any causal relationship to the cold acclimation process? Are the changes directly instrumental in either circumventing or tolerating the various stresses that occur during

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freezing, or are they only preliminary metabolic changes that precede the alterations that are directly involved? Rather than present a comprehensive listing of all changes, attention will be given to certain biochemical and physiological changes that serve to illustrate these points. Of ultimate concern is the elucidation of the changes that result in either preclusion, circumvention, or tolerance of the stress barriers that can arise during freezing.

A. BIOCHEMICAL ALTERATIONS FROM A DEVELOPMENTAL PERSPECTIVE

As was previously mentioned, cold acclimation is occumng during a period of very dynamic and dramatic fluctuations in the ambient environment. In addition, the cold acclimation process is only one of several developmental events that are occurring during this period. Cold acclimation is preceded by the slowdown or cessation of growth, the onset of dormancy, and the development of tillers or rhizomes, to mention only a few developmental processes. In addition, in cereal grains, the process of vernalization is occurring during the winter period. In such a developmental setting, is there any question that alterations in plant hormones, nucleic acid components, or protein complement might be detected? Thus, reports of alterations in RNA and DNA (Jung ef al., 1967; Shih ef al., 1967) are not unexpected. In fact, it would be very surprising if such changes did not take place. Similarly, the appearance of altered electrophoretic patterns of watersoluble proteins from acclimated alfalfa roots (Coleman er al., 1966; Gerloff et al., 1967) or from rhizomes of Bermuda grass (Davis and Gilbert, 1970) or from leaves of perennial ryegrass (Draper and Watson, 1971) is not unexpected. Although vernalization may influence the cold acclimation potential (Vasil'yev, 1961; Voblikova, 1965; Vincent, 1972), very few studies have considered the biochemical similarities or dissimilarities between the two processes. One exception is in the area of lipid alterations. Redshaw and Zalik (1968) demonstrated that, although noticeable differences in lipids were found after exposure to low temperatures, both spring and winter varieties exhibited similar trends in polar and neutral lipids and the constituent fatty acids. Subsequently, Thomson and Zalik (1973) concluded that changes in lipids that occur on exposure to low temperatures are not unique to vernalization. However, de Silva et al. (1975) studied lipid alterations in two near-isogenic lines of wheat (spring and winter) and observed that higher levels of phospholipids were found in the winter genotype than in the spring genotype. Also, in wheat grown at 2"C, the lipids of the winter type exhibited larger increases in linoleic and linolenic acids than did the lipids of the spring genotype grown at the same temperature. It was further suggested that these increases may be associated with the vernalization gene.

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Although the data are not conclusive, they serve to point out that some biochemical changes associated with the vernalization process may occur during the period of cold acclimation. B. BIOCHEMICAL ALTERATIONS FROM AN ENVIRONMENTAL PERSPECTIVE

Of prime concern is whether alterations in biochemical constituents are associated with the cold acclimation process, or whether they are merely manifestations of metabolic adjustments in response to low temperatures. Such metabolic adjustments in response to low temperatures is a common response in many organisms that do not undergo cold acclimation. An important and relevant example of such a low-temperature metabolic adjustment relates to qualitative changes in lipids and constituent fatty acids. Effects of temperature on the fatty acid composition of higher plants (Harris and James, 1969a,b; Hitchcock and Nichols, 1971). animals (Hilditch and Williams, 1964), and several microorganisms (Weete, 1974) have been well documented. In this diverse range of organisms, low temperature will generally stimulate the accumulation of unsaturated fatty acids-ven though the ability to survive freezing is not a universal phenomenon. However, since such a change coincides with the period of cold acclimation, it has frequently been inferred to be associated with the cold acclimation process. A positive correlation between lipid content and hardiness was reported by Sinnott in 1918; his rather comprehensive survey included more than 300 species of 100 genera over a 3-year period! Although many such early observations employed histological techniques that may have resulted in erroneous interpretations (Alden and Hermann, 1971), numerous studies using other techniques have since established this correlation (Levitt, 1972). Although the association of lipids and constitutive fatty acids with cold hardiness has had a long history, a renewed interest occurred in the early 1960’s and continues to this date. Such interest was stimulated by the initial reports of Lyons el al. (1964) that the degree of unsaturation of fatty acids of mitochondrial lipids was associated with chilling injury. One of the first investigations on agronomic crops subsequent to the report of Lyons er al. (1964) was with alfalfa (Gerloff et al., 1966). The fatty acid composition of root tissues of a nonhardy cultivar (Caliverde) and a hardy cultivar (Vernal) increased approximately twofold during the fall, and the increase was the result of a preferential increase in polyunsaturated fatty acids. Although the increases were similar in both cultivars, it was concluded that the large increase may play a role in acclimation. Using the same two cultivars, Kuiper (1970) demonstrated that at lower growth temperatures (15°C) changes in the

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lipid composition also occurred, as manifested by increases in the mono- and digalactosyl diglyceride, phosphatidyl choline, and phosphatidyl ethanolamine fractions. Furthermore, the hardier cultivar, Vernal, exhibited a higher percentage of these components than did the less hardy cultivar, Caliverde. Although the lowest temperature used (15°C) was considered to be conducive to hardening, no hardiness determinations were made, and it is extremely doubtful that cold acclimation was occumng. However, Grenier et af. (1972) demonstrated that total lipids in alfalfa roots increase during acclimation. Subsequently, it was shown that fatty acids increased in unsaturation, particularly in linoleic acid (18:2) (Grenier and Willemot, 1974). It was suggested that linoleic acid synthesis and hardening were related and that the mechanism suggested by Lyons et al. (1 964) may explain, in part, the varietal differences in hardiness of alfalfa. At this time, reports indicated that significant increases in the phospholipid content and a marked increase in linolenic acid (18:3) content occurred in wheat seedlings grown at 2"C, as compared with seedlings grown at 24°C (de la Roche et al., 1972). It should be noted that, in order to have material at a comparable stage of morphological development, the 2°C seedlings were 5 weeks old, whereas the 24°C seedlings were 72 hours old. In any case, the observations of increased lipid content and unsaturation were similar to those for alfalfa, although the increase in unsaturation was due to increased linolenic rather than linoleic acid. de la Roche et al. concluded that increased synthesis and unsaturation of fatty acids may contribute to increased freezing resistance. Membranes containing lipids with higher proportions of unsaturated fatty acids were viewed as being more fluid and less likely to be irreversibly damaged by freezing temperatures. They also considered that higher unsaturation increases membrane permeability as reported by Lyons and Asmundson (1965). In a subsequent paper, the increase in unsaturation was considered to be the result of altered fatty acid desaturase activity rather than a preferential synthesis of individual phospholipids (de la Roche et al., 1973). In 1974, Miller et al. considered the lipid composition of mitochondria of several hardy and unhardy cultivars of wheat with respect to total lipid content, fatty acid composition, respiratory activity, and electron spin resonance behavior. Although linolenic acid content increased after growth at 2"C, the increase in total unsaturation in all four cultivars, both hardy and unhardy, was quite similar. In addition, three temperature-dependent structural transitions, identified by electron spin resonance, occurred at lower temperatures in the seedlings grown at 2°C. Because of the lack of any significant differences in both of these parameters in either hardy or unhardy cultivars, it was concluded that the ability to withstand freezing at low temperatures could not be accounted for by lipid or functional changes in the mitochondria1 membrane. Although this might be interpreted to mean that lipid changes in membranes other than mitochondria may be related to cold acclimation, a subsequent paper (de la Roche el al., 1975)

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concludes that the increase in unsaturation is only a low-temperature response. In this study, changes in the lipid and fatty acid constituents were measured in the four different cultivars of varying hardiness in an attempt to dissociate changes due to low temperature from those related to cold acclimation. In all cultivars there was a uniform stimulation of linolenic acid synthesis, which resulted in a net increase in the unsaturation of membrane lipids. Since the acclimated plants of the different cultivars ranged in hardiness from -5°C to -18”C, it was concluded that the increase in linolenic acid per se was not a primary factor in cold acclimation between -5°C and -18°C. At this time, Willemot (1975) directed his efforts to wheat and concluded that increased phospholipid synthesis was not a prerequisite to hardening in winter wheat; however, in a subsequent paper (Willemot et al., 1977) he still maintained that varietal differences in frost hardiness may be related to changes in fatty acid content in alfalfa but not in wheat. This stance was based on additional work by Grenier et al. (1975), who studied the incorporation of I4C-acetateinto lipids of alfalfa roots. It is interesting to note, though, that Willemot (1977) later concluded that increased unsaturation of fatty acids is probably an important part of the mechanism of cold adaptation-even in winter wheat. Treatment of winter wheat plants with a derivative of pyridazinone (BASF 13-338) 36 hours before cold acclimation completely inhibited both the accumulation of linolenic acid in the roots and any increase in cold hardiness. The authors were satisfied that the failure to acclimate was not a secondary effect of phytotoxicity. The above reports are presented to illustrate the oscillations that exist in the interpretation of biochemical changes occurring during cold acclimation. Actually, “fluidity in interpretation’’would be a more aproposphrase! Usually such oscillations are the result of differingopinions of different investigatorsworking with different species. However, in this case both groups were working with the same species. Furthermore, while one laboratory (de la Roche) has apparently made a 180-degreechange from their initial stance that changes in unsaturation were related to cold acclimation, the other (Willemot) has also made an apparent 180-degree change in their stance-but from an initial point of concurrence with the conclusion that changes in unsaturation were not related to cold acclimation of wheat. Although this appears to be a somewhat bewildering dilemma, there are some subtleties in the terminology in the recent papers of the two groups that bear further discussion. For example: de la Roche et al. (1975) stated that “the increase in linolenic acid per se is not a primary factor in cold hardening, at least at temperaturesfrom -5” to -18°C . . .” Singh et al. (1977) stated: “. . . both unsaturation and bulk fluidity of the isolated lipids from these plants bear little relationship to their degree of freezing tolerance. ” Willemot et al. (1977) stated: “The lack of differences between fatty acid profiles of the two cultivars rules out the explanation of varietal diferences on the basis of major changes in fatty acid unsaturation.” And Willemot (1977) stated: “It is possible that

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linolenic acid accumulation is a prerequisite to hardening, but that all cultivars have acquired this characteristic and that less hardy cultivars have their frost resistance limited by otherfactors. ” Thus, if one delves deeply (emphasis added in the above statements) into the various reports, there appears to be some inkling of agreement. Although the strongest evidence that the increase in unsaturation is a lowtemperature response comes from the observations of de la Roche er al. (1975) where cultivars of contrasting hardiness were used, some caution must be exercised before summarily concluding that such a comparison could serve to distinguish biochemical alterations that are low-temperature responses from those that are causally related to cold acclimation. Although all the cultivars had similar killing points (-2°C) in the nonacclimated condition, they varied in their killing points (Marquis, -5°C; Cappelle-Desprez, -6°C; Rideau, - 13°C; Kharkov, - 18°C) after 5 weeks of acclimation. Thus, it was not as though acclimation was totally precluded in the less hardy varieties; only the final extent of hardiness varied. In other words, they all increased in hardiness from -2°C to at least -5°C. If freezing injury were viewed only as resulting from one stress, this might not have any significance; however, there is compelling evidence (Olien, 1967a) to indicate that freezing injury is the result of several stresses. Such evidence allows for the possibility that stresses are encountered in a sequential manner. Hence, it is entirely possible that the increase in unsaturation was associated with the increase in hardiness beyond -2°C but not beyond -5°C. Although de la Roche et al. (1975) alluded to such a possibility with the statement that “the increase in linolenic acid per se is not a primary factor in cold hardening, at least at temperatures from -5” to - 18°C. . . ,” they concluded that “stimulation of linolenic acid biosynthesis is merely a general response to the low temperature growth condition. ” And in a later paper (Singh et al., 1977), it is concluded that “both unsaturation and bulk fluidity. . . bear little relationship to their degree of freezing tolerance. It is important to note the expression “degree of freezing tolerance,” which may be interpreted to imply that the changes may be related to the initial stages of acclimation; however, this was not stated. Similarly, Willemot et al. (1977) demonstrated that both the hardy cultivar, Kharkov, and the unhardy cultivar, Champlein, increased in hardiness to the same extent (from -5°C to -12°C) after 1 week of acclimation. Furthermore, it was during this time that the largest increase in linolenic acid occurred in the roots-whether expressed as an absolute amount or as a percentage of the total fatty acids. Thus, the possibility remains that increases in unsaturation may be related to overcoming one of the initial stresses that is incurred in the extremely tender stages. If such were the case, then increases in fatty acid unsaturation might be related to the cold acclimation process but not be responsible for the extent of hardiness in hardier varieties and hence not responsible for varietal differences. If ”

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this were so, then changes in unsaturation of fatty acids might be one of the initial events occurring during cold acclimation, and any such changes should be detected after relatively short periods of time. Lending support to this possibility, Farkas et al. (1975) indicated that changes in the fatty acid composition of wheat and rye leaves were readily apparent after 2 days of exposure to cold. Furthermore, in the data of Willemot (1977) significant increases in the incorporation of 32Pinto lipids (expressed as percentage of radioactivity absorbed) occurred within 14 hours. Thus, the efforts of de la Roche and Willemot and their co-workers may have provided some valuable evidence to support the concept that cold acclimation involves a sequential series of events necessary to ensure survival after exposure to a series of freezing stresses. However, one problem remains. Specifically, in no instance, to the author’s knowledge, has it been experimentally demonstrated how an increase in fatty acid unsaturation would contribute to either the mitigation or the avoidance of any of the stresses currently known to occur during freezing. This includes any demonstrations that increases in unsaturation of fatty acids of plant membrane lipids could result in increased membrane water permeability in order to achieve the avoidance of intracellular ice formation. (This point will be addressed in the following section.) Furthermore, this is the same problem that existed when increases in fatty acid unsaturation observed in chilling resistant species (Lyons et al., 1964) were generally assumed to be beneficial in frost-hardy species. However, this is only an opinion formed from the lack of a complete understanding of the stresses arising during freezing and should not be construed to mean that increases in unsaturation cannot be beneficial-nly that sufficient information on the subject is lacking.

C. BIOCHEMICAL ALTERATIONS FROM A STRESS AVOIDANCE PERSPECTIVE

There are numerous factors that can influence the degree of injury incurred during freezing and that can be considered from the viewpoint of whether the stresses of the freezing process are avoided, mitigated, or tolerated. Levitt (1972) has delineated resistance into evasion, avoidance, and tolerance mechanisms, which is helpful in providing some uniform terminology in an area fraught with a multitude of interchangeable terms. Furthermore, Levitt has indicated that the problem of cold resistance should be analyzed and viewed in the context of stresses and resultant strains. Although Levitt has further distinguished strains as being either elastic or plastic, a strict and parochial usage of the terms evasion, avoidance, and tolerance or stresses and strains will be possible only in situations clearly defined with respect to time and location. For example, consider low-temperature tolerance: Tolerance of low tempera-

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tures can be achieved either by avoiding or by tolerating ice formation in the plant; if ice formation is tolerated, it can be either by avoidance or by tolerance of various mechanical stresses, depending on the location of ice formation in tissue; if intracellular ice formation is avoided and extracellular ice formation is tolerated, the latter can be through either the avoidance or the tolerance of the associated dehydration of the cell; if dehydration of the cell can be tolerated, then either the avoidance or the tolerance of the concentration of toxic solutes or other solution effects can be important. Thus, only each event and its subsequent repercussions can be considered as an avoidance or tolerance situation, and not the overall sequence of events. A similar picture can be considered for stresses and strains in that a particular stress can result in a strain that may, in turn, be considered as a stress. For example, extracellular ice formation is a stress that results in dehydration. It can be debated whether to consider the dehydration as a strain of the system (the cell) or as a resultant stress impinging on the system. Clearly, the semantics associated with cold resistance can be interpreted in several ways, and strict interpretations can diminish their usefulness as conceptual guides. As there is general agreement that membrane damage is a universal manifestation of freezing injury, it could be suggested that avoidance or mitigation of stresses would generally be a result of changes in the membrane environment, whereas tolerance mechanisms would be a result of changes in the membrane per se. There is little doubt that cold resistance is a composite of both possibilities. From a stress avoidance perspective, biochemical changes occurring during the period of cold acclimation should be first viewed in the context of the known physicochemical events and ensuing changes in the cellular environment (see Mazur, 1970) in order to determine whether these changes can result in an alteration of the various freezing stresses (Olien, 1967a). Such a sequence would include the physicochemical events that occur after the moment of extracellular ice formation. These events, which are amenable to avoidance or mitigation, include avoidance of intracellular ice formation, mitigation of the amount or type of extracellular ice formation, mitigation of cellular dehydration, and mitigation of toxic solute concentration and other solution effects.

I . Avoidance of Intracellular Ice Formation One of the initial potential stresses that can be encountered during freezing is the formation of intracellular ice. Siminovitch and Scarth (1938) observed that lethal intracellular ice formation occurred at a slower freezing rate in nonacclimated tissues than in acclimated tissues. Salcheva and Samygin (1963) reported that intracellular ice can form in wheat cooled at the relatively slow rates of 20"C/hr. Olien (1 967a) considers the ease with which ice can be induced to form within the protoplasts as an index of the transition from the tender (unhardy) to

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the hardy state. Several factors could be instrumental in preventing intracellular ice formation. Increases in cellular solute concentration, one of the most universal manifestations of cold acclimation (see Alden and Hermann, 1971; Levitt, 1972), would serve to depress the freezing point of the intracellular solution so that freezing would occur initially in the extracellular solution. Such an increase in solute concentration could be achieved either by an increase in solutes or by a decrease in the amount of solvent. Johansson (1970) and Johansson and Krull(l970) have suggested that cold acclimation of winter wheat may be due, in part, to an increase in solute concentrations. Thus, increases in sugars, amino acids, organic acids, and other osmotically active compounds could serve to achieve the necessary freezing-point depression. However, if viewed strictly from a colligative basis, such increases could only lower the freezing point to the extent of 1.86"Cl osmolal. To prevent intracellular ice formation at lower temperatures, there must be sufficient water efflux from the cell. As early as 1936, it was postulated that cold acclimation could result in an alteration in membrane water permeability in order to permit the rapid removal of water to extracellular sites of ice nucleation (Scarth, 1936; Levitt and Scarth, 1936b). This provided an explanation for the observation that intracellular ice formation occurred at slower freezing rates in nonacclimated tissues than in acclimated tissues. This concept has endured and has been cited by numerous individuals throughout the subsequent years (Levitt, 1972). However, later evidence by Stout et al. (1977) indicated that there may not be a direct cause-and-effect relationship between the two observations. calculations of the rate of ice formation during freezing at a relatively high rate, viewed in relation to membrane water permeability, as measured by a nuclear magnetic resonance technique, indicated that the amount of water efflux required for extracellular ice formation would not be limited by the water permeability of the plasma membrane in nonacclimated tissue. Hence, the decreased incidence of intracellularice formation in tissue may not be a result of increases in membrane water permeability. Sukumaran and Weiser ( 1972) also reported that no differences in water permeability were found between hardy and unhardy cultivars of potatoes. The data of Stout et al. (1977) indicate that the resistance to water efflux may be controlled by heat transfer mechanisms. If so, the magnitude of this resistance would decrease with an increasing freezing rate. Other factors that affect the rate of ice formation could contribute to the resistance. Olien (1967b) has described cell wall polymers that act as competitive inhibitors of ice formation; such inhibitors could explain the observation that acclimated cells survive faster cooling rates than do nonacclimated cells (Siminovitch and Scarth, 1938). The rate of ice formation can also be influenced by whether supercooling can occur (Burke ef al., 1976). The larger the amount of supercooling, the greater

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will be the freezing rate when ice nucleation does occur. However, for supercooling to be a factor in decreasing the freezing rate, less supercooling would have to be associated with acclimation, and this is the opposite of what is usually observed (Burke et a f . , 1976). Another possibility is that, since the plasma membrane serves as a significant barrier to nucleation of the cytoplasm (Levitt, 1962; Olien, 1971b; Mazur, 1970), an avoidance of intracellular ice formation may result from an alteration in the plasma membrane, which increases its effectiveness as a barrier to ice nucleation of the cytoplasm. 2 . Mitigation of Extracellular Ice Formation Considerable evidence has accumulated to indicate that an increase in cold resistance can be achieved by altering the stresses that occur during freezing. Whereas the previous section addressed alterations in the location of ice formation (intracellular versus extracellular), there is evidence to suggest that alterations in the patterns and types of extracellular ice formation can also occur. Thus, although Olien (1967a) considers the ease with which ice can be induced to form within the protoplasts (intracellular ice nucleation) as associated with the transition from an unhardy to a hardy state, resistance also involves modification of some stresses by production of substances that alter the water redistribution pattern (extracellular propagation). Both cases involve nonequilibrium freezing stresses. With respect to extracellular propagation, Olien (1964) has indicated that the structure of crystals forming between the protoplasts is the most important factor affecting initial injury, and the degree of hardiness depends on factors that modify this stress (Olien, 1965, 1968). In subsequent papers, however, it was acknowledged that inhibitors of freezing are not the sole factor in determining a cultivar’s degree of winter hardiness (Shearman er al., 1973) and that the relative degree of hardiness involves traits that affect both the stresses that develop as well as the resistance of the tissues to other stresses, which permits them to tolerate greater distortion (Olien, 1977). Olien (1964) indicates that masses of small or imperfect crystals cause little damage, but damage is increased if the masses are more perfect and solid. The presence of various cell wall mucilages can affect the structure of ice masses in the vicinity of cell walls (Olien, 1965). Also, smaller and more imperfect crystals were observed in hardier tissues (Olien, 1967b), and it was concluded that polymers (arabo-xylans) from winter cereals interfered with freezing by competing with water for positions in the ice lattice. Although the polymers did not prevent freezing, they greatly altered the structure of the ice. In artificial systems, extracts from barley were shown to interact weakly with the ice lattice, whereas polymers from rye interact strongly (Olien, 1967b). In subsequent work, the relationship between the average inhibitor rating of the polymers and the

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plant survival rating of various cultivars was not very good (Olien, 1970). Although activity of the kinetic inhibitors was commensurate with survival ability in some cultivars, other cultivars exhibited better kinetic inhibitor activity than was indicated by their survival rating (Shearman et al., 1973). However, such a demonstration would be expected only if the inhibitors were the sole factor involved in preventing freezing injury in the winter cereals studied, and this should not be assumed. In addition to modifying the type of ice crystals formed, the polymers may also influence the location of ice formation and prevent ice crystals from growing into critical regions (Olien, 1974a). The polymers are considered to give a plant control over both the location and the macro-strbcture of ice formation. It is envisioned that the polymers coat the ice crystal and tend to impede its growth. One point of concern relates to whether the polymers are specifically associated with the cold acclimation process or whether they are constitutive. Shearman ef al. (1973) demonstrated that the polymers were isolated from seeds rather than from plants exposed to acclimating conditions. The monosaccharide composition of the polymers isolated from seeds was similar to that of those isolated from crown tissue. Also, no compositional differences were evident between polymers showing activity and those that were inactive. However, Olien’s work indicates that one important aspect of the cold acclimation process involves alterations in the freezing stresses, and there is the possibility that differences in the hardiness of different tissues may be due to differences in the freezing stresses that occur.

3 . Mitigation of Dehydration There are numerous and varied hypotheses regarding the mechanism of freezing damage, but many of them share the basic belief that injury is a function of dehydration. Although there are several events associated with dehydration and individually they serve as the basis for the various hypotheses, any alteration that occurs during acclimation that reduces the amount of water removed from the cell during freezing could be considered beneficial. However, this statement must be qualified, and it is applicable only for the consideration of injury incurred during extracellularice formation. As previously mentioned, the most common change occurring during cold acclimation is an increase in the osmotic concentration, with either sugars, amino acids, or organic acids being responsible. Such an increase in osmotic concentration will influence the amount of water that must be removed from the cell in order to achieve vapor pressure equilibrium with the extracellular solution. Thus, Johansson (1970) and Johansson and Krull (1970) suggested that increases in hardiness of wheat plants resulted from increased solute concentration, which decreased the extent of cell dehydration at freezing temperatures. How-

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ever, Gustaet al. (1975) demonstrated that, in wheat, the amount of unfreezable water at a given temperature was not strongly dependent on the degree of cold acclimation. In contrast, the amount of water frozen that could be tolerated was significantly less in hardy plants. In other words, during cold acclimation resistance increased, but Johansson observed that injury was always associated with a constant degree of dehydration, whereas Gusta, Burke and Kapoor observed that injury occurred at different (increasing) degrees of dehydration. The former finding would imply that cold acclimation involves avoidance mechanisms, whereas the latter would imply tolerance mechanisms. Although Gusta et al. (1975) rationalized the differences, in either case a reduction in the amount of cellular dehydration would reduce the amount of injury. Therefore, regardless of whether the cell must avoid dehydration or whether it must tolerate dehydration, increases in osmotic concentration will be beneficial. 4. Mitigation of Toxic Solute Concentration Mitigation of toxic solute concentration is closely associated with mitigation of cellular dehydration. The distinction is that some hypotheses on the mechanism of injury indicate that the absolute degree of dehydration and solute concentration incurred are not by themselves injurious; rather, the concentration of specific and toxic compounds, generally considered to be salts, is responsible for injury. Thus, Heber and Santarius (1973) have considered that one component of cold acclimation involves the formation of protective compounds, which can result in protection through nonspecific colligative dilution of toxic compounds. On achieving vapor pressure equilibrium at a given freezing temperature, the protective compounds are concentrated along with the toxic compounds. Since the total concentration of the intracellular solution will be a function of the temperature, the toxic compounds will account for only a portion of this concentration. A further distinction from merely mitigation of dehydration, where the extent of protection will be a function of the initial concentration of solutes, is that protection on a colligative basis will also be a function of the ratio of protective compounds to the toxic compounds. Several compoundscan act as cryoprotectants, providing they are nontoxic over a wide range of concentrations and are osmotically active. Thus, most sugars and some organic and amino acids can function in this role (Heber et al., 1973). Frequently it is noted that on a molar basis some sugars are more effective than others (Tumanov and Trunova, 1963; Heber and Santarius, 1973), usually following the order trisaccharides > disaccharides > monosaccharides. Although this may be indicative of some specificity, differences in activities, especially in concentrated amounts, may account for the differential protection as observed in cryoprotection of chloroplast thylakoids (R. D. Lineberger and P. L. Steponkus, unpublished results).

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Heber (1968) has also indicated that mitigation of toxic substances may also be effected by cryoprotectiveproteins in a manner other than a colligative reduction of toxic compounds. Certain proteins isolated from hardy tissues of rye and barley can protect isolated chloroplast thylakoid membranes against freezing injury (Heber and Emst, 1967; Heber, 1968, 1970). The compounds are very effective at low concentrations and are more than twenty times as effective as sucrose. Whether the increases in total soluble proteins during cold acclimation of alfalfa (Bula et al., 1956; Wilding et af., 1960; Jung and Smith, 1961; Coleman ef al., 1966; Shih et al., 1967; Gerloff et al., 1967; Jung et al., 1967; Brown et af., 1970; Faw and Jung, 1972; Faw et af., 1976) or red and sweet clover (Bula and Smith, 1954; Hodgson and Bula, 1956) or wheat (Pauli and Mitchell, 1960; Zech and Pauli, 1960; Pauli et af., 1961; Pauli and Zech, 1964) contribute to cold resistance in a similar manner requires the demonstration of a cryoprotective influence of the water-soluble proteins.

D. BIOCHEMICAL ALTERATIONS FROM A STRESS TOLERANCE PERSPECTIVE

As cellular membranes are the primary site of freezing injury, it follows that cold acclimation must involve cellular alterations that allow the membranes to survive lower freezing temperatures. Such alterations may be in the cellular environment, as was just discussed, so that either the freezing stresses are altered or there is a direct protection of the membranes. However, cold acclimation may also involve changes in the membrane itself, so that its susceptibility to the freezing stresses is decreased. In 1937, Scarth and Levitt indicated that cold acclimation may render the plasma membrane more tolerant to freezing stresses. Evidence that cold acclimation results in changes in the tolerance of the plasma membrane has been provided by Scarth et al. (1940), and later Siminovitch and Levitt (1941) indicated that the plasma membrane of hardy protoplasts is more resistant to dehydration and is less easily ruptured by deplasmolysis or tension. Efforts by Siminovitch and co-workers (1967a,b, 1968) have been concerned with the localization of injury and resistance in cellular membranes. They concluded that resistance is an intimate property of the components of the plasma membrane, rather than some property arising from the purely colligative action of solutes. Resistance was considered to be associated with the observed increases in membrane structures, which was termed augmentation. Pomeroy and Siminovitch (1 97 1) provided electron microscopic evidence that the process of augmentation was manifested by marked invaginations in the plasma membrane. Wiest and Steponkus (1978) have shown that freezing injury in isolated protoplasts is the result of a membrane alteration that occurs when the protoplast is frozen and contracted, which subsequently limits the size that can be achieved on

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dilution and expansion. The contraction-inducedalteration does not result in lysis but affects the resilience of the protoplast so that there is a critical increment in surface area that can be tolerated. Augmentation of the plasma membrane could conceivably have an important protective effect in increasing the tolerance of the membrane to such an expansion-induced rupture. The concept of augmentation is specifically concerned with quantitative increments in the plasma membrane, rather than major qualitative changes (Siminovitch et al., 1975; Singh ef al., 1975). Other studies indicate that functional alterations in plasma membrane may occur following cold acclimation (Wiest and Steponkus, 1977); however, there is relatively little information regarding qualitative changes in the plasma membrane per se. This fact is attributable to the difficulties encountered in isolating plasma membranes in sufficiently pure form and in a state that can be proved to be identical to their state in vivo. Alternatively, other cellular membranes have been investigated with respect to alterations that occur during freezing (Steponkus ef al., 1977). There is some concern that changes in organelle membranes may not be related to freezing injury, since the plasma membrane is most often considered as the primary site of injury. However, if the plasma membrane is the site of freezing injury and if during cold acclimation protection of this membrane is achieved, it is reasonable to assume that other membranes should also acclimate, lest they become the primary site of freezing injury by default. Several reports of alterations in mitochondria structure and function have been presented, which may indicate that a link between cold acclimation and cold hardiness involves alterations in membrane structure (Miller et al., 1974). However, the membrane changes involve alterations of swelling and contraction characteristics that are influenced by membrane fluidity and may only be manifestations of a low-temperature stimulation of fatty acid unsaturation (Pomeroy, 1976, 1977). Garber and Steponkus (1976b) and Steponkus et al. (1977) have presented biochemical and electron microscopic evidence that chloroplast thylakoid membranes are altered during cold acclimation. Specifically, it was shown that lower concentrations of sucrose afford greater protection of proton uptake in thylakoids isolated from acclimated tissue than in those isolated from nonacclimated tissue. In addition, electron microscopy of acclimated and nonacclimated thylakoids revealed that there was a decreased protein particle concentration on the innerfracture face of acclimated thylakoids. This observation has been recently conf m e d to occur in the plasma membrane of acclimated cells grown in tissue culture (Sugawara and Sakai, 1978). It is interesting to note that the altered particle density occurs at a site-the inner-fracture face of the thylakoidsthat also exhibits alterations when a specific freeze-induced lesion, release of chloroplast coupling factor (CF,), is incurred. This would indicate that there is some structural dependence between CF,, which is released by freezing,

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and the inner-fracture face, where manifestations of cold acclimation can be observed. Such observations would support the hypotheses of several investigators (Tumanov, 1967; Sakai and Yoshida, 1968; Steponkus, 1971) that cold acclimation involves a change both in the cellular environment and in the membrane itself; in the final analysis they justify consideration of alterations in the cellular membranes as being partly responsible for an increased tolerance to freezing. However, future progress will depend on characterization of the specific membrane lesions in order to assess the significance of the various changes that occur during freezing. Although some problems are associated with isolation of the plasma membrane, recent studies with protoplasts (de la Roche et al., 1977; Steponkus and Wiest, 1978; Wiest and Steponkus, 1978) may contribute significantly to this area. Even with the information presently available, however, it is clear that cold acclimation can involve numerous events that alter both the stresses in the cellular environment and the tolerance of the membranes to these stresses. VI. Screening and Stress Proceduresfor Determining Cold Hardiness

Methods used for screening plant cultivars on the basis of cold hardiness have been varied and numerous. Field tests afford a direct measure of winter hardiness, but they are extremely variable from year to year, owing to differences in weather conditions during the fall (which may affect the extent of acclimation of plants entering the winter) as well as the weather conditions during the winter. Because of these yearly variations, trials must be run for a number of years; they are, therefore, extremely time-consuming. Furthermore, winter hardiness is a composite of cold hardiness, desiccation resistance, ability to tolerate or resist frost heaving, disease resistance, and probably several other factors as well. Advances in the genetic manipulation of plants are made much easier if the improvement of only one factor at a time is attempted. Although breeding for increased cold hardiness alone may result in increased susceptibility to other winter factors, the location of germplasm with high degrees of cold hardiness and possibly the chromosomal mapping of the genes conducive to increased cold hardiness may be found by such studies. With such information, attempts to breed for increased winter hardiness would be significantly enhanced. The development of rapid techniques for the screening of plants with high acclimation potential has led to the development of indirect screening methods for determining potential cold hardiness. These methods have arisen largely as a result of empirical correlations between some physiological or anatomical characteristic of seeds or seedlings of a few varieties and the cold hardiness of these varieties. However, as early as 1927 Hill and Salmon stated: “Many

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attempts have been made to correlate cold resistance with some easily observed morphological or physiological character. The relation of winter hardiness to the size of cells, the habit of growth, osmotic pressure of the cell sap, the water and sugar content of the tissue, the hydrophilic colloids of the protoplasm, and other characters have been studied. No results of great value have been secured, so far as finding a practical means of detecting winter-hardy varieties or strains is concerned. Nevertheless, research is still directed toward finding a foolproof indirect method of determining cold hardiness. For instance, Heinrichs (1959) observed that nonhardy cultivars of alfalfa germinate more rapidly and completely in the presence of 6-atm salt or sugar solutions than do hardy cultivars, but many exceptions were noted. Dovrat and Waldman (1967) observed a better inverse correlation between varietal hardiness and germination rate in 6-atm mannitol solutions than was found with the germination percentage after 5 days, although their method did not distinguish between the hardy cultivar Rambler and the intermediate Laduk. Present knowledge concerning the acclimation process, the freezing process, and the mechanisms of freeze-thaw injury to plants casts doubt that any single, indirect method of screening for cold hardiness will be found. Levitt (1972) has pointed out that direct freezing, followed by tests of viability, is the only fully reliable method of assessing cold hardiness. However, several methodological problems exist with this direct test of cold hardiness. The age of the plant, the acclimation procedure, the type of freezing test imposed, the type of tissue used, and the analysis of viability are factors that must be considered and optimized before the potential for acclimation can be determined. ”

A . ACCLIMATION PROCEDURES

The age of the seedling entering the acclimation process has a profound effect on its acclimation rate (Suneson and Peltier, 1934a), the killing point of the plant in the nonacclimated state (Kinbacher, 1962), and probably the acclimation potential of the plant. Seeds are commonly sown at the “typical” time in the fall and brought indoors for controlled freezing tests at various times throughout the winter (Weibel and Quisenberry, 1941). However, cultivars may be produced that possess the greatest acclimation potential when, for instance, a large number of tillers are present rather than at the three- or four-leaf stage. The cold hardiness of these varieties could be quite useful to the fanner, who would have to sow the seed earlier than normal, but the acclimation potential of these varieties would not be detected by the breeder. A comparison of plant age versus acclimation potential is rarely if ever done during screening, and the possibility therefore exists that a number of such varieties have been made but overlooked. Because of this it is suggested that plants of several ages be used during screening.

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An optimum acclimation procedure must be used before the plants are tested for hardiness. Seeds can be sown directly in the field where the natural acclimation process can occur. However, this procedure induces yearly variability and limits the researcher to conducting one experiment per year. Development of artificial acclimation procedures would eliminate both of these problems. From studies of environmental factors affecting the acclimation process, we know that low temperatures and light (especially in the case of plants whose endosperm reserves have been exhausted) are required. Since the farmer has no control over these environmentalfactors, the optimal artificial acclimation procedure conducted by the breeder should involve a simulation of “typical” weather conditions in that geographical area during the fall and early winter before the probability of a serious freeze becomes great.

B. FREEZING PROCEDURES

Two types of freezing tests are commonly practiced, each with its advantages and disadvantages. In many cases a large number of plants are exposed to a single freezing temperature, and varieties are ranked according to the percentage of plants surviving this single temperature (Hill and Salmon, 1927). The primary advantage of this technique is that only a single freezer is required, and information can be obtained concerning the relative ranking of varieties. However, it has been noted that more than one freezing temperature is required if varieties with a wide range of hardiness are to be compared (Warnes and Johnson, 1972a). Fowler et al. (1973) have concluded that freezing tests using one temperature are statistically valid only when differentiating varieties with large differences in hardiness. A great deal more valuable information can be obtained by exposing plants to a variety of freezing temperatures. The minimum temperature at which 50% (or any economically significant percentage) of the test population is killed can be immediately obtained from such a study (Pomeroy and Fowler, 1973). The temperature-versus-survival profile contains extremely valuable information in itself. As an example of this little-recognized importance, consider two genotypes, A and B. For the sake of hypothesis let us say that 50% of the populations of both A and B survive exposure to - 10°C. That is, both genotypes have an LD5,,of - 10°C. However, after exposure to, for instance, - 15”C, only 10% of population A survives, whereas 40% of population B survives. The L&, value implies that both genotypes are of equal cold hardiness, whereas the temperature-versus-survival profile demonstrates that B is clearly a superior genotype in terms of its cold hardiness. Although exposing the plants to a number of freezing temperatures requires more work than exposure to a single temperature, the additional information that can be obtained renders the procedure well worth the effort.

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If freezing is carried out in large rooms, entire plants can be exposed to the freezing process. This is an ideal situation. Unfortunately, the freezers available to most researchers are rather limited in size; thus, selection of a portion of the plant to test cold hardiness would afford maximum utilization of space. Kneen and Blish (1941) observed that, although the cold hardiness of neither the roots nor the leaves corresponds to that of the whole plant, only survival of the crown tissue appears to be related to plant survival. Many workers are currently conducting freezing tests on the crown and making inferences about the cold hardiness of the entire plant (Warnes er af., 1971; Warnes and Johnson, 1972a,b). Since the crown region is the growth center of winter cereals, and is capable of regenerating leaves and roots if they are excised, the assumption that survival of the crown is related to plant survival appears to be a valid one. Although such techniques are commonly used, they may not provide an accurate simulation of the freezing environment that the plants encounter under field conditions. From the extensive work of Olien, it should be evident that injury is not a function of temperature alone. As discussed, several factors can influence the freezing stresses incurred at a particular temperature and require standardization. Furthermore, since these factors may arise in certain regions of cultivation and not in others, or during certain years and not during others; a comprehensive analysis of stress resistance, based on current knowledge (Olien, 1977), should be attempted if any broad extrapolations are to be made and universally applied.

C. VIABILITY ASSAYS

After the freeze-thaw stress is imposed, a test of viability is required. The most direct method, but also the most time-consuming, is to determine the ability for regrowth. Numerous investigators have pointed out that viability determinations are accurate only after 3 weeks or more have elapsed from the time of the freezing test (Anderson and Kiesselbach, 1934; Warnes et al., 1971). The problem with this direct method of assessing viability is the time requirement. It can take a month or longer before the results of a freezing test are known. For this reason artificial tests capable of predicting tissue viability have been developed. These tests are based on the principle that freezing injury is a result of membrane disruption. Dexter et al. (1930, 1932) have developed a technique that measures the release of cellular electrolytes after freezing, which has been used quite extensively. Siminovitch et al. (1962, 1964) have used an analogous test of viability based on the release of amino acids from injured tissues. Metabolic competence of tissue after a freeze-thaw cycle can also be determined by the tissue’s ability to reduce triphenyltetrazolium chloride ( n C ) (Steponkus and Lanphear, 1967a; Ahnng and Irving, 1969). Although all these techniques have been used extensively for measuring tissue

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survival, several problems associated with their use should be acknowledged. First, since they are being used to “predict” plant survival, a calibration curve to determine the extent of leakage of compounds or TTC reduction that corresponds to death should be made for each species under investigation. In many cases this is not done. Second, although the techniques are extremely useful for determining injury in relatively homogeneous masses of tissue, such as roots or leaves, there is still the problem that survival of such tissues is not indicative of plant survival. However, if crown tissues are used to circumvent this problem, none of the indirect tests of viability will be reliable because of the inherent heterogeneity of the crown tissue. Injury to minute, but specific and highly critical, regions of the crown will not be reflected when efflux of compounds from (or reduction of TTC in) the total tissue mass is measured. Very specific techniques for these specialized regions need to be developed. Alternatively, the critical regions can be isolated, but this would eliminate any expediency factor. Thus, because of the above problems and the fact that crown survival most accurately predicts plant survival, direct regrowth measurements remain the best measure of freezing injury. However, there is one serious deficiency in this approach with respect to agronomic crops and especially winter cereals. Generally, researchers will choose an arbitrary survival percentage for comparison and evaluation of cultivars. Although this provides a relative evaluation of the freezing resistance of the tissue, it cannot be inferred that subsequent yield of the different cultivars with the same LD5, will be the equal. Some studies have considered the recovery of cereals from winter injury (Olien and Marchetti, 1976), but few, if any, have equated percentage survival ratings to yield. Considerable genetic variability may exist in this area, which may be overlooked in tests based solely on percentage survival. VII. Summary and Conclusions

Cold hardiness, one of the key components of the winter hardiness complex, is a significant problem confronting agronomists concerned with crop production in cold northern regions of the world. Ever since the earliest reports of the agricultural implications of low temperatures were recorded in 1127 (see Vasil’yev, 1961), considerable attention has been devoted to the problem. However, as is characteristic of most biological phenomena, that which initially appears to be a seemingly simple problem becomes an increasingly complex situation composed of many paradoxical facts. For example, although low temperature is responsible for the potentially lethal stresses that are imposed on a plant, it is also the primary environmental cue responsible for eliciting the plant’s potential to survive freezing temperatures. Although an understanding of freezing injury and cold acclimation has steadily

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evolved, the final answers have not yet been realized. A significant amount of information exists in regards to the physicochemical events associated with the freezing process, but the manner in which injury is effected is not fully understood. The importance of several environmental cues in the cold acclimation process is well established; however, the manner in which these cues are translated into increased resistance remains to be resolved. Although numerous biochemical changes occur during cold acclimation, the significance of most can only be speculated. Insufficient information on what constitutes freezing injury at the molecular level precludes the final integration of the many, already known facts. In addition, the lack of an appropriate conceptualization of the freezing process and cold acclimation can hinder our usage and interpretation of the known facts. Too often, individual aspects of both processes have been considered as mutually exclusive. Rather than searching for any one specific event to explain freezing injury, we might better view the freezing process as a sequential series of potentially lethal stress barriers. In turn, the cold acclimation process can be envisioned as a sequential series of events that enable the plant to avoid, mitigate, or tolerate the stress barriers as they arise. In such a conceptualization, any one single freezing stress would only become the limiting factor at a particular moment in time, depending on the immediate conditions and the successful swnounting of prior stress barriers. Similarly, whether any one particular resistance mechanism would become the primary factor depends on the immediate conditions. Thus, differences in hardiness between species may be due to distinctly different stress barriers that arise during freezing, whereas differences in hardiness between cultivars within a species may be due to differences in the extent of resistance to a given stress barrier. The improvement of agronomic crops with respect to cold hardiness will require considerable input and coordination of numerous disciplines and individuals. And, although an extreme range of diversity in the ability to survive freezing temperatures exists in the plant kingdom-between 0" and - 196°Conly relatively small increases (5°C) in the hardiness of a particular agronomic crop need be achieved in order to have a significant impact on world food production. REFERENCES Ahring, R. M., and Irving, R. M. 1969. Crop Sci. 9, 615-618. Alden, J . , and Hemann, R. K . 1971. But. Rev. 37, 37-142. Anderson, A , , and Kiesselbach, T. A. 1934. J . Am. Soc. Agron. 26, 44-50. Andrews, C. J . , and Burrows, V. D. 1974. Can. J . Plant Sci. 54, 565-571. Andrews, C. J . , Pomeroy, M . K . , and de la Roche, I. A. 1974a. Can. J . Plant. Sci. 54, 9-15. Andrews, C. J . , Pomeroy, M. K . , and de la Roche, I. A. 1974b. Can. J . Bof. 52, 2539-2546. Andrews. J . E. 1958. Can. J . Plant Sci. 38, 1-7.

94

PETER L. STEPONKUS

Andrews, J. E. 1960a. Can. J. Plant Sci. 40, 94-103. Andrews, J. E. 1960b. Can. J . Bor. 38, 353-363. Andrews, J. E., Homcks, J. S., and Roberts, D. W. A. 1960. Can. J. Bor. 38, 601-611. Brandts, J. F., 1967. In “Thermobiology” (A. H. Rose, ed.), pp. 25-72. Academic Press, New York. Brown, J. H., Bula, R. J., and Low, P. F. 1970. Cryobiology 6, 309-314. Bula, R. J . , and Smith, D. 1954. Agron. J . 46, 397-401. Bula, R. J . , Smith D., and Hodgson, R. J. 1956. Agron. J. 48, 153-156. Burke, M. J., Gusta, L. V., Quamme, H. A,, Weiser, C. J., and Li, P. H. 1976. Annu. Rev. Plum Physiol. 27, 507-528. Chandler, W. H. 1913. Mo. Agric. Exp. Srn., Res Bull. 8, 141-309. Coleman, E. A,, Bula, R. J . , and Davis, R. L. 1966. Plant Physiol. 41, 1681-1685. Dantuma, G . , and Andrews, J. E. 1960. Can. J . Bor. 38, 133-151. Davis, D. L., and Gilbert, W. B. 1970. Crop Sci. 10, 7-9. de la Roche, 1. A., Andrews, C. J., Pomeroy, M. K., Weinberger, P., and Kates, M. 1972. Can. J . Bor. 50, 2401-2409. de la Roche, I. A., Andrews, C. J., and Kates, M. 1973. PIanr Physiol. 51, 468473. de la Roche, 1. A,, Pomeroy, M. K., and Andrews, C. J. 1975. Cryobiology 12, 506-512. delaRoche, I. A., Keller, W. A., Singh, J., and Siminovitch, D. 1977. Can. J. Bor. 55, 1181-1185. de Silva, N. S., Weinberger, P., Kates, M., and de la Roche, I. A. 1975. Can. J. Bor. 53, 1899- 1905. Dexter, S. T. 1933a. Plant Physiol. 8, 123-139. Dexter, S. T. 1933b. Planr Physiol. 8, 297-304. Dexter, S. T., Tottingham, W.E., and Graber, L. F. 1930. Planr Physiol. 5, 215-223. Dexter, S. T., Tottingham, W.E., and Graber, L. F. 1932. Plant Physiol. 7,63-78. Dovrat, A., and Waldman, M. 1967. Crop Sci. 7, 1-2. Draper, S. R., and Watson, S. E. 1971. J . Sci. Food Agric. 22, 506-509. Farkas, T., Den-Hadlaczky, E., and Belea, A. 1975. Lipids 10, 331-334. Faw, W. F., and Jung, G. A. 1972. Cryobiology 9, 548-555. Faw, W. F., Shih, S. C., and Jung, G. A. 1976. Plant Physiol. 57, 720-723. Fowler, D. B., Siminovitch, D., and Pomeroy, M. K. 1973. Can. J . Planr Sci. 53, 53-59. Garber, M. P., and Steponkus, P. L. 1976a. Planr Physiol. 57, 673-680. Garber, M. P., and Steponkus, P. L. 1976b. Plant Physiol. 57, 681-686. Gerloff, E. D., Richardson, T., and Stahmann, M. A. 1966. Planr Physiol. 41, 1280-1284. Gerloff, E. D., Stahmann, M. A., and Smith, D. 1967. PIunr Physiol. 42, 895-899. Graiius, J . E. 1974. Mich.. Agric. Exp. Sin., Res. Rep. 247, 16-20. Greenham, C. G. 1966. Can. J . Bor. 44, 1471-1483. Grenier. G . , and Willemot, C. 1974. Cryobiology 11, 324-331. Grenier, G., Tremolieres, A., Themen. H. P., and Willemot, C. 1972. Can. J . Bor. 50, 1681-1689. Grenier, G., Hope, H. J., Willemot, C.. and Themen, H. P. 1975. PIanr Physiol. 55, 906-912. Gruentuch, R. 1935. Bull. Appl. Bor. Gener. Planr Breed., Ser. C 6, 145-152. Gullord, M., Olien, C. R., and Everson, E. H. 1975. Crop Sci. 15, 153-157. Gusta, L. V., and Fowler, D. B. 1976. Can. J. Planr Sci. 56, 673-678. Gusta, L. V . , and Fowler, D. B. 1977. Can. J. Plant Sci. 57, 213-219. Gusta, L. V . , Burke, M. J., and Kapoor, A. C. 1975. Planr Physiol. 56, 707-709. Hiinsel, H. 1972. In “The Winter Hardiness of Cereals” (S.Rajki, ed.) pp. 159-172. Agric. Res. Inst. Hung. Acad. Sci., Martonvasar. Harris, P., and James, A. T. 1969a. Biochim. Biophys. Acra 187, 13-18. Harris, P., and James, A. T. 1969b. Biochem. J. 112, 325-330. Heber, U. 1967. Plant Physiol. 42, 1343-1350. Heber, U. 1968. Cryobiology 5, 188-201.

COLD HARDINESS OF AGRONOMIC CROPS

95

Heber, U. 1970. Frozen Cell, Symp.. 1969 pp. 175-188. Heber, U., and Ernst, R. 1967. I n “Cellular Injury and Resistance in Freezing Organisms” (E. Asahina, ed.), Vol. 11, pp. 63-77. Inst. Low Temp. Sci., Sapporo, Japan. Heber, U. W., and Santarius, K. A. 1964. Planf Physiol. 39, 712-719. Heber, U., and Santarius, K. A. 1967. In “The Cell and Environmental Temperature” (A. S. Troshin, ed.). pp. 27-34. Pergamon, Oxford. Heber, U., and Santarius, K. A. 1973. I n “Temperature and Life” (H. Precht et af., eds.), pp. 232-263. Springer-Verlag, New York. Heber, U., Tyankova, L., and Santarius, K. A. 1971. Eiochim. Eiophys. Acra 241, 578-592. Heber, U., Tyankova, L.. and Santarius, K. A. 1973. Eiochim. Eiophys. Acra 291, 23-37. Heinrichs, D. H. 1959. Can. J. Plant Sci. 39, 384-394. Heinrichs, D. H. 1973. Can. J. Plant Sci. 53, 773-777. Heslop-Hamison. J. 1969. I n “Physiological Aspects of Crop Yield” (J. D. Eastin, ed.), pp. 291-321. Am. SOC.Agron. & Crop Sci. SOC.Am., Madison, Wisconsin. Hilditch, T. P., and Williams, P. N. 1964. “Chemical Constitution of Natural Fats,” 4th ed., p. 207. Chapman & Hall, London. Hill, D. D., and Salmon, S. C. 1927. J. Agric. Res. 35, 933-937. Hitchcock, C., and Nichols, B. W. 1971. “Plant Lipid Biochemistry.” Academic Press, New York. Hodgson, H. J . . 1964. Crop Sci. 4, 302-305. Hodgson, H. J., and Bula, R. J. 1956. Agron. J . 48, 157-160. Hudson, M. A., and Brustkern, P. 1965. Planta 66, 135-155. Jagendorf, A. T. 1975. In “Bioenergetics of Photosynthesis,” (Govindjee, ed.), pp. 413492. Academic Press, New York. Johansson, N. 0. 1970. Natl. Swed. Insr. Planr Prot. Contrib. 14, 364-382. Johansson, N. 0.. and Krull, E. 1970. Natl. Swed. Insf. Plant Prot. Contrib. 14, 343-362. Johnson, V. A,, Warnes, D. D., and Schmidt, J . W. 1970. Proc. FAOIRockefeller Found. Whear Semin., 3rd, 1970 pp. 145-153. lung, G.A,, and Larson, K. L. 1972. In “Alfalfa Science and Technology” (C. H. Hanson, ed.), pp. 185-209. Am. SOC.Agron., Madison, Wisconsin. Jung, G. A,, and Smith, D. 1961. Agron. J. 53, 359-364. Jung, G. A., Shih, S. C.. and Shelton, D. C. 1967. Cryobiology 4, 11-16. Kinbacher, E. J. 1962. Crop Sci. 2, 91-93. Klages. K. H. 1926a. J. Am. Soc. Agron. 18, 184-193. Klages. K. H. 1926b. J. Am. Soc. Agron. 18, 529-566. Kneen, E., and Blish, M. J. 1941. J. Agric. Res. 62, 1-26. Kuiper, P. J. C. 1970. Plant Physiol. 45, 684-686. Laude, H. H. 1937. J. Agric. Res. 54, 899-917. Levitt, J. 1956. “The Hardiness of Plants.” Academic Press, New York. Levitt, J . 1962. J. Theor. Eiof. 3, 355-391. Levitt, J . 1972. “Responses of Plants to Environmental Stresses.” Academic Press, New York. Levitt, J., and Dear, J. 1970. Frozen Cell. Symp.. 1969 pp. 149-174. Levitt, J . , and Scarth, G. W. 1936a. Can. J. Res., Secr. C 14, 267-284. Levitt, J., and Scarth, G. W. 1936b. Can. J. Res., Sect. C 14, 285-305. Lyons, J. M., and Asmundson, C. M. 1965. J. Am. Oil Chem. Soc. 42, 1056-1058. Lyons, J. M.. Wheaton, T. A., and Pratt, H. K. 1964. Plant Physiol. 39, 262-269. Maximov, N. A . 1912. Eer. Dtsch. Eor. Ces. 30, 52-65; 293-305; and 504-516 (cited by Chandler, 1913). Mazur, P. 1969. Annu. Rev. Plant Physiol. 20, 4 1 9 4 8 . Mazur, P. 1970. Science 168, 939-949. Metcalfe, E. L., Cress, C. E., Olien, C. R., and Everson, E. H. 1970. Crop Sci. 10, 362-367. Miller, R. W., de la Roche, I. A,, and Pomeroy, M. K. 1974. Plant Physiol. 53, 426433.

96

PETER L. STEPONKUS

Molisch, H. 1897. “Untersuchung uber das erfrieren der pflanzen.” Jena (cited by Chandler, 1913). Nath, J . , and Fisher, T. C. 1971. Cryobiology 8, 420430. Newton, R. 1924. J. Agric. Sci. 14, 178-191. Olien, C. R. 1961. Crop Sci. 1, 26-28. Olien, C. R. 1964. Crop Sci. 4, 91-95. Olien, C. R. 1965. Cryobiology 2, 47-53. Olien, C. R. 1967a. Annu. Rev. Plant Physiol. 18, 387408. Olien, C. R. 1967b. Crop Sci. 7, 156-157. Olien, C. R. 1968. In “Barley Handbook,” pp. 121-127. U.S. Dep. Agric., Washington, D.C. Olien, C. R. 1970. Mich., Agric. Exp. Stn. 123, 4-8. Olien, C. R. 1971a. Cryobiology 8, 244-248. Olien, C. R. 1971b. Barley Genet. 2, Proc. Inr. Symp., 2nd, I969 pp. 356-363. Olien, C. R. 1973. J. Theor. Biol. 39, 201-210. Olien, C. R. 1974a. Plant Physiol. 53, 764-767. Olien, C. R. 1974b. Mich., Agric. Exp. Sin., Res. Rep. 247, 1-10, Olien, C. R. 1977. US.,Dep. Agric., Tech. Bull. 1558. Olien, C. R., and Marchetti, B. L. 1976. Crop Sci. 16, 201-204. Palta, J. P., Levitt, J., and Stadelmann, E. J . 1977a. Plant Physiol. 60, 393-397. Palta, J . P., Levitt, J., and Stadelmann, E. J . 1977b. Plant Physiol. 60, 398401. Pauli, A. W. 1960. Agron. J. 52, 265-266. Pauli, A. W., and Mitchell, H. L. 1960. Plant Physiol. 35, 539-542. Pauli, A. W., and Zech, A. C. 1964. Crop Sci. 4, 204-206. Pauli, A. W., Kolp, B. J., and Stickler, F. C. 1961. Crop Sci. 1, 137-138. Paulsen, G. M. 1968. Crop. Sci. 8, 29-32. Peltier, G. L., and Kiesselbach, T. A. 1934. J. Am. SOC.Agron. 26, 681-687. Peltier. G. L., and Tysdal, H. M. 1932. J. Agric. Res. 44, 429444. Heifer, R. P., and Kline, J . P. 1960. Agron. J. 52, 621-623. Pomeroy, M. K. 1976. Plant Physiol. 57, 469473. Pomeroy, M. K. 1977. Plant Physiol. 59, 250-255. Pomeroy, M. K., and Fowler, D. B. 1973. Can. J. Plant Sci. 53, 489-494. Pomeroy, M. K., and Siminovitch, D. 1971. Can. J . Bot. 49, 787-795. Pomeroy, M. K., Andrews, C. J . , and Fedak, G. 1975. Can. J. Plant. Sci. 55, 529-535. Quisenberry, K. S. 1938. J . Am. SOC.Agron. 30, 399405. Rammelt, R. 1972. In “The Winter Hardiness of Cereals’’ (S. Rajki, ed.), pp. 185-195. Agric. Res. Inst. Hung. Acad. Sci., Martonvasar. Redshaw, E. S.,and Zalik, S. 1968. Can. J . Biochem. 46, 1093-1097. Rimpau, R. H. 1958.2. Pflanzenzuecht. 40, 275-318. Roberts, D. W. A., and Grant, M. N. 1968. Can. J . Plant Sci. 48, 369-376. Sakai, A., and Yoshida, S. 1968. Cryobiology 5, 160-174. Salcheva, G., and Samygin, G. 1963. Sov. Plant Physiol. (Engl. Transl.) 10, 50-57. Salmon, S. C. 1917a. J. Am. SOC.Agron. 9, 21-24. Salmon, S. C. 1917b. J . Am. SOC.Agron. 9, 353-380. Salmon, S. C. 1933. Kans.,Agric., Exp. Sta., Tech. Bull. 35, 1-66. Santarius, K. A. 1971. Plant Physiol. 48, 156-162. Santarius, K. A. 1973a. Biochim. Biophys. Acra 291, 38-50. Santarius, K. A. 1973b. Planfa 113, 105-1 14. Santarius, K. A., and Heber, U. 1970. Cryobiology 7, 71-78. Santarius, K. A.. and Heber, U. 1972. In “The Winter Hardiness of Cereals” (S. Rajki, ed.), pp. 7-29. Agric. Res. Inst. Hung. Acad. Sci., Martonvasar. Scarth, G. W. 1936. Trans. R. SOC. Can, Sect. 5 30, 1-10.

COLD HARDINESS OF AGRONOMIC CROPS

97

Scarth, G. W., and Levitt, J. 1937. Plant Physiol. 12, 51-78. Scarth, G. W., Levitt, J., and Siminovitch, D. 1940. Cold Spring Harbor Symp. Quant. Biol. 8, 102-109. Schaffnit, E. 1910. Mitt. Kaiser- Wilhelm-Inst. Landw. Bromberg 3, 93-1 15 (cited by Chandler, 1913). S h e m a n , L. L., Olien, C. R., Marchetti, B. L., and Everson, E. H. 1973. Crop Sci. 13, 514-519. Shih, S. C., Jung, G. A., and Shelton, D. C. 1967. Crop Sci. 7, 385-389. Siminovitch, D., and Levitt, J. 1941. Can. J. Res. Sect. C 19, 9-20. Siminovitch, D., and Scarth, G. W. 1938. Can. J . Res. 16, 467481. Siminovitch, D., Thenien, H., Wilner, J., and Gfeller, F. 1962. Can. J . Bor. 40, 1267-1269. Siminovitch, D., Thenien, H., Gfeller, F., and Rheaume, B. 1964. Can. J. Bor. 42, 637-649. Siminovitch, D., Rheaume, B., and Sacher, R. 1967a. In “Molecular Mechanisms of Temperature Adaptation” (C. L. Prosser, ed.). Publ. No. 84, pp. 3 4 0 . Am. Assoc. Adv. Sci., Washington, D.C. Siminovitch, D., Gfeller, G., and Rheaume, B. 1967b. In “Cellular Injury and Resistance in Living Organisms” (E. Asashina, ed.), pp. 93-117. Inst. Low Temp. Sci., Sapporo, Japan. Siminovitch, D., Rheaume, B., Pomeroy, K., and Lepage, M. 1968. Cryobiology 5, 202-225. Siminovitch, D., Singh, J., and de la Roche, 1. A. 1975. Cryobiology 12, 144-153. Singh, J., de la Roche, I. A., and Siminovitch, D. 1975. Nature (London) 257, 669-670. Singh, J., de la Roche, I. A., and Siminovitch, D. 1977. Cryobiology 14, 620-624. Sinnott, E. W. 1918. Bor. Gaz. (Chicago) 66, 162-175. Sinz, E. 1914. J. Landwirtsch. 62, 302-312. Smith, D. 1968. Cryobiology 5 , 148-159. Sprague, M. A. 1955. Plant Physiol. 30, 447451. Steinbauer, G. 1926. Plant Physiol. 1, 281-286. Steponkus. P. L. 1971. Plant Physiol. 47, 175-180. Steponkus, P. L., and Lanphear, F. 0. 1967a. Plant Physiol. 42, 1423-1426. Steponkus, P. L., and Lanphear, F. 0. 1967b. Plant Physiol. 42, 1673-1677. Steponkus, P. L., and Lanphear, F. 0. 1968. Physiol. Plant. 21, 777-791. Steponkus, P. L., and Wiest, S. C. 1978. In ”Plant Cold Hardiness and Freezing Stress” (P. H. Li and A. Sakai, eds.), pp. 75-91. Academic Press, New York. Steponkus, P. L., Garber, M. P., Myers, S. P., and Lineberger, R. D. 1977. Cryobiology 14, 303-321. Stout, D. G., Steponkus, P. L.,and Cotts, R. M. 1977. Plant Physiol. 60, 374-378. Sugawara, Y.,and Sakai, A. 1978. In “Plant Cold Hardiness and Freezing Stress” (P. H. Li ano A. Sakai, eds.), pp. 197-210. Academic Press, New York. Sukumaran, N. P.,and Weiser, C. J. 1972. Plant Physiol. 50, 564-567. Suneson, C. A., and Peltier, G. L. 1934a. J. A m . SOC.Agron. 26, 50-58. Suneson, C. A,, and Peltier, G. L. 1934b. J. Am. SOC. Agron. 26, 687-692. Suneson, C. A , , and Peltier, G. L. 1938. J. Am. SOC.Agron. 30, 769-778. Svec, L. V.,and Hodges, H. F. 1972a. Can. J. Plant Sci. 52, 165-175. Svec, L. V., and Hodges, H. F. 1972b. Can. J. Plant Sci. 52, 955-963. Thomson, L. W., and Zalik, S. 1973. Plant Physiol52, 268-273. Trunova, T. 1. 1965. Sov. Plant Physiol. (Engl. Transl.) 12, 70-77. Tsenov, A . 1972. In “The Winter Hardiness of Cereals” (S. Rajki, ed.), pp. 61-70. Agric. Res. Inst. Hung. Acad. Sci., Martonvasar. Tumanov, I. 1. 1967. Sov. Planr Physiol. (Engl. Transl.) 14, 440453. Tumanov, I. I., and Trunova, T. I. 1963. Sov. Plant Physiol. (Engl. Transl.) 10, 140-149. Tysdal, H. M. 1933. J. Agric. Res. 46, 483-515. Tysdal, H. M., and Pieters, A. J. 1934. J. Am. SOC. Agron. 26, 923-928.

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Uribe, E. G.,and Jagendorf. A. T. 1968. Arch. Biochem. Biophys. 128, 351-359. Vasil’yev, I. M. 1961. “Wintering of Plants.” Am. Inst. Biol. Sci., Washington, D.C. Vincent, A. 1972. In “The Winter Hardiness of Cereals” (S. Rajki, ed.), pp. 31-70. Agric. Res. Inst. Acad. Sci., Martonvasar. Voblikova, T. V. 1965. Sov. Plant Physiol. (Engl. Transl.) 12, 63-69. Wames. D. D., and Johnson, V. A. 1972a. Agron. J. 64, 285-288. Wames. D. D., and Johnson, V. A. 1972b. Crop Sci. 12, 403-405. Wames, D. D., Schmidt, J. W., and Johnson, V. A. 1971. Barley Gene:. 2 , Proc. Inr. Symp.. 2nd. 1969 pp. 364-377. Weete, J. D. 1974. Monogr. Lipid Res. 1, 1-393. Weibel, R. O., and Quisenberry, K. S. 1941. J. Am. Soc. Agron. 33, 336-341. Wiegand, K. M. 1906. Planr World 9, 31-32. Wiest, S. C., and Steponkus, P. L. 1977. J. Am. SOC.Hor:. Sci. 102, 119-123. Wiest, S. C., and Steponkus, P. L. 1978. Planr Physiol. 62 (in press). Willemot, C. 1975. Plant Physiol. 55, 356-359. Willemot, C. 1977. Planr Physiol. 60, 1-4. Willemot, C., Hope, H.J., Williams, R. J., and Michaud, R. 1977. Cryobiology 14, 87-93. Young, A. L., and Feltner, K. C. 1966. Crop Sci. 6, 547-551. Zech, A. C., and Pauli, A. W. 1960. Agron. J. 52, 334-337.

ADVANCES IN AGRONOMY, VOL. 30

THE ROLE OF ROOTING CHARACTERISTICS IN THE SUPPLY OF WATER TO PLANTS' H. M. Taylor and Betty Klepper USDA, Science and Education Administration, Federal Research, Iowa State University, Ames, Iowa, and Columbia Plateau Conservation Research Center, Pendleton, Oregon 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99 . . . . . . . . . . . . . . loo 11. A Model of Water Upt t System . . . . . . . . . . . . . . . . 105 111. Diurnal Water Potentials in IV . Axial Resistances . . . . .

Resistances in the Abso Rooting Volume. . . . . The Real World . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Factors That Man Can Control ............................................. 1x. A Final Thought . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ........................................................ References

V. VI . VII. VIII.

120 122 125 125

I. Introduction

Nearly every terrestrial plant undergoes a reduction in water potential each day. This reduction develops because water vapor diffuses out of the open stomata, whereas CO, diffuses into the substomatal cavity. Loss of water causes tissue to dehydrate and lowers the total chemical potential of the leaf water. Water then moves from the adjacent plant tissue along a path of decreasing potential. During morning hours, the radiant energy load on the leaves steadily increases, and the water potential decreases. The energy load decreases in the afternoon, there is less evaporation from the leaves and the tissues rehydrate until they become turgid during the night if sufficient water is supplied by the roots. Three major factors control how much plant water potential decreases during the daily stress period. These factors are ( a )the input of energy to the leaf and the resultant evaporation of water; (b)the difficulty with which water can move from internal evaporating surfaces through the stomata to the ambient air; and (c) the supply of water from the soil to substomatal evaporating surfaces within the leaves. We shall stress the third factor, the water-supplying capability of root systems in field situations, in this article. We shall not attempt to include all pertinent literature but shall present an account of the factors that affect water flow from the soil to the xylem of the plant at ground level, quoting extensively 'Journal Paper J-8906 of the Iowa Agriculture and Home Economics Experiment Station, Ames, Iowa, Project No. 1941, and Technical Paper 4673 of the Oregon State University Agricultural Experiment Station, Pendleton, Oregon. 99 Copyright @ 1978 by Academic Press. Inc. All rights of reproduction in any form reserved.

ISBN 0-12-ooO730-4

100

H. M. TAYLOR AND BETTY KLEPPER

from our research. This article will not cover physiological effects of a continuing water deficit on top growth and yield but will, from time to time, mention responses of plant tops to water stress because of a feedback response on root functions. Excellent reviews have been published recently on plant response to water stress (Hsiao, 1973), water stress and growth (Hsiao ef al., 1976), photosynthesis in water-stressed plants (Boyer, 1976), and plant hormone interactions with water stress (Vaadia, 1976). In addition, Jarvis (1975) has reviewed water transfer in plants, Tinker (1976) has reviewed transport of water to plant roots in soil, and Newman (1976) has reviewed water movement through root systems. This article will cover some material specifically covered by the last three authors, but will stress behavior of root systems under field conditions more than they did. II. A Model of Water Uptake by Roots

Many conceptual models have been developed to describe the uptake of water from soil by a root system. These models assume, either explicitly or implicitly, that uptake rate is a function of (a) transpiration rate, (b)plant root length (either total or active roots), (c) water uptake rate per unit of root length (either measured or calculated), and (d) a water potential difference between some point in the soil and some point in the plant or atmosphere. The models often differ only in assumptions incorporated to simplify calculations. Availability of largestorage-capacity computers has made several of these simplifications unnecessary. We therefore can use a comparatively complex method for combining root length, conductivity, and water potential effects on root system uptake patterns. This model provides a framework that allows us to pinpoint and discuss major gaps in our knowledge about patterns of plant water uptake. This partly tested model starts with assumptions that accurate rates of plant transpiration and root water uptake from each soil layer can be obtained. Evapotranspiration (Ritchie et al., 1972), evaporation of water from the land surface (Hillel, 1975), and water fluxes between soil layers (Klute, 1973) can be calculated, but direct measurements are preferable. Transpired water is withdrawn from leaf tissues, which in turn are continually resupplied through the vascular system by water taken up by roots. The source of transpiration water can be expressed by the equation Ta = A B p

+ Ua

where Ta = transpiration rate (cm3 H,0/cm2 land surface/min)

A& = rate of decrease of water stored in plants occupying the specified land surface (cm3 H,O/cmZ land surface/min)

101

ROLE OF ROOTING CHARACTERISTICS

V , = water uptake rate from soil by roots of plants occupying the specified land surface (cm3 H,0/cm2 land surface/min) Many models ignore A& and equate transpiration to root water uptake. This procedure usually provides satisfactory answers when only daily values are required and plants rehydrate to the same early morning water potentials on successive days. Under these specified conditions, the error due to ignoring a daily growth component of A&, usually will be less than 5% of transpiration-1-2% for soybeans [Gfycine max (L.) Merr.] in Iowa. If instantaneous transpiration rates and root water uptake rates are required, however, A&, can be appreciable. For example, Kramer (1937) found that the difference between transpiration and absorption (A&,) sometimes was greater than root absorption for sunflowers (Helianthusannuus L.) (Fig. 1). The AO,, values will be especially large, relative to transpiration, when succulent plants are first watered after undergoing severe water stress, at night when transpiration rates are low, or when major changes in transpiration rates occur rapidly. Under field conditions, roots absorb water from soils at different depths, with different water contents and with different physical properties. Therefore, it is convenient to partition water uptake among several soil volumes, such as the horizontal layers shown in Fig. 2. Then uptake from a layer can be determined as a function of (a) root length in the layer, (6) total water potential difference between bulk soil in the layer and plant xylem at the land surface, and (c)

0 '

oeoo

I

I

loo0

1200

I

I

1400 1600

I

I

I

1800 Po0 2200

I

2400

Time (hours)

FIG. I . Rates of transpiration and absorption of sunflowers (Heliutirhus utinuus L.) for 2-hour periods. Redrawn from Kramer (1937).

102

H. M. TAYLOR AND BETTY KLEPPER

FIG.2. A schematic definition of several components of Eqs. (2) and (3) superimposed on the root distribution (after Bohm, 1977) of 85day soybeans growr. in 100-cm-wide rows on loess soil in western Iowa. Each dot represents one root projecting from a prepared trench wall.

resistances to flow between bulk soil and xylem at the land surface. Water uptake of an isolated plant can then be calculated as 11

u = ix= l u i

(2)

where Uiis positive water uptake from a layer of soil (cm3/min). Water extraction by a densely planted crop can be partitioned equally among individual plants, and results can be stated on a land area basis, using the relationship U,,= (U)(planting density). For the sake of simplicity, however, consider the comparatively isolated plant in Fig. 2. Water uptake (U,) from soil volume, Vi, can be calculated by using the equation

ROLE OF ROOTING CHARACTERISTICS

ui

= (Vi)(Li)(qi)($si-

103

(3)

$ri)

where Vi = a rooted volume of soil (cm3) with uniform properties including uniform root density and water potential hi = root length density in Vi (cm/cm3) qi = average root water uptake rate in Vi (cm3 H,O/cm root/bar/min) t,bSi = total soil water potential in Vi (bars) $fi = total water potential in root xylem at midpoint of V, (bars) This equation implies that water uptake in the ith layer is equal to the product of ; rate of water three terms: total root length in the layer-that is, ( V i ) ( L U i )the uptake per unit length of root per bar; and the potential difference from bulk soil into the root xylem at the midpoint of Vi (bar). Field measurements of root xylem water potential deep in the soil profile are not available. Generally, however, accurate values can be obtained for h, the total water potential in plant xylem at the ground surface. An estimate of t,hfi can be made from JlP by subtracting from $ p the loss in potential due to elevation (a generally negligible loss) and the loss in potential due to friction developed between moving water columns and xylem vessel walls. Water potential loss due to elevation can be calculated from $ = - (0.001 bar/cm)(cm) (4) where z is distance (cm) from the land surface (negative). To calculate frictional losses, we must assign resistance values to the main roots carrying water upward in the profile. Figure 3 shows a taprooted system. The diagram shows the location of midpoints in successive layers. All water uptake from a layer is assumed to be channeled through this midpoint. In addition, all water from lower (or more distal) layers is assumed to be channeled through this same midpoint. Beginning at the bottom (nth) layer, Eq. (3) provides the rate of delivery of water to the midpoint, m,,:

un = (vn)(&m)(qn)($sn

(5)

- $rn)

A resistance to flow, R , , is located between the point m and men+,. Thus the potential decrease due to frictional forces ($Y,bars) from m, to qn-j, is, by an Ohm's law analogue, $fn = ($r

+

$.)n

- ($r

+

-

=

$z)n--I

= UnRn

(6)

Similarly, for the top layer, I1

IClf.1

=

$ri

+

$21

$p

2 Ui(RJ i=l

(7)

In general, for flux from the ith layer to the (i - 1) th layer, +fi

= ($r

+

- ($r + + z ) i - l =

i:

ut(Ri)

i=l

(8)

104

H . M. TAYLOR AND BETTY KLEPPER

FIG. 3. A schematic representation of a taprooted plant as visualized for the present model. Symbols m , to m, indicate midpoints of soil volumes V , to V , . R , to R,, indicate axial resistances between midpoints, and qP is xylem water potential at the land surface.

Thus, the xylem potential, t,bP, increases to $,., at the midpoint of the ith layer, where $A

= $p

- $zi -

Wi

(9) Since frictional loss between two points is not constant but depends on flow rate, values must be summed for individual layers for each situation. For example, if upper layers of soil are wet so that fluxes are high into adsorbing roots in the upper part of the profile, then resistance values will be high in xylem elements, and low midday values of JlP will not be transmitted to root xylem vessels in deep soil layers. The equation for uptake from a soil layer can now be written by substituting Eq. (9) into Eq. (3):

ui = ( v t ) ( L i ) ( q i ) ( $ s i

-

+ $zi + x$fi)

(10) The relationship of some of the components of this equation to a plant-soil system in the field can be seen in Fig. 2. We shall now discuss experimental data $p

ROLE OF ROOTING CHARACTERISTICS

105

showing patterns of diurnal changes in water Fotential values. We shall then review information available about axi, ’ 0- Actional resistances, which may cause $r to be higher than JlP, and shall discuss the patterns of rooting to be expected in field situations and how those rooting patterns can influence water extraction. 111. Diurnal Water Potentials in the Soil-Plant System

Figures 4, 5, and 6 show generalized patterns of water potential for three points in a soil-plant system. Data for such field crops as cotton (Gossypium hirsutum L.) and soybeans have been used to estimate $p and $s at some specified depth for a sunny (Fig. 4) and a cloudy day (Fig. 5) (wet soil) and for a sunny day (dry soil) (Fig. 6). Values for +,., root xylem water potential, have been plotted on the assumption that, in wet soil, most resistance to flow occurs during absorption, not axially (longitudinally) in xylem. The way in which $,. varies during the day depends on how much axial resistance occurs in the species under the conditions being studied. If axial resistances are very great, $,. will not vary nearly as much diurnally as is shown in Figs. 5 and 6. At a low flow rate, $T will nearly equal $ p . Total water potential in leaf xylem, $ I , of cotton usually is - 1 to -2 bars before dawn if most of the roots are in wet soil (Browning et al., 1975). For illustrative purposes, we shall assume that total xylem water potential at the land surface is about equal to because within-canopy xylem resistances do not appear to be large in cotton (Klepper et al., 1973). Leaf water potential, and thus JlP, decreases to -10 to -12 bars by 1400 hours during a sunny day, then increases to - 1 to -2 bars by 2000 hours (Fig. 4). During a cloudy day, $ p at 1400 hours usually is -8 to - 10 bars (Fig. 5). It may decrease to -20 to -25 bars at 1400 hours if most of the roots are in dry soil (& drier than -1 to -5 bars) (Fig. 6).

m

L.-.-.-I-.-.-.-.

E

!2

r

.-.L.2.-.L.L -.-.-.-!

4-

._ c

2 -8-

: L

s

P

-12-16‘

FIG. 4. A generalized diurnal pattern of soil (&), root xylem &), and plant &) water potentials on a “sunny” day when cotton and soybean roots are located in “wet” soil.

O L b -

.

.-.

.-L.

.-l-.L.-.L-.-l-.4.-.

-.

.-.

4-

1-8-

a

u:

5 -12-16 -

s

IV. Axial Resistances

We shall now consider the resistance to flow axially within the xylem elements that conduct water from layer to layer in the root profile. These resistances arise because of frictional forces between the moving water column and the vessel walls. Osmotic potentials (Fiscus, 1977), temperature differentials (Taylor and Cary, 1961), and electrical force fields (Briggs, 1967) may also be important. We do not yet have sufficient information to deal with these latter components of total water potential during axial flow. Water moves upward only slowly when transpiration is low, but as rapidly as 1 m d s e c when transpiration is high (Nobel, 1970). Frictional forces along unit length of xylem are low when water movement is slow, but it has been postulated that these frictional forces are high, at least in some species, when transpiration rates are high (Hellkvist et al., 1974). Richter (1973) discussed the difficulties Time (Hours) Midnight 0 2

Noon

4

6

8

10 ,

12 I

14 1

16

18

20

22

Midnight 24 <

-24

FIG. 6 . Generalized diurnal patterns of soil (&), root xylem (&). and plant (I/J~)water potentials on a sunny day when most of the upper roots of cotton or soybeans are located in “dry” soil, but some deep roots are in wet soil.

ROLE OF ROOTING CHARACTERISTICS

107

inherent in analyzing axial resistances, flow rates, and water potential gradients through horizontal planes within plant canopies. He pointed out that plant water potential is the same for two twigs only where they join. At all other points along the two twigs, the potentials can be determined only by considering both flow rates and axial resistances. Some workers (Emerson, 1954; Wind, 1955a,b; Dimond, 1966; Passioura, 1972; Ponsana, 1975) have used the Poiseuille-Hagen equation to calculate flow rates or hydraulic potential gradients in root xylem vessels. They assume that xylem consists of a bundle of capillary tubes, each with a uniform diameter along its length. The equation states

where Q = the rate of water flow (cm3/sec) r = the tube radius (cm) A+ = the decrease in hydraulic potential in the direction of flow bar) AL = the length of capillary tube or root member (cm) 7) = the viscosity of water (poise)

Greacen et al. (1976) summarized results from these calculations and conto cluded that axial resistances for cereal roots ranged from day bar cm day bar root/cm3 water. However, axial resistances may be as low as 7 X cm root/cm3 water for adventitious roots of corn @ea mays L.) (Newman, 1976). Ponsana (1975) found that the Poiseuille-Hagen equation predicted axial resistance satisfactorily for timothy (Phleum pratense L.), but measured resistances were 1.3 to 3 times as great as were calculated resistances for wheat (Triticum aestivum L.), ryegrass (Lolium perenne L.), and orchard grass (Dacrylis glomerata L.). A threefold disparity between measured and calculated axial resistance may seem large. However, when we consider the possible sources of error, this agreement is satisfactory in view of our limited knowledge. A small error in measurement of vessel radii will cause a large error in calculated flows. Furthermore, rough elliptical patches on the walls of metaxylem vessels (Clarkson, 1974) increase frictional resistance. Walls of xylem vessels contain lignin, which may change boundary layer properties, when compared to walls of glass tubes. Hydration shells around cations bound to exchange sites on vessel walls (Bell and Biddulph, 1963) may change flow properties. Lateral transfer of water along the length of the vessel complicates the determination of flow velocity. Finally, the radius of metaxylem vessels may increase with distance from the plant base (Passioura, 1972) or be different when grown under different environmental conditions (Meyer, 1976).

108

H. M. TAYLOR AND BETTY KLEPPER

Despite obvious difficulties in predicting axial resistances, Wilson et al. (1976) successfully used the Poiseuille-Hagen equation to explain drought tolerance and growth of blue grama (Bouteloua gracilis Willd. ex H.B.K.) seedlings. Axial resistance was greatest in the subcoleoptile internode and upper parts of the single seminal root. When the midday transpiration rate equaled the quantity of water that their calculations showed could flow through these two zones, growth stopped. When transpiration exceeded the water-carrying ability of these zones, some leaves died. They calculated that a velocity of 8 c d s e c in xylem was required to supply water when blue grama plants were 50 days old. Adventitious roots increased seedling survival. Adventitious roots decrease axial resistance because they increase the total cross-sectional area available for flow. Species that do not develop secondary xylem tissues often develop these adventitious roots during the growing season and thus supply increased leaf area without great axial resistance. Diameters of adventitious roots may increase at successively higher internodes on the plant. Roots at the first node of Zea mays are smaller in diameter, but their conductivity per unit of cross section is greater than that of adventitious roots from successive internodes (Luxova and Kozinka, 1970). Maize roots at the fifth node have xylem vessel areas about 100 times as great as those of seminal roots or roots of the first node. As a result, about 20 times as much water can flow, at a specified potential decrease, through roots formed at the fifth node as can flow through seminal roots (Luxova and Kozinka, 1970). Axial resistance can be increased when pathogenic organisms invade the vascular system. Waggoner and Dimond (1954) used the Poiseuille-Hagen equation to predict that invasion by fungal mycelia reduces the water-conducting properties of xylem by as much as 80%. In a review article, Talboys (1968) noted that vascular diseases increase axial resistance by vessel plugging due to ( a ) fungal mycelia, (b) polysaccharides, (c) wound reactions of tissues associated with xylem, and (d) debris and calcium uronide gels from macerated xylem cells. Axial resistance also may be increased if cavitation (gaseous embolism) occurs in xylem vessels of roots. Byrne et al. (1977) froze longitudinal sections of roots from cotton (Gossypium hirsutum L.) plants with different leaf water potentials (JII). They found marked decreases in airflow resistance of the frozen roots as leaf water potential decreased below - 10 bars. They interpreted their results as showing that the largest xylem vessels cavitated at -10 bars and thus allowed mass airflow, while the noncavitated vessels were blocked with ice. Leaf water potentials are frequently lower than -10 bars at midday even with “wellwatered” plants, but we do not yet know the relative importance of cavitation in water uptake by plants. Roots of many species undergo secondary growth and add new xylem tissue. This additional cross-sectional area for water conduction reduces axial resistance. There are, however, almost no quantitative data on magnitudes of axial

ROLE OF ROOTING CHARACTERISTICS

I09

resistance. Adverse soil conditions sometimes can prevent development of secondary xylem and significantly increase axial resistance. Many instances are reported in the literature where soil conditions distort the root stele, but the best documented effects on axial resistances are shown with root strangulation or root constriction of cotton by high-strength soil (Taubenhaus et a l . , 1931; Hubbard, 1931; Mathers and Welch, 1964). The injury occurs a few centimeters below the land surface. After radicles have penetrated moist, soft soil, it dries, hardens, and prevents secondary expansion of taproots. Below the high-strength layer, the roots seem normal. Leaf area and transpiration increase until the constricted roots can no longer transmit enough water for transpiration. Plants then wilt severely and soon die. If rain or irrigation reduces the strength of soil layers, root diameters increase rapidly within the formerly constricted zone, and high axial resistance is reduced. Some plant species root deeply in arid or semiarid environments. For example, Campion (1926) found Eucalyptus culaphylla roots hanging from the ceiling of an Australian cave when the ceiling was 45 m below the land surface. Similarly, Phillips (1963) found mesquite (Prosopisjuliforu)roots 53 m deep in an open pit mine. The plant water potential (Iclp) must decrease about 5 bars merely to lift water to the soil surface from these depths. Axial resistance must be low in roots of these species, or almost no water will be extracted from those depths. No measurements of extraction rates from these depths are published, but we can assume that the species occasionally derives some benefit from deep roots, or energy probably would not be expended to produce them. Plants adapted to semiarid and arid environments frequently have rooting depths greater than 3 m (Weaver, 1920). We suspect that axial resistance per meter of root depth usually is small in these species. Qualitative relationships of axial resistance with depth may be inferred from one of our experiments (Taylor and Klepper, 1975). We grew cotton in a soilfilled compartment (60 cm front to rear, 120 cm side to side, and 180 cm deep) at the Auburn rhizotron (Taylor, 1969), where the tops were exposed to a field-like environment (Browning et al., 1975). Rooting density was estimated at a glasssoil interface. After roots had penetrated to 180 cm, we covered the land surface to prevent water flow through it. Drainage from the compartment was also prevented. We monitored soil water content and rooting density as functions of depth and time, and plant water potential as a function of time. The experiment was stopped after the plants extracted 97% of the available water (above -15 bars $ 8 ) . Taylor and Klepper (1975) mathematically described water uptake at all times and depths for that experiment (Fig. 7). The parameters required by the model were ( a ) rooting density (cm root/cm3 soil) as a function of depth and time, (b) water potential difference between soil and leaf petiole as a function of time, (c) water fluxes between adjacent soil layers, and (d) water uptake rate per centime-

110

H. M. TAYLOR AND BETTY KLEPPER

0

soil Water Content (e crn3/crn3) 06 .10 .16 I

I

I

.20 t

August

FIG. 7. Soil water content as a function of soil depth and time for cotton at the Auburn rhizotron (after Taylor and Klepper, 1975). The solid lines connect measured water contents. The A's are water contents predicted by equations described in that article. The S's show starting points for predicted water contents at that depth.

ter of root (4,) as a function of soil water content ( 8 ) Our data showed that the fourth parameter was not a function of time or of depth within the profile (Fig. 8). An earlier experiment with cotton at the Auburn rhizotron (Taylor and Klepper, 1971) also indicated that the relationshipbetweenq, and 8 did not change for soil depths between 30 and 180 cm. We concluded that axial resistances of cotton roots were insignificant compared with other resistances between bulk soil and plant xylem at the land surface. Significant axial resistances apparently occur in soybeans, however. Willatt and Taylor (1978) conducted a field experiment on silt loam soil in western Iowa. They determined evapotranspiration rates, leaf water potentials, and water fluxes between soil layers as functions of time. They also determined soil water content and rooting density as functions of soil depth and time. Water uptake rate per centimeter of root per day ( q r ) approached zero at different soil water potentials, depending on soil depth. For example, qr approached zero at -15 bars JlS at depths of 1.5 m or less. For depths of 1.75-2.0 m, extrapolation of the relationship between qr and $$predicted zero qr at -0.8 bars J18. We believe that this apparent water potential difference probably was caused by axial resistance, which caused $, as defined in Eq. (3), to increase to a daily average value of about -0.8 bars at the 2-m depth. Two experiments (Taylor and Klepper, 1975; Willatt and Taylor, 1978) have now been discussed from which inferences can be drawn about the magnitudes of potential drops that occur as a result of friction during axial flow. Many of the same techniques were used in both experiments. These authors concluded that

111

ROLE OF ROOTING CHARACTERISTICS

axial resistance was insignificant in the cotton experiment and was substantial (0.07 bar/cm) in the soybean experiment. Hellkvist el al. (1974) found that the water potential decrease due to friction (+f) was about 0.06 bar/cm for a lateral root of Sitka spruce [Picea sitchensis (Bong.) Carr.] at a distance 50-80 cm from the trunk. The close agreement of the soybean and spruce t,bf's almost certainly is fortuitous. Axial resistances, even of the magnitudes of those in soybeans, cause major shifts in water extraction patterns, when compared with those of cotton. Figure 9 illustrates this point. In developing Fig. 9, we assumed that (ski was 5 x 10-7 cm3 H,O/cm root/bar/min (an average value of Taylor and Klepper, 1975); (b) the area of land surface was 1000 c d ; ( c )there were four soil layers, each 50 cm thick; (d)$p was - 15 bars; (e) L, was 1 .O cm root/cm3soil; and (fh,bs was -0.1 bar throughout the profile. If no axial resistance occurs, water is extracted equally from each quarter of the root zone. If, however, +f drops 0.07 bar/cm, water extraction from the bottom quarter of the profile will be only 16% of that in the top quarter. Of course, as we have stated earlier, +f probably will vary with depth in the profile rather than be constant with depth as we have assumed here. Most models of water uptake by root systems either ignore or incorporate a constant value for axial resistance. We have stated that axial resistance varies (a) among plant species (Emerson, 1954; Ponsana, 1975), (b) among soil depths in 90 r

a

-t

0

70 0 0 0

430

0 0

0

0 '

A","

o

A'

L

3.0-

0

4 20s ? 1.0I 3

0

OA A

A A

A& A A

o 3 0 c m and e

a

I 0

A 0

I

"

"

,

om

1

1

0.06

I

0.12

0.16

m QO-cmandlZOcrn l e O c m and 1-m

1

I

020

I

6

I

0.24 026

Water content (e. c m 3 / c m 3 )

FIG. 8. Water uptake rate ( q r ) as a function of soil water content ( 0 ) for cotton, after Taylor and Klepper (1975).

112

1

H. M. TAYLOR AND BETTY KLEPPER

I

o, 0.4

Water Uptake, Ui (cm3/rnin/layer) 02 , 0;’ 0: 0;2 0;31 0;4

03 ,

= 375 cma/min uj=033cm3/rnin = 0 bnr Wf = -1.75 bars Wr = -14.98 bars Wr = -13.12 bars

UI Wf

W f = O bar

Wf

= 0 bar

Wf = O bar

FIG. 9. A schematic representation, with calculated values, of uptake patterns for plants with negligible frictional resistance along the root axis (left side, cotton: Taylor and Klepper, 1975) and with sufficientfrictional resistance to cause a root water potential (&)decrease of 0.07 barcm-I (right side, soybeans: Willatt and Taylor, 1978). $p was assumed to be - 15 bars. See text for other assumptions.

one species (Willatt and Taylor, 1978), (c) between seminal and nodal roots and among different nodal roots of cereals (Luxova and Kozinka, 1970), ( d ) when the xylem is invaded by vascular pathogens (Talboys, 1968), (e) when the number of adventitious roots increase (Wilson et al., 1976), (f) when secondary xylem production is constrained by high-strength soil layers (Mathers and Welch, 1964), and (g) when water cavitates in xylem vessels of plants at low potentials (Byme et al., 1977). We also know that rooting density (&) constantly changes during the growing season (Taylor and Klepper, 1975). These L, changes alter axial resistance by altering flux. Our Eq. (10) provides a mechanism for incorporating differences in axial resistance among soil depths and with time. V. Resistances in the Absorption Pathway

The absorption pathway is composed of a soil cylinder, a soil-root interface (including the soil surface, the outer wall of the epidermis, and any root hairs or spaces in-between), epidermal and cortical layers, an endodermis, any stelar tissues that water must cross to get into xylem vessels, and the lumen of xylem vessels from the point where water enters to the midpoint of the soil volume under consideration. This absorption pathway is outlined in Fig. 10. All root

ROLE OF ROOTING CHARACTERISTICS

113

segments are treated as though they are equally permeable. They are given an equal overall value of resistance from bulk soil to the root xylem at the midpoint of the soil volume. The pathways A-M and B-M in Fig. 10 are given equal value even though ages of root and lengths of xylem traversed are different and even though we know that changes in tissue water content, temperature, oxygen stress, and other environmental factors can alter these values. Table I gives approximate distances in the radial part of this pathway for water movement into root xylem. The average distance between roots (r,, cm) was calculated after Barley (1971), using Ogston’s (1958) theory that the halfdistance between randomly dispersed line segments is given by the equation The values of& , 1 cm/cm3, and root diameter, 0.5 mm, commonly occur in crop situations. We have guessed the distance across the different root tissues from looking at roots of several monocotyledonous and dicotyledonous species. The table illustrates several points. First, the width of the soil cylinder associated with each root is very much larger than the root-20 times as large in this example. Second, root tissue is mostly cortex. In this example, 80% of the distance across

FIG. 10. Pathway of water absorption of bulk soil to the midpoint (m)of a soil layer via the root xylem. A and B represent two different points in bulk soil.

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H. M. TAYLOR AND BETTY KLEPPER

TABLE I Approximate Cell Numbers and Distances in the Radial Pathway for Water Flux from Bulk Soil to Xylem Vessels of a “Typical Crop Plant” with a Rooting Density of I .O Cm/Cm3and a Root Diameter of 0.5 Mm

Pathway component

Cell layers (number)

Soil (r, - r,) Soil-root interface Root tissue (total) Tissues outside endodermis Endodermis Stele

20 12

I

I

Radius (mm) Wet

Dry

5.0

5.0

Variable, maybe 0.01 or less 0.25 0.20 0.01 0.05

0. I or less 0.20 0.15

0.01 0.05

the root is cortex and epidermis. A value of more than 50% is appropriate for most crop plants. Thus, water travels mostly through cortical cells en route to the xylem. Furthermore, cortical cells are large and have well-defined air spaces, whereas stelar cells are smaller and more compact. In some species, cell walls in the stele are thicker than those in the cortex. It seems, then, that these two parts of the pathway will have different resistivities (resistance per unit path length). Actual cortical resistance may be considerable, regardless of its resistivity, because of large cortical distances. Anderson and Reilly (1968)found hydraulic conductivities (Lp,cm/sec/atm) of intact Zea mays roots to be half as great as for stripped steles (stele plus endodermis), with Lp = 0.14 X cm/sec/atm for intact roots and 0.26 X 1W6cm/sec/atm for stripped stele. Their data imply that cortical and epidermal resistance in maize is not negligible. Measurements by Jarvis and House (1969)imply that maize cortical tissues are less permeable to water than stelar tissues. Thus, there is evidence that other resistances in the radial pathway, in addition to endodermal resistances, restrict rapid water entry into root xylem. However, data of Clarkson and Sanderson (1974)indicate that the endodermis is the site of a significant resistance to radial water flux in barley. Understanding of the pathway of water flux across tissues would be helpful in assigning resistance values. Newman (1976) suggests that considerable water movement may occur through symplasmic pathways, and his calculations of pathway permeabilities support his argument. We suggest that most of the literature is consistent with the notion that water moves partly through cell walls and partly through symplasmic pathways, with the relative proportions varying with environmental and plant

ROLE OF ROOTING CHARACTERISTICS

115

conditions that affect resistivity, such as flow rate, oxygen tension, temperature, and root anatomical changes with age. We think that, when the relevant resistivities of various root cell types are measured, they will not differ by orders of magnitude but rather by factors of 2 or 3. Thus, we believe that it is useful to think of root resistance to radial flow of water as being spread across the root radius rather than being entirely concentrated in one layer of cells such as the epidermis or endodermis. Cell layers near the center of the root will, of course, influence total tissue resistance to water flow more than will other cell layers merely because fluxes increase as concentric cylinders of cells become smaller. For the roots of a typical crop plant (Table I), fluxes across the endodermis will be 5 times as great as those across the epidermis. If we assume a xylem vessel in the center of the stele to be 0.02 mm in diameter, then flux across the xylem wall will be 25 times as great as that across the epidermis if all the water is delivered to a central metaxylem element. Xylem vessel walls must be very permeable, compared with tissues near the root epidermis, to handle these fluxes, but it is entirely conceivable that considerable resistance is associated with transfer of water across the wall into the vessel lumen, despite numerous pits in vessel walls. Potential gradients established across a root of a steadily transpiring plant must be steeper near the center of the root, even if all cell layers are of identical resistivity. Also, we expect steeper gradients across any cell layers that contain highly resistive materials. Until better experimental data are available, we prefer to assign some radial resistance to all the root tissues. We thus are better able to accommodate the fact that roots shrink and swell diurnally (Huck et al., 1970). If radial resistance to water flow were orders of magnitude greater in the endodermis than in the rest of the cortex, we would not expect to see diurnal shrinkage, because steep potential gradients would be established internal to the endodermis, while outer cortical and epidermal cells would remain at a potential not very different from that of bulk soil. Shrinkage of root tissues occurs diurnally (Huck ef af., 1970), and Cole and Alston (1974) have shown that root diameters may decrease by 50% as they dry from -2 to - 10 bars. Thus, roots undergo long-term shrinkage as surrounding soil dries. If the root has grown along a ped surface, soil shrinkage may decrease soil-root contact, but if the root has created a pore through a ped of clay soil, the pore itself may shrink as the soil dries and thus maintain root-soil contact (White, 1975). Generally, however, root shrinkage probably causes a gap at the root-soil interface. Tinker (1976) has written an excellent review about the possible effects of root shrinkage on radial resistance to water flow. He discusses the possible effects of mucigel, root hairs, vapor gaps, unsymmetrical arrangement of shrunken roots in soil pores, and microscale arrangement of soil particles. We agree with him that more information is urgently needed about these effects on radial resistance.

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H. M. TAYLOR AND BETTY KLEPPER

Much of the soil physics literature published during the last three or four decades has dealt with physics of water retention and movement in soil. When reading this chapter, some soil physicists will feel that soil water flow has been ignored, or at least slighted. At this point, we reemphasize that (a) water travels further in soil than radially in plant tissue (Table I); (b) the soil provides an alternative pathway to the roots for water movement from one soil volume to another; and (c) soil resistance to water flow, especially in the rhizosphere, can exert a major control on the magnitude of qf, the term in Eq. (3) that represents water uptake rate of unit root length. We shall briefly mention some unresolved soil water flow problems in the section entitled The Real World, but our primary objective is to stress plant rooting characteristics that are important in soilplant-water relations. We have discussed both axial and radial resistances to water flow from midway between roots located deep within soil to the xylem at the land surface. By now, the reader may have decided that water uptake by a root system is too complex for rational analysis at this time. That conclusion obviously is justified for some situations. However, we successfully modeled water uptake by cotton plants grown in a rhizotron compartment (Fig. 7). In that analysis, we assumed (a) that the radial resistance to water flow from the midpoint between roots to lumen of the xylem was a function only of volumetric water content of the soil layer-that is, that the radial resistance-water content relations did not vary with root age or with soil depth; and (b)that axial resistance was negligible. Since the model was successful, the two assumptions probably were valid for that situation. However, the possibility exists that compensating factors may have operated. For example, we indicated that deep roots were, on the average, younger than shallow roots. Thus, higher radial resistance of old roots located near the land surface may have exactly compensated for higher axial resistance of young roots located deeper in the profile. Data sets of the sort collected by van Bavel er al. (1968a,b), Arya er al. (1975a,b,c), Allmaras et al. (1975a,b), Taylor and Klepper (1975), and Sivakumar (1977) are needed especially for hourly, rather than daily, time periods. VI. Rooting Volume

The total quantity of water available at any one time for withdrawal by a plant increases with available soil water content and with volume of soil occupied by its roots. The total rooted soil volume enters the model in two ways. First, we include a term V, that is a specified volume of soil with uniform properties and rooting density. This soil volume varies with time and with planting geometry. In closely spaced rows, Vi will be the soil volume between two depths, such as between 0 and 15 cm in Fig. 11. In wider spaced rows (and especially early in the

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117

FIG. 11. A schematic representation of V, superimposed on root distribution of 44-day-old soybeans grown in 25-cm-wide rows on loess soil in western Iowa (after Bohm, 1977). Each dot represents one root projecting from a prepared trench wall.

growing season), Vi will be one of several strips of soil bounded by two depths, and by two distances from the row, such as that shown in Fig. 12. With isolated plants, V, can be represented by one of several concentric cylindrical shells bounded by two soil depths. The dimensions of V, vary with time. Second, soil volume, V, , enters the model during water uptake calculations. Water movement through soil into V, is calculated; then the product of V, and he,, the volumetric

FIG. 12. A schematic representation of V, superimposed on root distribution of 44-day-old soybeans grown in 100-cm-wide rows on loess soil in western Iowa (after Bohm, 1977). Each dot represents one root projecting from a prepared trench wall.

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H. M . TAYLOR AND BETTY KLEPPER

change in soil water content, is added; and finally water movement out of Vi through the soil pathway is subtracted to provide the total quantity of water extracted from soil volume Vi by plant roots. Plant species differ greatly in the shape and size of their root systems and in their water extraction patterns. Weaver (1920) showed that depth and lateral spread of roots for a particular species was modified substantially by environment. He also showed that species differ in their rooting patterns for a particular environment. For example, cactus (Opuntia spp.) roots occur mostly in the upper 30 cm of soil, with only a few anchorage roots penetrating below 0.5 m. These shallow roots are profusely branched and may spread laterally as far as 10-15 m from the plant base. Cactus root systems absorb a large proportion of their total water supply from small rainfalls. Conversely, mesquite (ProsopisjulifZoru) may root as deeply as 53 m (Phillips, 1963). These deep roots assure mesquite trees of a continuing supply of water even during long droughts. Cactus and mesquite thus coexist readily in climax vegetation sites. Weaver (1919, 1920, 1926), Weaver and Bruner (1927), and Kutschera (1960) have described lateral extent and depth of rooting for many plant species. The characteristic rooting pattern of each species is genetically controlled but environmentally modified. We shall discuss, in detail, idealized patterns for cotton (Gossypium hirsurum), a taprooted dicotyledonous plant, and maize (Zea mays), a fibrous-rooted monocotyledonous plant. We chose those two crops because their root systems have been studied extensively under several environments. When a cotton seed germinates, the primary root (taproot) forces its way through the micropyle and pushes downward into the soil (Tharp, 1960). The taproot often reaches the 20- to 25-cm depth before the shoot emerges and lateral roots develop. The taproot will continue to grow downward at rates up to 6 cdday (Taylor and Ratliff, 1969). The depth to which this primary root penetrates depends on the length of the growing season and on the soil environment it encounters (Pearson, 1974). Lateral roots radiate outward from the taproot and extend up to 2 m from isolated cotton plants. Lateral spread is much less when cotton is planted in rows, but roots of cotton, like those of soybeans (Bohm, 1977), probably interpenetrate among adjacent rows. Total root length and plant height increase with time until cotton bolls form. After that, plant height remains constant and total root length decreases because some roots die (Browning et al., 1975). The general pattern of maize (zea mays) root development contrasts sharply with that of cotton. The primary root and its enclosing sheath, the coleorhiza, elongate and break through the pericarp. The primary root soon breaks through the coleorhiza. About 40-55 hours after germination under favorable conditions, one to five, and occasionally up to thirteen (Wiggans, 1916) seminal lateral roots develop, and the coleoptile elongates upward (Kisselbach, 1949). Crown (nodal)

ROLE OF ROOTING CHARACTERISTICS

I19

roots then develop successively on six to ten nodes. Rooting depth increases with time at rates up to 7.7 c d d a y (Taylor et af., 1970) and finally reaches depths of about 2 m for a 2-m-tall, mature maize plant in loess soil. At that time, total root length may be as much as 10 km per plant (Kisselbach, 1949). Within a species, large plants have greater root lengths than small plants. The location of these roots within the soil depends on soil conditions and previous crop history. Plant tops and roots tend to be in some dynamic equilibrium, which can be shifted to a limited degree by stresses imposed on the plant. However, roots elongate fastest in soil volumes where conditions are most favorable. Thus, rapid elongation of a particular root segment depends on adequate supplies of photosynthates and growth regulators from shoots, and also on soil conditions around that particular root segment. These growth conditions cause drastic alterations both in the total rooted volume of soil and in the rooting density within that volume. A large quantity of literature is available on the effects of various soil factors on root elongation, and rooting density. For example, one book (Carson, 1974) reviews effects on root growth of soil temperature, structure, strength, oxygen, carbon dioxide, water, aqueous ammonia, pH, calcium, aluminum, copper, zinc, lead, boron, and manganese, and of rhizosphere biology including mycorrhizae and feeder root diseases. Other recent articles have shown that root growth is affected by soil salinity (Jensen, 1975), nematodes (O’Bannon and Reynolds, 1965), herbicides (Vorderberg, 1961), ethylene (Smith and Robertson, 1971), and nitrates, phosphorus, and potassium (Drew, 1975). We have compiled this partial listing of soil factors that affect rooting to illustrate the almost overwhelming complexity of the soil-root system. Despite these problems, some progress has been made in developing models that describe rooting densities as functions of soil conditions and time (Hackett and Rose, 1972; Lungley, 1973; Gerwitz and Page, 1974; Hansen, 1975; Lambert et af., 1975; Greacen and Hignett, 1976; Hillel et al., 1976). The soil-root system is much too complicated to use most of these models to describe field situations. Several of them (Hackett and Rose, 1972; Lungley, 1973; Hansen, 1975; Lambertet al., 1975; Hillelet al., 1976) predict elongation rates of individual roots or root systems from a knowledge of soil parameters. In the preceding paragraph, we listed twenty-four soil factors that affect root elongation rates and called this list incomplete. Taylor et af. (1972) attempted to predict the length of cotton taproots 100 hours after germination with only temperature, aluminum ion activity, and soil strength (penetrometer resistance) as experimental variables. Eight coefficients were needed to predict 68% of the variance in length at the end of less than 5 days’ growth. Yet, we need to predict soil volumes and rooting densities for the plant’s lifetime. There is hope, however, for some situations. Gerwitz and Page (1974) found that root dry weights decreased exponentially with depth in 71 out of 101 case

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H. M. TAYLOR AND BElTY KLEPPER

histories. Thus, we may be able to use this exponential relationship to predict rooting density with depth and time when once we have calibrated a particular plant species and soil profile. The exponential relationship fails when part of the soil zone occupied'by roots dries below some critical water potential. For example, Taylor and Klepper (1974) found that cotton rooting density decreased, regardless of other soil and plant factors, whenever soil water content decreased below 0.08 cm3/cd (+A=- 1 bar) (Fig. 13). Klepper et al. (1973) found that soil drying drastically shifted the relationship between cotton rooting density arid depth. Rooting density decreased linearly with depth at the start of a drying cycle but increased linearly with depth after 20 more days of water extraction. The relationship of rooting density with depth did not shift for a nearby soil profile that remained nearly at "field capacity" (Fig. 14). We believe that other types of intermittent soil stresses besides water status will affect the exponential pattern of rooting density. Therefore, much research is needed before we can model rooting volumes or rooting densities with satisfactory precision. VII. The Real World

All current models of water uptake by root systems contain assumptions that are not strictly valid for everyday field situations. We shall now discuss some real world problems that cause problems in applying Eqs. (1) through (10).

I

28

94

.2o

.is

I

.12

.oe

m

I

o

Water content (crn3/crn3)

FIG. 13. Rooting density (L) of cotton as a function of soil water content (0) for four depths of a uniform soil profile (Taylor and Klepper, 1974).

ROLE OF ROOTING CHARACTERISTICS

121

FIG. 14. Rooting density (I.,,) of cotton as a function of depth on two dates. The well-watered profile was maintained above - 1 bar soil water potential throughout the intervening period, while the drying profile soil water content decreased with time. (Klepper et al., 1973).

First, our and values may change up to 5 bars in a few minutes when a cloud passes over the experimental site (Stansell el al., 1973). We do not know how these rapid fluctuations of Jlp will affect I)r deep within the soil profile. We also do not know how these rapid water potential fluctuations affect transpiration. Second, we have assumed that all roots are uniformly spread within each soil volume V, . Even a cursory examination of a field soil profile shows that the roots often are concentrated along shear planes or ped surfaces, or in holes created by worms or roots of earlier plants (Taylor, 1974). In many highly structured soils, very few roots penetrate peds. Obviously, calculations of radial path length are virtually meaningless if they are based on average rooting density of V, . Our Eqs. (1) through (10) do not contain a path length parameter, but single-root models (Philip, 1957; Gardner, 1960; Cowan, 1965) do contain that parameter. Third, we have assumed that neither radial nor axial resistances differ among the root lengths within soil volume V,. Some models incorporate this assumption, but others assume that only new, white roots are effective in water uptake. We believe that the real world situation lies somewhere between these two extremes and probably varies depending on species, previous history, and environmental conditions. Many more data are needed to resolve the question about relative uptake rates of “old” and “new” roots. Fourth, we have assumed that soil properties within each volume Vi do not vary with direction, distance, or time, but do vary, uniquely, with water content; this is, of course, not true. Many field soils are highly structured, and surface properties of these structural units differ from those of the unit’s interior. Thus,

H. M . TAYLOR AND BETTY KLEPPER

122

radial resistance of soil along the pathway will vary from one location to another. Peds are not all uniform in shape, so that the number of ped surfaces (cutans) will vary with the direction in which they are counted. Soils exhibit hysteresis, and their properties do not vary uniquely with water content. Finally, we believe that any model of water uptake by roots should incorporate the feature that rooting density, L,,,changes with time, sometimes quite rapidly. A measure of Lo at one time during an experiment is not sufficient unless that L,, is used only for the 3 or 4 days before and after the sample date. We suppose that we again may have created a feeling of hopelessness about modeling water uptake by root systems in field situations. We do not agree that the situation is hopeless. It is complex and very difficult; however, most models benefit from the self-correcting feature that radial resistance varies inversely with soil water content. If, for a given time period, predicted water withdrawal is less than actual withdrawal, then predicted water content will be greater than actual content at the beginning of the next period. Then, predicted water extraction will be calculated using resistances that are lower than actual resistances. Thus, models tend to correct themselves during successive extraction periods. Advances in both computer hardware and programming techniques will allow us to use models with more parameters and shorter time increments. However, these computational advances require greater quantities of more precise data. Without these data banks, models of water uptake by root systems will remain academic exercises. Advances will be most rapid where teams of people, both “number-gatherers and “number-crunchers,” cooperate closely. ”

VIII. Factors That Man Can Control

Some factors that control water uptake by root systems can be modified. The researcher should examine the functioning soil-plant-atmosphere system in order to choose the particular approaches most likely to be successful for local field situations. One obvious method for modifying water uptake rate by root systems is to increase the soil water content around part, or all, of the roots. This greater soil water content results in greater qt ’s (Taylor and Klepper, 1975) and lessened radial resistances. The increased water content can be caused by increased soil water intake, reduced evaporation, and reduced deep drainage. We also have the option of reducing planting density (plants per area). This technique increases the soil volume available to each plant and thus increases its available water supply. Even though increased water supply will increase top growth, the plant will remain for a longer period in the state where leaf water potential is controlled mostly by plant, rather than soil, water factors (Fig. 4 versus Fig. 6).

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123

Soil profile characteristics can be improved so that plants increase the volume of soil occupied by their roots. We can disrupt high-strength soil layers that restrict rooting depth or rooting density at deeper depths (Taylor and Bruce, 1969). We can control wheel traffic that causes restricted rooting in the plowed layer between rows of crops (Trouse et al., 1975), and we can improve soil drainage where intermittent high water tables restrict rooting (Letey , et al., 1967). We can either increase or reduce surface soil temperatures to allow more thorough exploration of surface soil layers, especially when plants are young (Richards el al., 1952). We can control soil cultivations that cut off shallow roots. We can increase calcium supply where soil levels are too low to support rapid root elongation (Howard and Adams, 1965), lime soil to reduce aluminum toxicity (Adams and Lund, 1966), and leach soil to reduce salinity (Ayers et al., 1943). We can fertilize soil to increase plant size, thus increasing total root length and often increasing rooting depth (Black, 1966), and we can apply pesticides to control pathogens that restrict rooting (O’Bannon and Reynolds, 1965). We sometimes can also control pathogens through certain kinds of tillage operations, thus increasing rooting depth and density with depth (Lyda and Burnett, 1975; Rea, 1939). Plant root systems may also be altered through plant breeding or selection. Zobel (1975) estimated that 30% of tomato (Lycopersicon esculentum Mill.) genes affect some aspect of root development and that 6% of a tomato population contained root mutants that were not coupled to any shoot character. Thus, mankind has the opportunity to alter plant root system characteristics independent of shoot characteristics. These altered root parameters may alter diurnal or seasonal patterns of leaf water potential. We shall now discuss some possibilities that are being investigated. Passioura (1972) suggested that cereals grown under dryland conditions should be selected for a small number of seminal roots and for a small diameter of metaxylem vessels in these seminal roots. His logic was that resultant high axial resistances would reduce water uptake sufficiently to restrict leaf area. The reduced leaf area would ration the available water to allow some seed production, even if no rain fell during the growing season. If the land surface were wetted by rainfall, adventitious roots would form, axial resistance would decrease substantially, water uptake would increase, and the leaves would develop normally. Meyer (1976) found significant varietal differences in radii of metaxylem vessels of wheat seminal roots and in numbers of seminal roots. Thus, it is possible to select wheat plants for high or low axial root resistance. However, high axial resistance is often considered an undesirable characteristic. Many grasses used to provide green forage for animals produce more forage when daytime t,bt is high than when it is low. Low axial resistances tend to keep t,bt high for longer periods in a drying cycle, especially for deeply rooted plants. Further

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research is needed on manipulating axial resistances of grasslike plants and on implications of axial resistance for yield under a range of environmental conditions. Further research is also needed on methods of altering axial resistances of dicotyledonous plants. Earlier we mentioned an experiment (Willatt and Taylor, 1978) where soybeans were grown in western Iowa on a deep loess soil. Even though “available” water and roots both were located at depths below 1.5 m, midday leaf water potentials were significantly lower than those of nearby irrigated soybeans. Presumably, these midday potentials would have been higher if axial resistance had been less. Decreased axial resistances would not have eliminated severely depressed midday leaf water potentials, however. The soil profile was near the -15 bar & value to depths greater than 1.5 m when midday potentials were depressed the most compared with nearby imgated plants. Thus, water withdrawal was concentrated in a few deep soil layers. The soybeans needed, in addition to lower axial resistances, either great intake for each existing root (high 4 i ) or many roots (high L.v) to supply sufficient water for transpiration at high i,bl ’s during midday. We may be able to manipulate qf , on either a short-term or a long-term basis. Several authors (Brouwer, 1965; Stoker and Weatherley, 1971; Barrs, 1973; Hailey et al., 1973; Lawlor and Lake, 1976) have shown that “root resistance” (a combination of axial and radial resistance) may or may not vary with flow rate, depending on circumstances surrounding the experiment. In addition, Parsons and Kramer (1974) have shown that “root resistance” is lower during the day than at night. It is conceivable that both day-night and flow rate effects on “root resistance” are metabolically linked and can be changed by some type of foliar spray. In the long-term situation, plants probably can be bred or selected for greater or lesser q1’s. More information is needed about radial root resistance and the factors that control it before we can determine whether it will be useful or practical to alter qi in field situations. Nearly all the currently available “root resistance” data are difficult to interpret for qr data because of the confounding effects of axial resistance. We can also manipulate the partitioning of photosynthate into tops and roots. For example, wheat (Triricurn aestivum L.) plants with a particular top weight can be selected for significant variations in their root weights (MacKey, 1973). For a given root weight, root lengths can vary significantly among soybean [Glycine m u (L.) Merr.] isolines (Allmaras et al., 1975b). Thus, plants with a specific top size will have varying amounts of root length, depending on both genetic potential and environment (Hurd, 1974; Zobel, 1975). Hurd (1974) has used these principles in developing Pitic, a durum wheat (Triticum durum L.) variety obtained from crossing and backcrossing Pelissier onto Lakota. Pelissier has a root system with high rooting density (high L), and Lakota has a sparse root system but is disease-resistant. The three lines that reached final stages of

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even though Lakota made up three-fourths of the yield testing all had high L,, parentage. We believe that breeding and selection can increase the total annual supply of water in deep soils that recharge annually by increasing volume of soil explored by roots even where no obvious soil problems occur. Species have different genetic potentials for extending into less favorable soil volumes. For example, roots of peanut (Arachis hypogaea L.) can penetrate soil horizons that have aluminum ion activities that stop root growth of cotton (Adams and Pearson, 1970). Differential tolerance of root growth to aluminum ion activity also can be found among the varieties of a particular species. Foy et al. (1974) found large differences in root growth among thirteen genotypes of sunflower (Helianrhus annuus L.) and suggested that a breeding program could develop varieties that had even higher aluminum tolerances. These future varieties should have an increased water supply when grown in locations where acid subsoils reduce rooting volume. IX. A Final Thought

We have (a) presented a model of water uptake by root systems, (b)discussed the components of that model, (c) shown how situations in the real world differ from those inherent in models, and (d) discussed techniques for, and possible consequences of, altering various components of the model. One task remains-to provide, in a few words, an overview of our efforts. We believe that mankind has many opportunities for changing rooting characteristics of plants to benefit their water status. An additional word of caution seems appropriate, however. We may sometimes desire to decrease some parameter, but in other situations we may wish to increase the same parameter. For example, consider radial root resistance of wheat. In semiarid or arid situations, we may wish to increase radial resistance in order to ration an available water supply. However, in humid environments we may want to reduce radial resistance in order to prevent plants from undergoing large decreases in midday water potential. The reduced diurnal dip in water potential might increase leaf area and thus increase forage or grain yield. Only a few of the techniques that we have discussed will be applicable for any particular situation. The researcher must examine closely plants, soils, and environments in order to arrive at the most logical choice of a technique to alter plant water status in a beneficial manner. REFERENCES Adarns, F., and Lund, Z. F. 1966. Soil Sci. 101, 193-198. Adams, F., and Pearson, R. W. 1970. Agron. J . 62, 9-12.

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Allmaras, R. R., Nelson, W. W., and Voorhees, W. B. 1975a. Soil Sci. SOC. Am., Proc. 39, 764-771. Allmaras, R. R., Nelson, W. W., and Voorhees, W. B. 1975b. Soil Sci. Sor. Am., Proc. 39, 771-777. Anderson, W. P., and Reilly, E. J. 1968. J . Exp. Bot. 19, 19-30. Arya, L. M., Farrell, D. A., and Blake, G. R. 1975a. Soil Sci. SOC.Am., Proc. 39, 4 2 4 4 3 0 . Arya. L. M., Blake, G. R., and Farrell, D. A. 1975b. Soil Sci. Soc. Am., Proc. 39, 430-436. Arya, L. M., Blake, G. R., and Farrell, D. A. 1975c. Soil Sci. SOC. Am., Proc. 39, 437-444. Ayers, A. D., Wadleigh, C. H., and Magistad, 0. C. 1943. J . Am. Soc. Agron. 35, 796-810. Barley, K.’P. 1971. “Encyclopedia of Science and Technology,” 3rd ed. McGraw-Hill, New York. B m s , H. D. 1973. In “Plant Response to Climate Factors” (R. 0. Slatyer, ed.), pp. 249-258. UNESCO, Paris. Bell, C. W., and Biddulph, 0. 1963. Plant Physiol. 38, 610-614. Black, C. A. 1966. In “Plant Environment and Efficient Water Use” (W. H. Pierre el al.. eds.), pp. 177-206. Am. SOC.Agron., Madison, Wisconsin. Bohm, W. 1977. Z. Acker- Pflanzenbau 144, 103-112. Boyer, J. S. 1976. Philos. Trans. R . SOC.London. Ser. B 213, 501-512. Briggs, G. E. 1967. “Movement of Water in Plants.” Blackwell, Oxford. Brouwer, R . 1965. Symp. SOC.Exp. Biol. 19, 131-149. Browning, V. D., Taylor, H.M., Huck, M. G., and Klepper, B. 1975. Ala.. Agric. Exp. S i n . . Bull. 467. Byrne. G. F., Begg. J. E., and Hansen, G. K. 1977. Agric. Meteorol. 18, 21-25. Campion, W. E. 1926. “The Depth Attained by Roots.” Aust. For. J . Sydney. Carson, E. W. 1974. “The Plant Root and Its Environment.” Univ. of Virginia Press, Charlottesville. Clarkson, D. T. 1974. “Ion Transport and Cell Structure in Plants,” pp. 209-210. Wiley, New Y ork . Clarkson, D. T., and Sanderson, J. 1974. In “Structure and Function of Primary Root Tissues” (J. Kolek, ed.), pp. 87-100. VEDA Publ. House, Bratislavia. Cole, P. J., and Alston, A. M. 1974. Plant Soil 40, 243-247. COWZUI, I. R. 1965. J . Appl. EcoI. 2, 221-239. Dimond, A. E. 1966. Plant Physiol. 41, 119-131. Drew, M. C. 1975. New Phytol. 15: 479490. Emerson, W. W. 1954. J. Agric. Sci. 45, 241-245. Fiscus, E. L. 1977. J. Exp. Bot. 28, 71-77. Foy, C. D., Orellana, R. G., Schwartz, J. W., and Fleming, A. L. 1974. Agron. J . 66, 293-296. Gardner, W. R. 1960. Soil Sci. 89, 63-73. Genvitz, A., and Page, E. R. 1974. J . Appl. Ecol. 11, 773-782. Greacen, E. L., and Hignett, C. T. 1976. “A Water Balance Model and Supply Index for Wheat in South Australia,” Tech. Pap. No. 27. Div. Soils, CSIRO, Adelaide, Australia. Greacen, E. L., Ponsana, P., and Barley, K. P. 1976.h “Water and Plant Life” (0.L. Langeet al., eds.), pp. 86-100. Springer-Vedag, Berlin and New York. Hackett, C., and Rose, D. A. 1972. Aust. J. Biol. Sci. 25, 669-679. Hailey, J . L., Hiler, E. A , , Jordan, W. R., and van Bavel, C. H. M. 1973. Crop Sci. 13, 264-267. Hansen, G. K . 1975. Acra Agric. Scand. 25, 129-149. Hellkvist, J., Richards, G. P., and Jarvis, P. G. 1974. J . Appl. Ecol. 11, 637-667. Hillel, D. 1975. Soil Sci. 120, 230-237. Hillel, D., T a l p , H., and van Keulen, H. 1976. Soil Sci. 121, 242-255. Howard, D. D., and Adams, F. 1965. Soil Sci. SOC.Am., Proc. 29, 558-562. Hsiao, T. C. 1973. Annu. Rev. Plant Physiol. 24, 519-570.

ROLE OF ROOTING %HARACTERISTICS

I27

Hsiao. T. C., Acevado, E.. Fereres, E., and Henderson, D. W. 1976. Philos. Trans. R . Sac. London, B Ser. 213, 479-500. Hubbard, J. W. 1931. J. Agric. Res. 44, 39-47. Huck, M. G., Klepper, B., and Taylor, H. M. 1970. Plant Physiol. 45, 529-530. Hurd, E. A. 1974. Agric. Meteorol. 14, 39-55. Jarvis, P., and House, C. R. 1969. J. Exp. Bot. 20, 507-515. Jarvis, P. G. 1975. In “Heat and Mass Transfer in the Biosphere. Vol. 1. Transfer Processes in the Plant Environment” (D. A. de Vries and N. H. Afgan, eds.), pp. 369-394. Wiley, New York. Jensen, C. R. 1975. Acra Agric. Scand. 25, 3-10. Kisselbach, T. A. 1949. Nebr.. Agric. Exp. Stn.. Res. Bull. 161. Klepper, B., Taylor, H. M., Huck, M. G., and Fiscus, E. L 1973. Agron. 1. 65, 307-310. Klute, A. 1973. SSSA Spec. Publ. 5, 9-35. Kramer, P. J. 1937. Am. J. Bot. 24, 10-15. Kutschera, L. 1960. “Wurzelatlas.” Dtsch. Landw. Ges., Frankfurt, West Germany. Lambert, J . R., Baker, D. N., and Phene, C. J. 1975. “Simulation of Soil Processes Under Growing Row Crops,” Pap. 75-2480. Am. SOC.Agric. Eng., St. Joseph, Michigan. Lawlor, D. W., and Lake, J. V. 1976. J. Appl. Ecol. 13, 639-646. Letey, J., Stolzy. L. H., and Kemper, W. D. 1967. In “Irrigation of Agricultural Lands” (R. M. Hagan et a / . , eds.), pp. 941-949. Am. SOC.Agron., Madison, Wisconsin. Lungley, D. R. 1973. Plant Soil 38, 145-159. Luxova, M., and Kozinka, V. 1970. Biol. Plant. 12, 47-57. Lyda, S. D., and Burnett, E. 1975. In “Biology and Control of Soil-Borne Plant Pathogens” (G. W. Bruehl, ed.), pp. 63-68. Am. Phytopathol. Soc., St. Paul, Minnesota. MacKey, J. 1973. Proc. I n t . Wheat Genet. Syrnp., 4th, 1973 pp. 827-842. Mathers, A. C., and Welch, N. H. 1964. Agron. J . 56, 313-315. Meyer, W. S. 1976. Ph.D. Thesis, University of Adelaide., Adelaide, Australia. Newman, E. I. 1976. Philos. Trans. R . Soc. London, Ser. B 213, 463-478. Nobel, P. S . 1970. “Plant Cell Physiology: A Physiochemical Approach.” Freeman, San Francisco, California. O’Bannon, J . H., and Reynolds, H. W. 1965. Soil Sci. 99, 251-255. Ogston, A. G. 1958. Faraday Soc. Trans. 54, 1754-1757. Parsons, L. R., and Kramer, P. J. 1974. Physiol. Plant 30, 19-23. Passioura, J. B. 1972. Aust. J. Agric. Res. 23, 745-752. Pearson, R. W. 1974. In “The Plant Root and Its Environment” (E. W. Carson, ed.), pp. 247-270. Univ. of Virginia Press, Charlottesville. Philip, J. R. 1957. Congr. Int. Commun. Irrig. Drainage, 3rd, 8, pp. 125-154. Phillips, W. S. 1963. Ecology 44, 424. Ponsana, P. 1975. Ph.D. Thesis, University of Adelaide, Adelaide, Australia. Rea, H. E. 1939. Tex.. Agric. Exp. Stn., Bull. 513. Richards, S . J., Hagan, R. M., and McCalla, T. M. 1952. In “Soil Physical Conditions and Plant Growth” (B. T . Shaw, ed.), pp. 303-480. Academic Press, New York. Richter, H. 1973. J. Exp. Bot. 24, 983-994. Ritchie, J. T., Burnett, E., and Henderson, R. C. 1972. Agron. J. 64, 168-173. Sivakumar, M. V. K. 1977. Ph.D. Thesis, Iowa State University, Ames. Smith, K. A,, and Robertson, P. D. 1971. Nature (London) 234, 148-149. Stansell, J. R., Klepper, B., Browning, V. D., and Taylor, H. M. 1973. Agron. J. 65, 677-678. Stoker, R., and Weatherley, P. E. 1971. New Phytol. 70, 547-554. Talboys, P. W. 1968. In “Water Deficits and Plant Growth” (T. T. Kozlowski, ed.), Vol. 2, pp. 255-304. Academic Press, New York. Taubenhaus, J. J., Ezekiel, W. N., and Rea, H. E. 1931. Plant Physiol. 6, 161-166.

128

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Taylor, H. M. 1969.Ala., Agric. Exp. Srn., Circ. 171. Taylor, H. M. 1974.I n “The Plant Root and Its Environment” (E. W. Carson, ed.), pp. 271-291. Univ. of Virginia Press, Charlottesville. Taylor, H. M., and Bruce, R. R. 1969.Trans. Inr. Congr. Soil Sci.. 9rh, 1968 Vol. 1, pp. 803-81 1. Taylor, H.M., and Klepper, B. 1971.Ausr. J . Biol. Sci. 24, 853-859. Taylor, H. M., and Klepper, B. 1974.Agron. J. 66, 584-588. Taylor, H. M., and Klepper, B. 1975.Soil Sci. 120, 57-67. Taylor, H. M., and Ratliff, L. F. 1969.Soil Sci. 108, 113-119. Taylor, H. M., Huck, M. G . , and Klepper, B. 1972.I n “Optimizing the Soil Physical Environment toward Greater Crop Yields” (D. Hillel, ed.), pp. 57-77.Academic Press, New York. Taylor, H. M.. Huck, M. G., Klepper, B., and Lund, Z.F. 1970.Agron. J . 62, 807-809. Taylor, S. A., and Cary, J. W. 1961.Trans. Inr. Congr. Soil Sci., 7rh, 1969 Vol. 1, pp. 80-90. Tharp, W. H. 1960.US.Dep. Agric., Agric. Handb. 178. Tinker, P. B. 1916.Philos. Trans. R . SOC.London, Ser. B 213, 445-461. Trouse, A. C., Jr., Dumas, W. T., Smith, L. A., Kummer, F. A., and Gill, W. R. 1975. “Residual Effects of Banier Removal for Root Development.” Paper 75-2534.Am. Soc.Agric. Eng., St. Joseph, Michigan. Vaadia, Y. 1976.Philos. Trans. R . SOC.London, Ser. B 213, 513-522. van Bavel, C. H. M., Stirk, G. B., and Brust, K. J. 1968a.Soil Sci. Soc. Am., Proc. 32, 310-316. van Bavel, C.H. M., Brust, K. J., and Stirk, G. B. 1968b. Soil Sci. SOC.Am., Proc. 32, 317-321. Vorderberg, K. 1961.Nachrichten bl. Dtsch. Pflanzenschundiensres (Berlin) [N. 5.1 IS, 68-70. Waggoner, P. E., and Dimond, A. E. 1954.Am. J. Bor. 41, 637-640. Weaver, J. E. 1919.Carnegie Insr. Washington Publ. 286. Weaver, J. E. 1920.Carnegie Insr. Washington Publ. 292. Weaver, J. E. 1926. “Root Development of Field Crops.’’ McGraw-Hill, New York. Weaver, J. E., and Bruner, W. E. 1927. “Root Development of Vegetable Crops.’’ McGraw-Hill, New York. White, E. M. 1975.Soil Sci. 119, 461465. Wiggans, R. G. 1916.3.Am. Soc. Agron. 8, 31-37. Willatt, S. T., and Taylor, H. M. 1978.J . Agric. Sci., 90, 205-213. Wilson, A. M., Hyder, D. N., and Briske, D. D. 1976.Agron. J . 68, 479484. Wind, G.P. 1955a. Nerh. J. Agric. Sci. 3, 60-69. Wind, G. P. 1955b.Nerh. J . Agric. Sci. 3, 259-264. Zobel, R. W. 1975.In “The Development and Function of Roots” (J. G. Torrey and D. T. Clarkson, eds.), pp. 261-275. Academic Press, New York.

ADVANCES IN AGRONOMY, VOL. 30

HYBRID COTTON: SPECIFIC PROBLEMS AND POTENTIALS Dick D. Davis Department of Agronomy, New Mexico State University, Las Cruces, New Mexico

I. Introduction ............................................................ 11. Heterotic Expression of Cotton Hybrids.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. General Considerations ............................................... B. Levels of Heterosis . . . . . . . . . . . . . . ........................ C. Yield Components and Heterosis . . . D. Heterosis for Seed Yield . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Effects of Heterosis on Phenology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Vegetative Vigor .................................................... B. Seedling Vigor.. . . . . . . . . . . . . ................................. C. The Plant Canopy ................................................... D. Earliness Interactions . . . . . . . IV. Plant Type and Harvest Efficiency A. Problem Phenotypes ................................................. B. Usefulness of Short-Branch Phenotypes .................................. V.

VI.

VII. VIII.

IX.

X. XI.

130 131 131 131 133 134 134 136 136 137 138 138 138 139 139 Pest Resistance Potential for Hybrids 140 A. Insect Resistance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . 140 B. Disease Resi 142 Fiber Properties o .................. 142 A. G.hirsutum ................................... 142 B. G . hirsutum 143 Breeding Hybrids WI ..................... 144 The Production of Hybrid Seed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 147 A. Genetic and Cytoplasmic Male Sterile Systems.. . . . . . . . . . . . . . . . . . . . . . . . . . . 147 B. Pollination of Male Sterile Cotton . . . . . . . . . . . . . 148 The Association of H 150 A. Yield Levels. . . 150 B. Problems Associated with Heavy Pubescence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 151 Breeding Methodology ................................................... 152 Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153 References ............................................................. 153

IJoumal article No. 638, Agricultural Experiment Station, New Mexico State University, Las Cmces, New Mexico.

129 Copyright 0 1978 by Academic Press. Inc. All rights or reproduction in any form E S Z N C ~ . ISBN 0- 12-ooO730-4

130

DICK D. DAVIS I. Introduction

A quarter-century has passed since Loden and Richmond (195 1) gave a comprehensive review on hybrid vigor in cotton. Since that time, several aspects of basic hybrid research have advanced greatly. In fact, the technology required to produce commercial hybrid cotton was developed only in the last decade. The profit potential in hybrid cotton is so large that Indian seedsmen marketed considerable quantities of seed in 1974, produced by hand emasculation and pollination. The seed sold for prices starting at $6.50 per kilogram (Delouche, 1975). Yield increases in commercial fields have ranged from 7.5 to 37 quintals per hectare of seed cotton (Sundaram, 1975). Profitability in hand-crossed commercial seed is the ultimate testimonial to the value of cotton hybrids. Theoretically, the breeder now has in hand all the tools necessary to produce large quantities of bee-pollinated hybrids. The purpose of this chapter is to show that the promise of reward is very great even though completion of the task may be difficult. The development of successful hybrids usually necessitates three breeding programs in parallel: (a) one to develop successful male sterile female parents, usually as pairs of isogenic A (male sterile) and B (fertile) lines, (b) another to develop promising fertility-restoringmale parents (R lines), and (c) an extensive testing program to isolate the best combinations out of the thousands that are possible. Success in a hybrid program is not simply a matter of obtaining yield and fiber quality in a single hybrid but also requires attention to a multiplicity of qualitative and quantitative factors, such as earliness, disease and storm resistance, plant height, and plant shape. Sufficient basic research has been done on some of these factors to predict accurately the chances of success in transfening useful properties into the prospective parents of future hybrids. The physical process of transferring these important factors has only begun in the last five years in the case of hybrid parents, whereas pedigree selection breeding programs conducted in many state universities and private companies have been working with these same factors for 50 years or more. Therefore, the “pure line” cultivars have a half-century lead time over hybrids in developing the proper balance of agronomic and fiber traits required to produce successful commercial cultivars. However, since the breeder of hybrids will be able to draw upon the experience of basic research of the last fifty years, hybrids should advance rapidly. The timetable for release of the first hybrids can only be estimated at present. Breeders who obtained the original Gossypiurn harknessii male sterile and restorer stocks when they first became available may have already developed 10th-backcross A and B lines and 6th-backcross R lines. The testing of cross combinations on a systematic basis could begin in 1978. The first commercial prototype hybrids could appear by 1981, barring unforeseen difficulties.

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II. Heterotic Expression of Cotton Hybrids

A. GENERAL CONSIDERATIONS

The biggest incentive for attempting the production of hybrid cotton is to take advantage of the considerable heterosis that is already known to exist in the crop. A recent review on heterosis in crop plants listed cotton as showing very low heterosis (Sinha and Khanha, 1975). However, this review ignored the bulk of recent literature, which shows that the best F, hybrids have exceeded commercial check varieties by as much as 138% (Patel, 1971). Hybrid vigor in cotton is not necessarily associated with parents that show inbreeding depression. Simpson (1954) compiled beltwide data showing that cotton was an often-cross-pollinated species. In spite of the fact that high levels of cross-pollination may occur, cotton cultivars are not greatly divergent from self-pollinated species in their response to inbreeding depression. Kearney (1923) found no effect of inbreeding upon the fertility of Pima cotton. Young and Murray (1966) and Brown (1942) did record some inbreeding depression in upland cotton, but the effect was small. Simpson and Duncan (1953) generally confirmed that small but measurable yield reductions occurred when highyielding cultivars of upland cotton were subjected to continued self-pollination. Apparently many cultivars easily adapt to self-pollination, since out-crossing has been reduced to nearly zero at some locations (Meredith and Bridge, 1973). Inbreeding need be used only to the extent of producing uniform parental strains. Named varieties are usually sufficiently pure to serve as hybrid parents, although most varieties have some residual variability (Simpson and Duncan, 1953; Thomson, 1973). The highest-yielding cultivars usually produce the highest-yielding hybrids. This pattern applies to intra-hirsufum hybrids (Hawkins et al., 1965; Miller and Lee, 1964; Marani, 1963) and to interspecific hybrids (Omran et al., 1974). The same trend is seen in other papers, where the correlation between high-yielding parents and outstanding hybrids was not specifically pointed out by the authors.

B. LEVELS OF HETEROSIS

Some investigators such as Thomson (1971), Miller and Lee (1964), and Hawkins et al. (1965) have noted that the percentage of heterotic yield increase may be greater at low yield levels than at maximum yield levels. Thus, the absolute magnitude of yield increase may be more important than the percentage increase, so both figures are included in Table I, which lists the most significant reports of heterosis in cotton. The yield results are arranged in order of the

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TABLE I Heterosis for Yield. Superiority of the Best F, Hybrid over the Best Commercial Check in Net Yield and Percentage Increase

Investigator

Commercial check comparison

Check yield level (kidha)

Best F, hybrid net increase over check (kidha)

A. Interspecific Hybrids (G. hirsutum X G . barbadense)“ 520 Coker-100 A 1040 Marani (1967) 394 Acala 15 17-C 890 Barnes and Staten (1961) 198 Laxmi 579 Katarki (1971) 189 Fryxell er al. (1958) Acala 1517-C 895 b Omran er al. ( 1974) Coker 100 WR b b Acala 15 17-C b Stroman (1961) 400 Bulg. 3279 Karev (1969) E Christidis (1955) Local cultivars C Patel (1971) Thomson ( 197 I ) Marani (1968 ) Hawkins er al. (1965) Meredith and Bridge (1972) White and Richmond (1963) Jones and Loden ( I95 I ) Miller and Marani (1963) Turner (1953a) Kime and Tilley (1947)

B. Intraspecific G . hirsurum Hybrids” 662d Gujurat 67 Stoneville 7A I622 Coker IOOA 1640 pope 875 Deltapine 16 913 Acala 4-42 1040 Pandora 572‘ Coker 100 888 Pandora b Stoneville 4B b

915 27 I 260 192 138 I05 77r NS b b

Performance percentage increase

50 44 34 21 41 38

l

I38 17 16 22 12 10 14 34 13

“Further excellent work has been reported in abstracts of Indian, Bulgarian, and Soviet research. Without access to original data it is not possible to tabulate the amount of heterosis in these studies. bYield per unit area not directly computable. Data reported on plots of unspecified size. CChristidis’best F, combination was G. hirsurum X ( G . hirsurum X G . barbudense). Seed cotton yield increase only. The hybrid was lower in lint yield, but exact lint percentage was unavailable. dYield reported in seed cotton. Converted to lint at gin out-turn reported at 33.5% for the hybrid. ‘Yield reported in seed cotton. These were arbitrarily converted to lint yields at a lint percentage of 35.

absolute increment in yield in kilograms per hectare. The highest absolute increments reported for interspecific hybrids have exceeded 500 kg/ha, or about 1 bale per acre. Levels of heterosis are reported in various ways, with some investigators prefemng to use the mid-parent as the base line and others the better parent as the basis of comparison. Meredith and Bridge (1972) suggest the term “useful heterosis” for comparing the yields of hybrids to the highest-yielding, adapted commercial check cultivar. “Useful heterosis” has direct economic meaning,

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and where not specified otherwise heterosis will mean “useful heterosis.” Some of the original papers reported higher levels of heterosis for the combinations listed here since the basis of comparison was generally the mid-parent. I have chosen to compare all the hybrids in a given test with the outstanding commercial Gossypium hirsutum check variety also included in that test. These comparisons are not difficult to make, as high-yielding commercial varieties have often been used as one of the parents of an experimental hybrid. The yields of interspecific hybrids have been reported to be as much as 80% above commercial levels, as compared with a 0-128% increase reported for intraspecific hybrids. Soviet investigators also claim yield increases up to 50% with interspecific hybrids (Anonymous, 1973). Since the range of heterosis in interspecific hybrids approximately equals the levels found in intra-hirsutum hybrids, both types should merit considerable attention. Such spectacular results will not be expected on a commercial scale, since most of these tests have been conducted on very small plots and harvested by hand.

C. YIELD COMPONENTS AND HETEROSIS

A simplified cotton yield model can be represented by bollshnit area X seed cottodboll X lint percentage (Ken-, 1966). The nature of heterosis in Gossypium has been partly clarified, and it appears that hybrid vigor affects different yield components in intraspecific versus interspecificcrosses. In G. hirsutum x G. barbadense crosses the primary component of heterosis is the number of bolls produced per unit area (Marani, 1963, 1964, 1967; Fryxell et al.. 1958; Davis, 1974), whereas in G. hirsutum intra-specificcrosses this component, although still the most important, is greatly moderated (Miller and Marani, 1963; Turner, 1953a, Harris and Loden, 1954), and heterosis for boll weight may contribute significantly to the yield model (Thomson, 1971). Interspecific hybrids exhibit negative heterosis’ for lint percentage (Fryxell et al., 1958; Omran et al., 1974; Marani, 1963, 1967). This is due to the fact that the seed index (g/100 seed) is markedly increased (Marani, 1963, 1967), whereas the lint index (g lint/100 seed) is increased only slightly. This effect is generally overcompensated for by the bolls-per-unit-area component of yield, and low lint percentage should not be regarded as a real problem for two reasons: (a) There are many combinations in which the negative heterosis for lint percentage is relatively small and does not seriously affect overall heterosis for lint yield. (b) Low lint percentage means that the percentage of heterosis for seed yield will be greater than the seed cotton yields would indicate. ‘The F, decrease in the absolute numerical value of a character relative to the mean for the parents.

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D. HETEROSIS FOR SEED YIELD

The heterosis for seed yield is important, since cottonseed now used for animal feed may eventually be partially diverted to human food. Cottonseed flour produced by the liquid cyclone process with the gossypol removed is an excellent and valuable food product. Thus, we should consider the outstanding seed yield as an asset favoring hybrids. A pilot plant erected by the Plains Cooperative Oil Mill, Lubbock, Texas, has demonstrated that the liquid cyclone process can produce commercial quantities of cottonseed protein concentrates. Design problems still exist, however, and further investments in research and development are required before cottonseed refining can become a feasible commercial venture (Ed Breihan, manager, personal communication). In any discussion of cottonseed protein for human food, the glandless genotype must be considered. Here it will only be mentioned in passing for several reasons. Glandless hybrids will eventually emerge, but there is no reason for assuming that glandless hybrids will be easier to develop than glandless cultivars, and as yet there is no appreciable acreage devoted to glandless cultivars after a generation of research. The literature on this subject is already voluminous. The extreme susceptibility of glandless toLygus and other key insects points up the glaring need to incorporate some type of insect resistance into glandless stocks (Tingey et al., 1975; Jenkins, 1978). 111. Effects of Heterosis on Phenology

Hybrid vigor in cotton can be further divided into numerous developmental components. Some of these would be germination, emergence, rate of internode (both vertical and horizontal) formation, internode elongation, time and rate of square formation, flowering and fruit setting, boll growth and maturation, rate of leaf formation, and extent of leaf expansion. Traits other than direct yield components have important and often complex secondary influences on plant development, yield, and fiber properties. The correct balance will have to be maintained between these components of vigor to obtain maximum production. Table II shows the pattern of general combining ability for agronomic traits in interspecific hybrids. The heterotic responses exceed the parental range in several traits and for some traits heterosis is in an undesirable direction. In most interspecific crosses, for example, there is a tendency for the hybrid to maintain excessive vegetative vigor at the expense of the fruiting components. The optimum plant conformation may be variable, depending on the cultural requirements, but the most highly productive hybrids listed in Table I are tall, broad, long-branched plant types. Hybrids to be used in narrow row culture would have to be smaller and quite different in conformation (Brashears et al., 1968; Ray and Hudspeth, 1966; Wanjura and Hudspeth, 1963). Attention will also have to be given to the fiber properties of hybrids, particu-

TABLE I1 Generalized Heterotic Response in Certain Agronomic and Fiber Properties of G. hirsutum X G . barbadense Hybrids Character

Seedling vigor

Response evaluation

Plant i.haracters Asset-early attainment of adequate framework for fruiting. Liability or neutralaepends on SCA

Overall plant height Node number Node length Leaf size Petiole hair Bract size Boll size

Neutral Liability-plant too rangy Liability-leaf/fruiting index too high Neutrrl Liability---niay contribute to trash Neutral~onipensationsmade in flowering, shedding

Boll number

Asset-primary

Lock number Seeds per troll

Neutral Liabiiity-increases number of bolls required to produce I kg of lint Liability- m r e seed cotton required to produce 1 kg of lii:t (hut text)

rates

Lint pcrcenrage

yield component

Fiber finencss Fiber length

Fiber properties Variable4epcnds on end-use requirements Neutral to liability-depends on end-use requirements

Fiber maturity Length uniformit) Fiber strength

Neurral4epends on SCA Neutral Asset-high strength important to most end uses

Source

Barnes and Staten (1961) Ware (1930), Barnes and Staten (1961), Marani (1967), Davis (1973) Ware (1930). Kearney (1923b) Ware (1930). Kearney (1923b), Davis (1973) Kearney (1923b) Kearney ( 1923b) Kearney ( I923b) Marmi( 1963. 1967),Davis( 1973).Fryxellrrci/. (19.58). Barnes and Staten (1961) Marani (1963. 1967). Fryxell ef d.(19.58). Davis (1973). Omran rt a/. ( I 974) Kearney ( I 923b) Marani (1963. 1967) Marani (1963, 1967). Fryxell rt al. (19.58). Davis (1973). Omran et al. (1974) Fryxell et al. (1958). Marani (1968d), Davis (1974) Fryxell ef al. (1958), Kearney (1923), Barnes and Staten (1961) Fryxell et a / . (1958) Fiyxell et a / . (1958). Davis (1974) Fryxell er a/. (1958). Marani (1968d). Davis (1976)

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larly interspecific hybrids. In the United States, the Southeast, the Delta, the Plains, and the Irrigated West are distinct regions utilizing different cultivars. No single hybrid combination can be expected to fill all the specifications needed for localized growing conditions or fiber end uses. It will be necessary to produce hybrids of several classes according to objectives and problems distinctive to each class. A. VEGETATIVE VIGOR

In areas where hand-thinning and hand-picking are still economically feasible, large-statured hybrids will not be a great problem. However, to take advantage of the heterosis in interspecific crosses in mechanized operations, it will be necessary. to control the growth habit of the Fl plant. Indications are that G. barbadense-G. hirsururn Fl ’s generally exceed the larger parent in height (Barnes and Staten, 1961; Marani, 1967). This height increase is primarily due to lengthening of internodes, as the number of internodes does not differ greatly from that in the higher parent (Ware, 1930; Kearney, 1923a; Davis, 1974). Kearney (1923b) indicates that the fruiting branches are usually quite long, resembling the G. barbadense parent in this respect. The generalized Fl interspecific hybrid, therefore, is a tall, luxuriant plant, which, despite its great productivity, is not suited to modem mechanized culture. In addition to cultural and harvesting difficulties, excessively vegetative plants are associated with late maturity, although plant vigor of the hybrids may sometimes be variable on different types of soil (Uzenbaev, 1967). The generalized agronomic problem is to “hold” the vegetative vigor of the plant in check, while increasing the productivity. There are a number of approaches to use in controlling the vegetative vigor of the F, hybrid. Highly effective qualitative genes that have a direct effect on plant habit include: (a) okra leaf Lo, ( b ) short fruiting branch (cl, or d 2 ) ,and ( c ) early dwarf (not symbolized, probably two or three major genes). Early dwarf genes can be handled qualitatively, since they are easily transferred and are partially dominant in the F1 (Davis, 1974). First indications are that incorporation of one or two of these traits can “reduce” an interspecific F1to a stature smaller than that of our best commercial G. hirsutum cultivars. All three of these factors in combination could reduce the final structure of a hybrid to such a degree that narrow row culture should be possible. B . SEEDLING VIGOR

Much of the advantage of hybrids over pure line cultivars may be due to superiority in early stages of development. Significant increases in seedling vigor

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have been reported in G. hirsutum X G . hirsutum crosses (Thomson, 1971; Harris and Loden, 1954; Galal ef al., 1966). Abd-Alla and Bird (1973) found hybrid vigor for root growth in intraspecificG. hirsutum crosses that was attributable to dominance or gene interaction. Seedling vigor has been reported to be much greater in interspecific crosses (Marani and Avieli, 1973; Muramoto et al., 1965) than in G. hirsutum intraspecific hybrids. Davis (1974) has shown that interspecific hybrids involving an early dwarf parent were taller than the check variety “Acala 1517-70” until mid-July. At this point, 10 weeks after planting, the hybrids were about 2 weeks ahead of commercial upland cotton in fruiting development. A large heterotic effect for vegetative growth in the early weeks of development is a strong positive feature (Kame and Zirpe, 1973). This may ultimately be the means of further reduction in the effective growing season, with a corresponding increase in plant efficiency of grams of lint produced per day (Production Rate Index, Bilbro and Quisenberry, 1973). Seedling heterosis acts as the thrust to push interspecific hybrids out ahead of standard cultivars especially when grown under a suboptimal temperature regime (Marani, 1968c; Marani and Avieli, 1973). Following the seedling stage, the onset of heavy fruiting may act as a regulator controlling plant growth. C. THE PLANT CANOPY

Interspecific hybrids also show superiority in the development of the plant leaf canopy independently of the heterosis for plant height. This leaf area superiority was quantitatively measured on one hybrid by Muramoto et al. (1965). Hybrid leaf area was four times as great as that of the parents 8 weeks after planting. Watson (1952) regarded leaf area index, or the capacity of the photosynthetic system, as a critical factor in increasing yield in crops. It is of vital importance in the weeks immediately following sowing, when the index is below unity. Smith and Falcon (1973), however, found that California-grown Acala SJ-1 cotton can tolerate up to 50% loss of leaf area in the establishment phase without apparent loss in yield. The subject needs further investigation to explain these apparent contradictions. Okra leaf is another plant morphological factor that acts to modify growth. Kohel (1974) notes that the okra leaf gene is found in natural populations and apparently has positive selective values under some conditions, presumably those conditions favoring early maturity (Kohel and Richmond, 1971). Thomson (1972) found super okra associated with normal yield as well as earliness and reduced stature. Andries et al. (1969) reported that several upland cultivars isogenic for okra leaf had a fruiting rate 50% above their normal leaf counterparts early in the season. This effect is sufficiently sustained for isogenic okra leaf types to mature about 4 days earlier than normal types. Andries et al. (1969)

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have shown that light interception is much greater in okra leaf than in normal leaf cotton for a given leaf area index. Karami and Weaver (1972) report further that heterozygotes for okra leaf were intermediate between the homozygous okra and normal leaf genotypes for earliness and rate of fruiting. Pure line cultivars must be either normal or okra leaf type, but by crossing okra leaf with normal leaf parents intermediate okra leaf Fl hybrids can be produced. Since there is strong heterosis for leaf size in interspecific hybrids (Keamey, 1923b), intermediate okra leaf will be valuable in reducing the density of the canopy and improving light penetration. D. EARLINESS INTERACTIONS

The time of initiation of fruiting and the subsequent rate of fruiting is very important in controlling vegetative vigor, and parents carrying certain early dwag factors transmit the tendency for early square initiation to their progeny. An experimental Yugoslav-Kekchi-Acala X Pima S-4 hybrid produced squares earlier, was shorter at maturity, and was slightly earlier in boll maturation than Acala 1517-70 (Davis, 1974), in spite of a longer boll period. The long boll period of interspecific hybrids is presumably associated with their extra-long fiber. Recent experiments have shown that Pima S-4 requires 12 days more for the fiber in a developing boll to attain full length than does the short-fibered upland cultivar, Stoneville 213 (Schubert et al., 1976). Interspecific hybrids are apparently similar to Pima in this respect. Current experiments (Davis, 1978) have uncovered a similar dwarfing effect obtained on the interspecificcrosses involving another early dwarf parent derived originally from Del Cerro and Storm Proof cottons. There may well be other short-statured G. hirsurum types that will respond similarly. 111. Plant Type and Harvest Efficiency

A. PROBLEM PHENOTYPES

Another morphological trait of some importance is the conformation of the sympodia (fruiting branches). The normal tendency in interspecific Fl 's is for the fruiting branches to be quite long. Coupled with the tendency to tall growth, this often results in very large bushy plants. When square initiation is induced at a low node on the plant due to the early dwarf factors, then the first fruiting branch lies close to the ground, where it is difficult to harvest. This problem is similar to one that was faced by American Pima breeders recently in the S-3, S-4dilemma. The S-3 type fruits higher off the ground, and hence is better adapted for mechanical harvest. The S-4type, fruit.. ing close to the ground, is earlier maturing. A compromise plant type between

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these extremes, which will sacrifice some earliness and some spindle-picker efficiency, but still be acceptable in both traits, may possibly be the best objective (Feaster and Turcotte, 1965). However, the newest release of American Pima (S-5) is an early, low-growing type. Yield and early maturity are apparently paramount to harvestibility in the plant type of Pima cultivars. Low fruiting is partially alleviated by cultural practices. Commercially acceptable plant types should be adaptable to moderately thick stands, and thick stands have a tendency to force the fruit load upward on the plant (Fowler, 1966). High-yielding interspecific hybrids at stands of about 10 plants per meter were spindle-picked without difficulty two years in succession (Davis, 1976). Quisenberry (1975a) has reported that the internode lengths for main stem and fruiting branches can be manipulated independently in G. hirsutum. B . USEFULNESS OF SHORT-BRANCH PHENOTYPES

The harvest efficiency problem may possibly be attacked genetically by incorporating the genes for cluster (cl,) and short fruiting branch (cf,)into both parents of a hybrid. Heterozygotes for the cl, gene have been reported to have branches of intermediate length (Kearney, 1930). S. G. Stephens, Geneticist, Cotton Inc., Raleigh, North Carolina (personal communication), indicates that there is considerable interaction between the cluster genes cl, and cl, and the background genotype. In general, both genes act as recessives, but in some instances the heterozygote may be more or less intermediate to the normal and the cluster phenotypes. If the objective is to produce hybrids with short fruiting branches, then the cl, gene is probably the best choice to incorporate as a homozygous recessive in both parents. The cll gene in G. hirsururn generally produces phenotypes with very short sympodial nodes. The cl, gene in G. barbadense produces plants that fruit directly on the main stem axis with sympodia completely missing. This is a satisfactory plant and seems to be characteristic of commercial G. barbadense cultivars obtained from the Soviet Union. However, when transferred to G. hirsuturn, the cl, gene often produces deleterious effects on the plant. The main stem node may be completely aborted and replaced by a sympodial branch, resulting in a distorted plant of very little productivity. Moreover, a study by Bevandoss et al. (1971) showed evidence that two recessive factors control branching habit in certain strains of G. barbadense. The overall problem of genetically controlling the width of the plant profile in hybrids may be a difficult one to solve, particularly in interspecific hybrids. C. BOLL SHAPE AND HARVEST EFFICIENCY

Another morphological factor involved in harvesting efficiency of cotton is boll conformation. Corley (1970) found that boll size (diameter), boll shape

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(roundness), boll length, peduncle length, and degree of boll opening all affected picking efficiency. To these properties can be added lock angle (Friesen, 1968) and interseed cohesive forces (Friesen and Colwick, 1971). A simplified summation of the above research would indicate that bolls of elliptical shape, but not excessively long, with short peduncles and not flared too widely after opening would be harvested most efficiently. Corley (1970) has noted that varieties in the desired range of storm resistance for once-over harvesting were as good or better in terms of total field losses for twice-over harvesting as the varieties with lesser storm resistance. It would appear, then, that a medium level of storm resistance (measured by energy required for picking the seed cotton from the bur) would be highly desirable even if spindle-picking is the preferred method of harvest because of considerations of fiber quality. Where maximum yield is the goal, and only minor consideration is given to fiber quality, then cultivars with high levels of storm resistance may be sought becaLse of the greater yields obtainable by the stripper harvest method (Tupper, 1966; Saunt, 1967). Both the Macha (extremely tight boll) and Lankart (intermediate boll) types of heritable storm resistance are readily available in earlymaturing G. hirsutum. The Macha type of storm resistance was reported by Jones and Ray (1953) to be due to a single, incompletely dominant gene. The total storm resistance picture, particularly the Lankart type, however, is apparently more complex (J. E. Quisenbeny , personal communication). Some strains may have bolls that are fluffy in appearance, yet quite resistant to storm loss (Niles and Richmond, 1962). Good storm resistance has been found in G. barbadense also (Young, 1975). Theoretically, it should be possible to fix storm resistance at any level desired in an Fl hybrid, although the process may be one of trial and error. Stripper harvest hybrids must obviously have acceptable plant shape for machine harvest as discussed above and may require several years to develop. Combinations with acceptable storm resistance for spindle-picking are already available.

V. Pest Resistance Potential for Hybrids

A. INSECT RESISTANCE

Several qualitative characters found in certain cottons give measurable levels of protection against certain insects. An inherent plus factor in interspecific hybrids would be its probable higher level of resistance to Heliothis, because of factors inherited from the G. barbadense parent. Commercial G . barbadense tends to be resistant because it is glabrescent (Lukefahr et al., 1965, 1971) and high in gossypol content (Lukefahr and Houghtaling, 1969). The F, hybrid with G. hirsutum should be intermediate for hairiness (Kearney, 1930), although

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epistasis has occurred in certain instances (Peebles, 1929). In certain locales pubescent cottons would be preferable to smooth because of resistance to jassid (Empoasca spp.) (Reed, 1974) and other sucking insects. A high percentage content of analogous terpenoid compounds reinforces gossypol as insect deterrents in cotton plant tissues (Lukefahr and Houghtaling, 1969). High terpenoid levels in fruiting parts of the plant are difficult to obtain in good agronomic types of G. hirsutum. In this species high gossypol tends to be highly correlated with bolls that are smaller than the yield model optimum.’ High-level gossypol concentration may be easier to obtain in an interspecific hybrid, since boll size in the F, tends to be intermediate to the parents (Fryxell et al., 1958; Keamey, 1923b; Marani, 1967; Davis, 1974). The gossypol content of an interspecific F, hybrid reported by Singh and Weaver (1972a) was close to the level of the high-gossypol Pima S-4 parent. These same authors (1972b) indicate that high gossypol conferred some resistance to the boll weevil. Kearney (1930) had earlier indicated that glandulosity was intermediate in the cross he studied. The nectariless trait has also been shown to reduce infestations of the damage due to Heliorhis spp. (Lukefahr er al., 1965; Davis et al., 1973). There is good evidence to show that plant bugs (Lygus spp.) are also suppressed by nectariless (Schuster et al., 1976). The nectariless trait has been transferred to a wide range of G. hirsutum cultivars and to some G. barbadense lines, so that ample parental material is available. Apparently the nectariless trait is easily transferred into good agronomic types (Meredith et al., 1973). The okra leaf trait modifies the microclimate by reducing plant height and increasing light and air penetration into the interior of the canopy, thus reducing susceptibility to boll rots (Andries et al., 1969). These microclimatic effects induced by okra leaf also confer strong resistance to the banded-wing whitefly (Trialurodes aburilonea) and a suppressing effect on boll weevil (Anthonomous grandis) (Jones, 1972). Two other traits of primary interest to American breeders because of their suppressing effects on boll weevil are frego bract and Ak Djura red (Jones, 1972). Frego bract would be difficult to handle in hybrids, since it is a recessive character and conditions susceptibility to Pseudatomoscelis seriatus and Lygus linearis. Ak Djura red, on the other hand, has not shown serious disadvantages, and may eventually be useful in hybrids. It appears that there are no known “broad-spectrum” resistance characters (with the possible exception of gossypol), so breeding for insect-resistant hybrids is likely to vary according to the major pest species encountered in each geographic region. Host plant resistance to insects is doubly important in potential parents of hybrid cotton, since any spraying to control pest insects may also suppress ‘The most recent test results indicate a breakthrough in high-yielding, high-gossypol upland cotton (M. J . Lukefahr, personal communication).

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pollinator insects. Intensive area-wide spraying for insect control has depleted populations of bees for pollination in many locations throughout the cotton belt. Natural crossing at Stoneville, Mississippi, had dropped from 18% in 1952 (Simpson, 1954) to less than 0.1% in 1969 (Meredith and Bridge, 1973), owing to intensive insecticide spray programs continued for many years. By contrast, spraying is only occasionally required in the isolated desert valley surrounding Las Cruces, New Mexico. This latter location has maintained a range of 5-15% frequency of natural crossing for many years. Bee populations are vital to any scheme of hybrid cotton.

B. DISEASE RESISTANCE

The F, hybrids that fruit heavily will probably tend to be more susceptible to Verticillium wilt than their G. barbadense parents, which are often quite tolerant. However, true genetic tolerance can be transferred into the G. hirsutum parents also, with minimal loss of earliness (Staten, 1971). Cotton wilt tolerance can probably be placed at any level desired. A heritable type of resistance to Fusurium wilt and root-knot nematodes has been shown to be partially dominant in G. hirsutum x G . hirsutum F, progenies (Shepherd, 1974). Bacterial blight (black arm)resistance is also available. The E$ gene is fully dominant, and the &, B4, and B:, genes are partially dominant (Knight, 1953). Some of these genes are already well distributed in both G. hirsutum and G . barbadense breeding stocks. A single, nearly immune parent would confer high-level resistance to an F, hybrid (Mahill and Davis, 1978). The genetics of reaction to other leaf blight diseases is less known. VI. Fiber Properties of Hybrids

A. G. hirsutum

X

G. hirsutum CROSSES

There is sufficient data now available to say that intraspecific crosses among varieties of upland cotton, G. hirsutum, behave quite differently than do the F, crosses of G. hirsutum X G . barbadense. In general, the fiber performance of an intervarietal G. hirsutum cross can be expected to be relatively stable and similar to the mid-parental value. The genetic control of these properties is largely additive, although partial dominant effects have been detected for upper-half mean length (Marani, 1968a; Miller and Marani, 1963; Verhalen and Murray, 1967, 1969; Ware et a l . , 1943; Ware and Harrell, 1944; Quisenberry, 1975b; Al-Rawi and Kohel, 1970). Similarly, there has been a slight heterosis relative to the mid-parent reported for fiber coarseness (Barnes and Staten, 1961; Ware and

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Harrell, 1963; Marani, 1968a; Al-Rawi and Kohel, 1970). Verhalen and Murray (1969) have even detected a slight overdominance for micronaire. Some studies have also shown specific combining ability for fiber coarseness (Quisenberry , 1975b). Innes (1974) detected significant epistasis for fiber length and strength in a series of test crosses among upland lines of highly diverse backgrounds. The genetic diversity, which included several instances of interspecific introgression, was thought to be a major contributor to epistasis. Significant epistasis was not found by several other investigators in intraspecific crosses using pure upland stocks (Lee et al., 1967; Miller and Lee, 1964; Baker and Verhalen, 1975). Despite these reports of heterosis, the overriding consideration in all the investigations listed is the fact that the fiber properties consistently fall close to those of the mid-parent, well within the parental ranges. Even though some partial dominance is detected, additive genetic variance seems to predominate, and the levels of heterosis are low. In synthesizing intervarietal crosses within G. hirsutum, it would be expected that, if both parents are satisfactory for all fiber traits, then the Fl hybrid would generally be expected to be satisfactory. This assumption would not begin to hold true in dealing with interspecific hybrids. B. G . hirsutum x G. barbadense CROSSES

The evidence of hetero.. .; in fiber properties of interspecific crosses is much more spectacular than that in the intra-hirsutum crosses. However, not all aspects of heterosis for interspecific fiber properties are necessarily favorable. The 2.5% span (upper-half mean) length of interspecific hybrids exhibits full dominance, or in some cases overdominance (longer than the longest-fibered parent) (Fryxell et al., 1958; Marani, 1968a; Davis, 1974; Stroman, 1961; Omran et al., 1974; Ali and Lewis, 1962). On the other hand, there is generally less heterosis for 50% span length (mean length), (Fryxelletal., 1958; Marani, 1968d; Davis (1974). In general, the uniformity ratio of interspecific hybrids was lower than that for either parent. There are exceptions to this rule, and hybrids with satisfactory uniformity were found in specific combinations of selected parental lines (Davis, 1978). Another constant pattern in interspecific hybrids seems to be the negative heterosis for micronaire values. This means that interspecific hybrids can be expected, on the average, to produce fiber that is considerably finer than that found in either parent (Fryxell et al., 1958; Stroman, 1961; Ali and Lewis, 1962; Marani, 1968a; Davis, 1974; Omran et al., 1974). Interspecific hybrids also seem to show variation with respect to TI fiber strength. Commercial varieties of G. hirsutum and G. barbadense generally differ by a large margin in T, fiber strength. Although a long and continuous range of fiber strength is represented in

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both species, G . barbadense has 30-50% greater fiber strength on the average. Specific combining ability is likely to be of paramount importance in producing interspecific hybrids of high tensile strength. Fryxell et al. (1958) reported that nearly all interspecific hybrids studied were within the range of the parents; however, certain parents produced better combinations of tensile strength than others. Stroman (1961) reported crosses that approached the G . burbadense parent in tensile strength. Marani (1968a) reported that most crosses he studied showed heterosis relative to that of the mid-parent for tensile strength but not generally as high as that of the G. barbudense parents; however, two G. burbadense parents, Ashumuni and Pima s - l , produced Fl hybrids with higher T, values than either parent. Omran et al. (1974) further stressed the importance of specific combining ability in optimizing the fiber strength of G. hirsutum x G . barbudense hybrids. VII. Breeding Hybrids with Marketable Fiber Properties

Gossypium hirsutum intraspecific crosses do not show extreme heterosis for fiber property traits. Their values generally fall close to the mid-parental values, and hence the marketability of the hybrid can be reasonably well extrapolated from the mid-parent. Interspecific hybrids show strong and complex heterosis responses in the various fiber properties. It will be much more difficult to evaluate the market value of the interspecific hybrids and may require an extended period of time. In evaluating the combining ability for fiber properties in the interspecific hybrids, the eventual end use must be kept clearly in mind. The heterosis for fiber length is a character of little value. Only small quantities of cotton are generally needed with the extra-long staples of lS/16-l% inches (upland standards) that are often produced by the interspecific hybrids. On the other hand, their lower uniformity may be a definite disadvantage. Types with extremely low uniformity should probably be avoided, as this trait may result in more comber waste, perhaps weaker fibers, and increased difficulty in spinning. Since there does not seem to be a large market for cotton of extra-long staple, it would probably be better to concentrate in the medium to long staple range of 13/32-13/16 inches. In the Western United States these qualities are usually supplied by the Acalas. Certain Delta and Southeastern cultivars have staples up to 1% inches, but usually lower tensile strength than the Acalas. Cottons of this staple have a wide degree of utility for many end uses, depending on their relative fineness values. Gossypium barbadense parents with shorter fiber will have to be located in order to produce interspecific hybrids of intermediate staple length. This is a rather difficult task, presumably because of the half-century of effort that has

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gone into producing improved, longer-stapled G. barbadense cultivars for the commercial crop. However, certain genetics and breeding programs have source material, selections, and segregates of shorter staple length. This germ plasm, now accumulating, must be tested to determine its value in the synthesis of interspecific hybrids of medium staples. For present standards on ring-spinning textile systems, micronaire has been only marginal to fair ( 3 . 1 4 0 ) in interspecific crosses. Gossypium barbadense fiber must have micronaire of 3.5 or better, plus satisfactory grade and staple, to be in strong demand on the current American market (R. T. Hoover, R. T. Hoover & Company Cotton Merchants, El Paso, Texas). Fryxell et al. (1958) indicate that low micronaire in the F, may be independent of earliness, and this conclusion is confirmed by Davis (1976, 1978). This is a problem that may require special effort to solve. There is, as yet, no evidence of specific combining ability, and coarse-fibered cottons are not necessarily good combiners for micronaire (Fryxell et al., 1958; Davis, 1974, 1976). However, there is evidence to suggest that coarse-fibered parents tend to produce F, hybrids with higher absolute micronaire levels (Marani, 1968d). This is not an indication of favorable combining ability, but rather an inevitable consequence of the fact that, if all crosses fall uniformly below the mid-parent, then crosses involving coarsefibered parents will produce F, hybrids with higher micronaire. There is no evidence of any linear relationship of parent to progeny, and even the best combinations reported have relatively low micronaire values. Specific qualitative genes for coarser fiber are needed, and the best candidates are the okra leaf gene, Lo, and certain alleles affecting plant pubescence, such as Sm;',H2 (pilose), and possibly HI.There also appear to be other quantitative factors affecting micronaire. Kohel and Richmond (1971), working with isogenic lines, found okra leaf to have no significant influence on micronaire. On the other hand, Andries et al. (1969) found that three backcross lines of okra leaf cotton had significantly higher micronaire than did the recurrent normal leaf parental lines. Since okra leaf affects maturity, and maturity in turn affects micronaire, okra leaf may possibly influence micronaire through secondary effects. The pilose gene, H,, shortens the fiber of a strain by about '/Q inch. This decrease in lint length is coupled with a corresponding increase in micronaire. Kohel and Richmond (197 1) found isogenic H 2 to have extra high micronaire as compared with the isogenic line with the normal allele. The 2.5% span length was reduced 5 cm; the 50% span length was reduced somewhat less. In eleven families tested by Lee (1964), the average increase attributable to the H 2 locus was 1.05 micronaire units. Pilose was essentially abandoned in upland breeding because of the loss in length even though Hz G. barbadense has been recovered with no loss in length (Dark, 1960). Most F, interspecific hybrids would still have medium staple with 5 mm loss in length. The pilose gene will make breed-

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ing for smoothness more difficult, since H2is epistatic to Sm:l (Ramey, 1962). The pubescent Tanguis cultivars (H, ) are the coarsest-fibered commercial G. burbudenses, indicating that there might be some relationship between fiber coarseness and hairiness genes other than H , . The full economic implications of the negative heterosis for fiber fineness in interspecific hybrids are unknown. It may depend largely on whether the hybrids are fine and mature, or fine and immature. If the low micronaire values obtained are due primarily to reduced diameter of the fibers, and if the interspecific hybrids still have thick walls and good maturity, then there should be a very wide range of utility for these fibers. Long, fine, strong, mature fibers are needed for many of the more select uses of ring-spinning frames. There is an urgent need for more basic research associated with the relative maturity of the fibers of the interspecifichybrids. Measurements on one selected hybrid showed that reduced micronaire was due to reduced fiber diameter and not to reduced wall thickness (Davis, 1976, 1978). The available data for tensile strength of interspecific hybrids indicate that specific combinations will produce the tensile strength required to meet many end-use requirements that are currently demanded of American Pima and Egyptian cottons. Strength is apparently a highly desirable property in any cotton fiber, and most interspecific hybrids will produce stronger-fibered cottons than our current medium-staple and long-staple upland crop, since nearly all interspecific hybrids show slight heterosis relative to that of the mid-parent. Economic implications of the heterosis for high-fiber elongation in interspecifichybrids will have to be explored. This would probably be a positive effect in processing cotton fibers. Recent developments in open-end spinning make this commercial innovation a potentially large market for blends containing fine, mature, strong cotton (Int. Inst. for Cotton, 1974). Experts in the field indicate that open-end spinning may eventually require up to 30%of the raw cotton produced. Conceding that interspecific hybrids may fall below the quality requirements for very fine, ring-spun yams, there is still a potentially larger market for these types in blending with the short, weak stripper cottons in producing open-end yams. Open-end yams are typically about 10-20% weaker than ring-spun yams of the same count (Heap, 1975). Strong, fine fibers from low-grade Pima when used as 25% of a blend can increase yarn strength to satisfactory levels (Towery, 1975). The fine, strong, apparently mature fibers of interspecific hybrids meet idealized open-end requirements very well (cf. Konishi, 1975). This market is only in early stages of development, but prices bid for low-grade Pima for this end use are much below prices paid for premium Pima grades. Interspecific hybrids should compete for this market segment very strongly, since, at yield levels competitive with those of current upland cultivars, they would be profitable at price levels slightly above the prices

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paid for Acala but considerably below those paid for high-grade Pima or Egyptian fibers. VIII. The Production of Hybrid Seed

A . GENETIC AND CYTOPLASMIC MALE STERILE SYSTEMS

Two recessive genetic male sterile systems are known that give complete sterility (Koheland Richmond, 1962;Weaver, 1968).A third genetic system (Roux, 1961),the ms3type, has more promise, since the degree of sterility can be environmentally manipulated. The same ms3 lines that are completely sterile in hot, dry environments may be partially fertile and capable of reproducing themselves in cool, moist environments. Any normal pollen would serve as a restorer to an rns3 line. However, since the advent of cytoplasmic male sterility, all serious breeding work with the genetic steriles has been dropped. Three cytoplasmic male sterile systems are now available to breeders (Meyer and Meyer, 1965; Meyer, 1969, 1973~).Two of them have the disadvantage of being environmentally influenced to an excessive degree. Only in Arizona have the G. anomalum and G . arboreurn cytoplasmic male steriles shown a usable degree of sterility. Even there the G. harknessii sterile is considered to be superior (L. S. Stith, University of Arizona, Tucson, personal communication). With appropriate nuclear genes, stocks carrying G. arboreurn or G . anomalum cytoplasm are usually sterile when maximum temperatures rise above 32"C, and the sterility is enhanced by a low relative humidity, high wind movement, and high pan evaporation (Sarvella, 1966). Cool, humid days any time in the flowering season can induce some fertility. These conditions inducing fertility are likely to occur at most locations where cotton is grown in the United States, with the exception of Arizona and Southern California. There is a cytoplasmic-genetic interaction of the G. anomalum and G . arboreurn cytoplasms with the ms3 locus (Meyer, 1969), that might eventually result in a workable male sterile-restorer system. Work with these cytoplasms and the genetic male steriles has generally been abandoned because of the apparent superiority of the G. harknessii materials that-have been developed by Vesta Meyer of the Delta Branch Experiment Station, Stoneville, Mississippi (Meyer, 1971, 1973a,b,c). Male steriles derived from G. harknessii have flowers that are normal except for the reduced stamens. Seed set with G. harknessii steriles has been exceptionally good (Rosales and Davis, 1976; Stith, 1974). In addition to an environmentally stable sterility, G. harknessii stocks appear to have excellent agronomic properties and to be very attractive to honeybees (Moffettet a l . , 1975b). Present stocks (14th backcross of G. hirsutum onto G . harknessii cytoplasm) bloom profusely and set a good crop of bolls at Las Cruces.

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It is very easy to restore fertility in crosses of the type (G. harknessii x G . hirsutum) x G . barbadense. The corresponding cross (G. harknessii X G . hirsutum) x G . hirsutum becomes largely infertile after several backcrosses.' A single dominant gene from G. harknessii (Meyer, 1975; Weaver, 1977) is essential for fertility restoration. There is evidence that G. barbadense carries a gene for enhancement of fertility. This phenomenon has been noted by Meyer (1969) and by Weaver and Weaver (1977). A G. barbadense restorer giving 100% restoration and heterosis for pollen production was evaluated at Las Cruces in 1977 (Davis, unpublished data). The genetics of the G. barbadense fertility enhancement phenomenon are unknown. It would seem advisable for breeders to use a segregate of Meyer's DESHAF 16 or 277 crossed with G. barbadense that has been segregate-selected for fertility as the basic female stock in a backcross program to produce G. hirsutum restorers. If selection for high fertility is made after each cross, then both the G. barbadense and the G . harknessii factors for fertility should be retained. The G. harknessii male sterile-restorer system seems to be at present by far the best system to use in synthesizing commercial hybrids. However, certain other genetic-cytoplasmic male sterile systems should also be developed to broaden the genetic base, and G. longicalyx may provide an alternative,* although the genetics of fertility restoration are obscure (Vesta Meyer, personal communication). There is always the possibility that some difficulties may be found at a later date with the G. harknessii system. No such difficulties are presently indicated, but, if for no other reason than to reduce the potential genetic vulnerability of the crop, other genetic male sterile and cytoplasmic male sterile systems should be developed and evaluated as quickly as possible.

B. POLLINATION OF MALE STERILE COTTON

Shedding of young bolls on male sterile plants was reported to be excessive in Texas (Kohel and Richmond, 1962) in areas of low natural cross-pollination. They also observed a 25% reduction in seed set under high natural crossing. No such difficulty has been experienced in New Mexico, where an intermediate level of cross-pollination occurs. For several years at Las Cruces it was observed that the stigmas of male sterile flowers were coated with pollen by noon unless they were protected from natural cross-pollination. In 1973, experiments showed that boll shedding was higher on G. harknessii male steriles than on high-yielding, 'There may be exceptions. Several American breeders report progress in incorporating fully effective fertility restoration factors into the G . hirsurum genome. 2Dr. L. S . Stith, Department of Plant Sciences, University of Arizona, Tucson, has indicated to the author his intention to attempt the development of a G . longicalyx cytoplasmic-genetic male sterile and restorer.

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fully fertile Acala strains. However, the G. harknessii steriles bloomed more abundantly, and total planting seed yield was approximately equal to that of open-pollinated Acala checks. No difficulty was experienced in obtaining satisfactory yields on male sterile rows adjacent to pollinator rows in fields within 400 m of a commercial honeybee apiary (Rosales and Davis, 1976). There is considerable evidence that natural crossing varies from one genotype to another, and that higher crossing capacity can be selected for (Finkner, 1954a,b; Harvey and Weaver, 1964). Fortunately, G. harknessii A lines are very attractive to honeybees (Moffett er al., 1975b). McGregor has shown that the honeybee is an effective pollinator of cotton. In experiments conducted in 1955 and 1956 (McGregor, 1959) using two and one-half colonies per acre in desert sites in Arizona, he was able to get excellent coverage of stigmas of Pima cotton by honeybees. The correlation between the number of honeybees per 100 flowers and the number of stigmas coated with pollen was extremely high, with r = 0.98. McGregor estimates that ten bees per 100 flowers (instantaneous count basis) are sufficient to get excellent crosspollination. More recent production experiments (Rosales and Davis, 1976) would indicate that only two bees per 100 flowers would be sufficient for nearnormal production. Moffett et al. (1975) and Johansson (1959) have documented the foraging habits of honeybees in cotton fields. Moffett et al. noted that frequency of bee visitation to cotton suffers because of competition of other plant species. They point out that cotton hybrid pollination fields should be located or managed so that cotton does not have to compete with species, such as Tamarisk, that strongly attract bees. Some experimentswith hybridizing cotton were attempted in Arizona in the 1950s (Peebles, 1956). These depended on honeybees as the pollination vector, and the honeybees were concentrated in an area with one or more hives per acre in an attempt to remove the extra-floral nectar rapidly enough so that the bees would be forced into the flowers, and would thus presumably become a more effective pollinating agent than they would be under normal circumstances (Grout, 1955).The present availabilityof genes ne, and ne2,which remove the leaf and bract nectaties from the cotton plant, renders these expedients of oversaturating with honeybees unnecessary. However, the data of Rosales and Davis (1976) cast doubt on the attractiveness of nectariless genotypes to honeybees. The bumblebee is conceded to be a most effective pollinator of cotton when adequate populations are present. The endemic species in Southern New Mexico (Bombus sonorus and Bombus morrisoni) have population densities that are quite variable from year to year and cannot be depended on as pollinators. This same pattern may be true elsewhere. Currently, experiments are in progress in Oregon to domesticate the bumblebee. If these are successful, they can be effective pollinators even in relatively small, stable populations (Thies, 1953), probably much smaller than equally effective honeybee populations. At the present time (McGregor, 1976) the honeybee should be considered the solid base level for

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cross-pollination because of the ease with which populations can be manipulated. Wild bees, such as Bombus and Mellissodes (McGregoret al., 1955; Butler et al., 1960), may add effectively to the base. IX. The Association of Heterosis and Plant Pubescence A . YIELD LEVELS

Basic research relating to hybrid performance is very incomplete, but already there are some clear indications that plant pubescence may be related to agronomic performance. The highest yields ever reported in intra-hirsurum hybrids (Thomson, 1971) exceeded 1800 kg/ha, and had as either one or both parents a highly pubescent strain of African upland. The greatest interspecific heterosis for yield in New Mexico has been found in crosses where a highly pubescent G. barbadense strain served as one parent in interspecific crosses with upland. In G. barbadense varieties the pubescence factor has been intensified during the past quarter-century, presumably because of the association of pubescence with yield and early maturity. Dr. E. F. Young (personal communication), of the Texas A&M Experiment Station, El Paso, has segregated pubescent and glabrescent sib selections out of his major breeding families. When the pubescent lines were tested against the glabrescent types, the former were found to be outstanding in yield and earliness. Since the pre-1940 Pima varieties were all glabrescent, the present pubescent Pima types presumably arose from intercrossing with Tanguis types andor from the introgression of small portions of the G. hirsutum genome into G . barbadense. In several cases this interspecies introgression has been intentional (Feaster and Turcotte, 1962). The most pubescent of the current types are represented by family E1097, which has extreme types that are cleistogamous, owing to the self-adhesion of the highly pubescent petals. This type of G. barbadense also has considerablepubescence on the outer carpel wall. This is a condition first noted by Peebles (1929) and found to be associated with transgressive segregation in a G. barbadense X G . hirsururn hybrid. Since materials of this general genotype were common in the old El Paso breeding stocks, and since the pubescent boll type is unique to hybrid types and different from both of the cultivated American species, it is quite likely that the El097 material represents stabilization of the transgressive segregation for pubescence into G. barbadense. The possible significance of the pubescence factor in a hybridization program is indicated by the performance of El097 as a hybrid parent. El097 is one parent of the highest-yielding hybrid combination tested in New Mexico, and its combining ability for earliness is especially pronounced (Davis, 1978). Pima S-4 is another good combiner with G. hirsururn, and this excellent modem cultivar has diverged from the glabrescent type of original Pima to a condition

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roughly equivalent to normal G. hirsurum types with low-grade pubescence (Lee, 1971). B. PROBLEMS ASSOCIATED WITH HEAVY PUBESCENCE

If the genes conditioning heavy pubescence have pleiotropic effects on yield and combining ability in cotton, then a number of problems are raised, including insect resistance and susceptibility, and grade, processing, and properties of the raw fiber. Damage due to certain insects may be suppressed by heavy pubescence, notably the Afro-Asian jassids (Empoasca spp.) (Knight, 1952), boll weevil (Anrhonornus grandis) (Stephens and Lee, 1961; Wessling, 1958), and leafworm (Spodopfera littoralis, Kamel, 1965). On the other hand, heavy pubescence conditions increased susceptibility to the American Heliothis complex (Lukefahret a f . , 1971), and the tobacco budworm and cotton bollworm may be the hardest-to-control insect pests found in the American cotton belt. The literature is conflicting concerning the effect that increased pubescence has on the incidence of many other insects. (For a more complete bibliography on the effects of pubescence, see Webster, 1975). The effects of pubescence on certain insects may be partially confounded by interaction with other factors such as nectariless (Lukefahr et al., 1966, 1969; Davis et a f . , 1973), high gossypol content (Lukefahr and Houghtaling, 1969), and leaf thickness (Batra and Gupta, 1970). The sensitivity to certain insects attributable to glabrous phenotype may be partially overcome by one or more of these factors. Or it may be possible to find phenotypes essentially glabrous but with protective pubescence on the tissues usually attacked by insects. It has been indicated that it is the minute squares in glabrescent terminals that are apparently hypersensitive to attack by small populations of mirids such as the cotton fleahopper (Pseudafornoscelisseriatus, Niles ef a f . , 1974), or possibly the cotton leafhopper (Empoasca spp., Lukefahr, 1975). These same authors and others note the benefit of glabrescent foliage in conferring Heliothis resistance. Ramey's studies (1962) and Lee's (1968, 1971) observations would indicate that high levels of stem and leaf pubescence can be suppressed by certain of the smooth leaf alleles (Srn?' ,Sm, ,Sm3). Therefore, the F, produced from a cross of smooth x heavily pubescent will be a medium-smooth leaf type with pubescent terminals. This phenotype might be a possible compromise type with satisfactory levels of resistance both to mirids and Heliothis. High levels of pubescence also create some problems in ginning and cleaning (I. W. Kirk, former Director, USDA-ARS Ginning Laboratory, Mesilla Park, New Mexico, unpublished data), as will be reflected in classers grades. The fine trash generated in these types could well contribute to further byssinosis problems in spinning mills (Wakelyn, 1972). Fine trash of this general type can also

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cause problems of ends-down, yarn’imperfections, and excessive rotor wear in open-end spinning systems (Heap, 1975; Towery, 1975; Wirth, 1975; Lord, 1975). Intensive study is needed on the genetics of plant pubescence because of its great bearing on yield, insect resistance, and fiber performance. Knowledge of the phenotypic interaction of gene loci and allelic interactions conditioning the distribution, length, and density of plant pubescence is of primary importance in the successful development of cotton hybrids. X. Breeding Methodology

No new or difficult concepts are necessary for the production of a hybrid. The cytoplasmic-genetic system composed of A, B, and R lines is similar to the three-way crosses successfully used in sorghum (Poehlman, 1959; Quinby and Schertz, 1970), with the exception that bees rather than winds are the pollination vector. Presumably existing lines can be found that are suitable parents for high-yielding and agronomically sound hybrids. If so, then the basic procedure involved in creating A and R lines is the time-honored backcross procedure (Briggs and Allard, 1953). The many specific heritable traits that may be eventually desired in specialized hybrids, such as disease resistance, dense pubescence, cluster habit, storm resistance, early maturity, and short statute, will be wanted in combinations not to be found in any existing parental line. To accomplish this objective, the artistry and science of the same breeders that have created the excellent array of modem “pure line” cultivars will be needed. Synthesis of parental lines with new combinations of specific heritable traits will be a “conventional” breeding problem and will be simple or difficult to accomplish in direct proportion to the number of genes involved and the presence of adverse or favorable linkage relationships. It has been found convenient in our own program to create R lines by keeping the restorer gene(s) together with G. harknessii cytoplasm as the female line in the backcross cycle. The donor line is used exclusively as the pollen parent. Since the restorer gene(s) are fully dominant, segregates carrying the restorer factor can be identified in the FI generation of each backcross. It is thus possible to make two backcrosses per year in creating R lines, as well as A lines. Many R lines will be synthesized from G. barbadense donor lines. Since the restorer gene(s) have been released in a G. harknessii X G . hirsutum (Meyer, 1973c)background, there will be some difficulties usually encountered in purifying species crosses. One way to avoid this difficulty involves haploid techniques. By the semigametic process (Turcotte and Feaster, 1974), haploid tissue derived from pollen can be identified and transformed in a single generation (by means of colchicine doubling) into pure line restorer. By using an early generation restorer

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segregate from the (G. harknessii X G . hirsurum) X G . barbadense backcross sequence, pure line restorers can be synthesized that have a mixed random complement of G . hirsurum and G . barbadense chromosomes. Thus, an extremely great variety of distinct restorer lines is possible. Dr. Jerry R. Barrow, USDA-ARS geneticist, has already synthesized a pure line restorer (tested, 1976) by means of the semigametic technique and has isolated 35 potentially pure line restorers in haploid form. Dr. Barrow and a number of other cotton researchers are actively working to duplicate the success achieved by workers in other crops in pollen culture (cf. Kasha, 1974). If this technique is perfected, then many mixed types of restorers that would be difficult to stabilize in pure lines by the backcross method may be isolated with relative ease. XI. Summary

On the basis of the research data in hand there seems to be ample justification to give a high priority to the attempt to produce commercial hybrid cotton. The heterosis associated with African upland varieties indicates that yield advances are still realizable at optimum cultural levels. Under suboptimal conditions, hybrids may give percentage yield increases that are quite spectacular. In many spindle-picker harvest areas, production costs are very high, and new yield plateaus must be found if the quality cotton industry is to continue to thrive. The commercial acceptance of interspecific hybrids will depend on finding ways to preserve heterosis for yield in manageable plant types. The prospects to achieve this goal seem quite good. The G . harknessii cytoplasmic-genetic male sterile-restorer system has yet to show any insurmountabledefects, and the prospects for adequate seed production appear to be very good. The breeding methodology required for synthesis of cotton hybrids is already familiar to cotton breeders. There are some situations where hybrids might be employed in the not-toodistant future, other areas where development would take more time, and still other places where a hybrid may never fit at all. Specialized types with stormproof bolls for stripper harvest and narrow plant profiles for narrow-row, high-population culture are not yet available to evaluate. Many other genetically controlled factors such as okra leaf, dwarf, early maturity, glandless, nectariless, and factors controlling length, density, and distribution of pubescence may be important to consider in the development of hybrids. REFERENCES Abd-Alla, S. E.. and Bird, L. S. 1973. Z . Pflanzenzuechr. 69, 123-128. Ah, M . , and Lewis, C. F. 1962. Crop Sci. 2, 20-22.

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Al-Rawi, K. M., and Kohel, R . J . 1969. Crop Sci. 9, 779-783. Al-Rawi, K . M., and Kohel, R. J . 1970. Crop Sci. 10, 82-85. Andries, J . A,, Jones, J . E., Sloane, L. W., and Marshall, J. G. 1969. Crop Sci. 9, 705-710. Anonymous. 1973. U . S . . Dep. Agric. FAS M-254. Baker, D. N., and Myrke, D. L. 1966. Proc. Beltwide Cotton Prod. Res. Conf., Nurl. Cotton Counc., 1966. pp. 102-109. Baker, J . L., and Verhalen. L. M. 1975. Cotton Grow. Rev. 52, 209-223. Barnes, C. E., and Staten, G . 1961. N. M . . Agric. Exp. Stn.. Bull. 457. Batra, G. R., and Gupta, D. S. 1970. Cod@:G r . Res. 47, 285-291. Bevandoss, M., Narayanan. A., Jayaraman. N., and Damodaran, A. 1971. Andhru Agric. J . 18, 160-163. Phnr Breed. Ahsrr. 44, 151 (1974). Bilbro, J. D., and Quisenberry. J . E. 1973. Crop Sci. 13, 392-393. Brashears. .4. D.. Kirk, I. W., and Hudspeth, E. B.. Jr. 1968. Tex., Agric. Exp. Stn., Misc. Publ.

872. Briggs, F. N., and Allard, R. W. 1953. Agron. J . 45, 131-138. Brown, H. B. 1942. J. Am. Soc. Agron. 34, 1084-1089. Butler, G. D., Todd, F. E.. McGregor. S. E . , and Werner. F. G. 1960. Ariz., Agric. Exp. Stn., Tech. Bull. 139. Christidis, B. G. 1955. J . Genet. 53, 225-231. Corky, T. E. 1970. Truns. ASAE 13, 768-773 and 778. Dark, S. 0. S. 1960. Emp. Cotton Grow. Rev. 37, 266-269. Davis, D. D. 1974. Crop Sci. 14, 745-749. Davis, D. D. 1976. Agron. Abstr. p. 49. Davis, D. D. 1978. Crop Sci.. in press. Davis, D. D., Ellington, J . J., and Brown, J. C. 1973. J. Environ. Quul. 2, 530-535. Delouche, J. C. 1975. Seedsmen's Dig. 26(10), 76-78. Feaster, C. V., and Turcotte, E. L. 1962. U . S . , Dep. Agric.. Agric. Res. S e n . ARS 3441, 1-15. Feaster, C. V., and Turcotte, E. L. 1965. Crop Sci. 5, 460-464. Finkner, M. D. 1954a. Agron. J . 46, 70-75. Finkner, M. D. 1954b. Agron. J. 46, 124-128. Fowler, J . L. 1966. M. S. Thesis, Texas A&M University, College Station (unpublished). Friesen, J. A. 1968. Truns. .4SAE 11, 529-531. Friesen, J . A., and Colwick, R. F. 1971. Truns. ASAE 14, 621-624 and 628. Fryxell, A,, Staten, G., and Porter, J . H. 1958. N . M . . Agric. Exp. Stn., Bull. 419. Galal, H. E., Miller, P. A., and Lee, J. A. 1966. Crop Sci. 6, 555-559. Grout, R. A. 1955. Am. Bee J . 95, 10-1 I. Harris, H. B., and Loden, H. D. 1954. Agron. J . 46, 4 9 2 4 9 5 . Harvey, L. F., and Weaver, J . B., Jr. 1964. Proc. Beltwide Cotton Prod. Res. Conf., Nurl. Cotton Counc. 1964, pp. 66-72. Hawkins, B. S . , Peacock, H. A . , and Ballard, W. W. 1965. Crop Sci. 5, 543-546. Heap, S. A. 1975. Proc. Tech. Semin. Open End Spinning, Nutl. Cotton Counc., 1975, pp. 1-10. Innes, N. L. 1974. Cotton Grow. Rev. 51, 85-98. International Institute for Cotton. 1974. Cotton Grow. Rev. 51, 167-176. Jenkins, J. N . 1978. Glandless Cotton: Its Significance, Status, and Prospects. ARS-USDA, Beltsville, MD. Johanssen, T. S. K. 1959. J . Econ. Enr. 52, 572. Jones, D. L., and Ray, L. L. 1953. Agron. Abstr. p. 90. Jones, J. E. 1972. Proc. Beltwide Cotton Prod. Res. Conf., Nutl. Cotton Counc., 1972, pp. 88-92. Jones, J. E., and Loden, H. D. 1951. Agron. J. 43, 514-516.

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15s

Kamel, S. A. 1965. Emp. Cotton Grower Rev. 42, 41-48. Karami, E., and Weaver, J. B., Jr. 1972. Crup Sci. 12, 317-320. Karev, K. 1969. Rmtenievud. Nauki 8, 3-10, Plant Breed. Ahstr. 41, 151 (1971). Karve, A. D., and Zirpe, A. G . 1973. Cotton Dev. 2, 30-32. Kasha, K. J., ed. 1974. ”Haploids in Higher Planfs.” Guelph. Ontario, Canada. Katarki, B. H. 1971. pp. 35-36. Kearney. T. €1. 1930. J. Agric. Res. 41, 379-387. Kearney, T. H. 1923a. U.S.Dep. Agric., Bull. 11, 34. Kearney. T. H. 1923h. U S .Dep. Agric., Bull. 11, 64. Kerr, T. 1966. Proc. Beltwide Cotton Prod. Res. Conf., Natl. Cotton Counc., 1966, pp. 276-287. Kime, P. H., and Tilley. R. H. 1947. J. Am. Soc. Agron. 39, 308-317. Knight, R. L. 1944. J. Genet. 46, 1-27. Knight, R. L. 1952. J. Genet. 51, 47-66. K,ight, R. L. 1953. J. Genet. 51, 270-275. Kohel, R. J. 1974. Cotton Grow. Rev. 51, 281-292. Kohel, R. J., and Richmond, T. R. 1962. Agron. J. 54, 525-528. Kohel, R. J . , and Richmond, T. R. 1971. Crop Sci. 11, 287-289. Konishi, T. 1975. Proc. Tech. Semin. Open-End Spinning. Natl. Cotton Counc.. 1975. pp. 40-42. Lee, J . A. 1964. Crop Sci. 4, 442-443. Lee, J . A. 1968. Genetics 60, 578-575. Lee, J . A. 1971. Crop Sci. 11, 4 4 8 4 5 0 . Lee, J. A., Miller, P. A., and Rawlings, J. 0. 1967. Crop Sci. 7, 477481. Loden, H. D.. and Richmond, T. R. 1951. Econ. Bat. 5, 387-408. Lord, P. R. 1975. Proc. Tech. Semin. Open-End Spinning. Natl. Cott. Counc., 1975. pp. 19-22. Lukefahr, M. J. 1975. Proc. Beltwide Cotton Prod. Res. Conf., Natl. Cotton Counc., 1975, p. 93. Lukefahr, M. J., and Houghtaling, J. E. 1969. J . Econ. Entomol. 62, 588-591. Lukefahr, M. J., Martin, D. F., and Meyer, J. R. 1965. J. Econ. Entomol. 58, 516-518. Lukefahr, M. J., Cowan, C. B., Pfrirnrner, T. R., and Noble, L. W. 1966. J. Econ. Entomol. 59, 393-395. Lukefahr, M. J., Shaver, T. N., and Parrott, W . L. 1969. Proc. Beltwide Cotton Prod. Res. Conf. Nail. Cotton Counc.. 1969. pp. 81-82. Lukefahr, M. J., Houghtaling, J. E., and Graham, H. M. 1971. J. Econ. Entomol. 64, 486-488. McGregor, S. E. 1959. Science 129, 97-98. McGregor, S. E. 1976. U.S.,Dep. Agric., Agric. Handb. 496, 171-190. McGregor, S. E., Rhyne, C., Worley. S . , Jr., and Todd, F. E. 1955. Agron. J. 47, 23-25. Mahill, J . H., and Davis, D. D. 1978. Crop Sci. in press. Marani, A. 1963. Crop Sci. 3, 552-555. Marani, A. 1964. Crop Sci. 4, 265-268. Marani, A. 1967. Crop Sci. 7, 519-522. Marani, A. 1968a. Crop Sci. 8. 36-38. Marani, A. 1968b. Crop Sci. 8, 11 1-1 13. Marani, A. 1968c. Crop Sci. 8, 299-303. Marani. A. 1968d. Crop Sci. 8, 653-657. Marani, A,, and Avieli, E. 1973. Crop Sci. 13, 15-18. Meredith, W. E., and Bridge, R. R. 1972. Crop Sci. 12, 304-310. Meredith, W . E., and Bridge, R. R. 1973. Crop Sci. 13, 551-552. Meredith, W. E . . Jr., Ranney, C. D., Laster, M . L., and Bridge, R. R. 1973. J. Environ. Qual. 2, 141-144. Meyer, V. G. 1969. Crop Sci. 9, 237-242.

.

156

DICK D. DAVIS

Meyer, V. G. 1971. J. Hered. 62, 77-78. Meyer, V. G. 1973a. Proc. Beltwide Cotton Prod. Res. Conf., Nail. Cotton Counc.. 1973, p. 65. Meyer, V. G. 1973b. Crop Sci. 13, 439-444. Meyer, V. G . 1973c. Crop Sci. 13, 778. Meyer, V. G. 1975. J. Hered. 66, 23-27. Meyer, V. G.,and Meyer, J. R. 1965. Crop Sci. 5 , 4441148. Miller, P. A., and Lee, J . A. 1964. Crop Sci. 4, 646-649. Miller, P. A., and Marani, A. 1963. Crop Sci. 3, 441-444. Moffett, J. O., Stith, L. S., Burkhart, C. C., and Shipman, C. W. 1975a. Environ. Entomol. 4, 203-206. Moffett, J. O., Stith, L. S., Burkhart, C. C., and Shipman, C. W. 1975b. Crop Sci. 15, 782-784. Muramoto, H., Hesketh, J., and El-Sharkawy, M. 1965. Crop Sci. 5, 163-166. Niles, G.A,, and Richmond, T. R. 1962. Tex., Agric. Exp. Sin., Misc. Publ. MP-577, 1-9. Niles, G.A., Walker, J. K., Jr., and Gannaway, J. R. 1974. Proc. Beltwide Cotron Prod. Res. Conf., Nail. Cotton Counc.. 1974. pp. 83-85. Omran, A. 0.. El-Ganayni, A . E., and Galal. H. 1974. Cotton Grow. Rev. 51, 192-209. Patel, C. T. 1971. Corron Dev. 1(2), 1-5. Peebles, R. H. 1929. J. Hered. 20, 340-347. Peebles, R. H. 1956. Am. Bee J. 96, 51-53. Poehlman. J. M. 1959. “Breeding Field Crops,” pp. 290-294. Holt, New York. Quinby, J. R., and Schertz, K. F. 1970. I n “Sorghum Production and Utilization.” (J. S. Wall and W. M. Ross, eds.). Avi Publ. Co., Westport, Connecticut. Quisenbeny, J. E. 1975a. Crop Sci. 15, 197-199. Quisenbeny, J. E. 1975b. Crop Sci. 15, 202-204. Ramey, H. H. 1962. Crop Sci. 2 , 269. Ray, L. L., and Hudspeth, E. B. 1966. Agron. Abstr., p. 30. Reed, W., 1974. Cotton Grow. Rev. 51, 106-123. Richmond, T. R., and Kohel, R. J. 1961. Crop Sci. 1, 397401. Rosales, F. E., and Davis, D. D. 1976. Crop Sci. 16, 99-10], Roux, J. E. 1961. Coron Fibres Trop., Engl. Ed. 14, 363-70. Sarvella, P. 1966. Crop Sci. 6, 361-364. Saunt, J. E. 1967. Cotton Grow. Rev. 44, 190-202. Schubert, A. M., Benedict, C. R., Gates, C. E., and Kohel, R. J. 1976. Crop Sci. 16, 539-543. Schuster, M. F., Lukefahr, M. J . , and Maxwell, F. G. 1976. J. Econ. Entomol. 69, 400-402. Shepherd, R. G. 1974. Crop Sci. 14, 872-875. Simpson, D. M. 1954. US.,Dep. Agric., Tech. Bull. 1094. Simpson, D. M., and Duncan, E. N . 1953. Agron. J. 45, 275-279. Singh, I. D., and Weaver, J . B. 1972a. Crop Sci. 12, 294-297. Singh, I. D., and Weaver, J. B. 1972b. J. Econ. Entomol. 65, 821-824. Sinha, S. K., and Khanna. R. 1975. A h . Agron. 27, 123-174. Smith, R. A., and Falcon, L. A. 1973. Cotton Grow. Rev. 50, 15-27. Staten, G. 1971. New Mexico Stare Univ. College Agric. Home Econ.. Memoir Ser., No. 4, 48 pp. Stephens, S. G.,and Lee, H. S. 1961. J. Econ. Ent. 54, 1085-1090. Stith, L. S. 1974. Proc. Beltwide Cotton Prod. Res. Conf., Natl. Cotton Counc., pp. 145-146. Stroman, G. N. 1961. Crop Sci. 1, 363-366. Sundaram, K. 1975. In “Cotton International,” 43rd ed., pp. 166-168 and 247. Meister, Memphis, Tennessee. Textile Topics. 1976. Textile Research Center, Lubbock, Texas.IV(8) 4 pp. Thies, S. A. 1953. Agron. J. 45, 481-484.

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Tingey, W. M., Leigh, T. F., and Hyer, A. H. 1975. Crop Sci. 15, 251-253. Thomson, N . J. 1971. Aust. J. Agric. Res. 22, 759-770. Thomson, N. J. 1972. Aust. J . Agric. Res. 23, 285-293. Thomson, N . J. 1973. J . Agric. Sci. 80, 147-160. Towery, J. D. 1975. Proc. Tech. Semin. Open-End Spinning, Nail. Cotton Counc. pp. 33-39. Tupper, G. R. 1966. Trans. Am. SOC.Agric. Eng. 9, 1 10-1 13. Turcotte, E. L., and Feaster, C. V. 1974. In “Haploids in Higher Plants” (K. Kasha, ed.), pp. 53-64. Turner, J. H. 1953a. Agron. J . 45, 484-486. Turner, J. H. 1953b. Agron. J . 45, 487-490. Uzenbaev, E. H. 1967. Tr. Vses. Nanchno-Issled. Inst. Khlopkovod. 12, 82-100, Plant Breed. Abstr. 41, 408 (1971). Verhalen, L. M., and Murray, J. C. 1967. Crop Sci. 9, 31 1-315. Verhalen, L. M., and Murray, J. C. 1967 Wakelyn, P. J. 1972. Text. indu. (arlanta) 136 92-99. Wanjura, D. F. and Hudspeth, E. B., Jr. 1963. Tex., Agric. Exp. Stn., Prog. Rep. 2266. Ware, J . 0. 1930. J . Am. Soc. Agron. 22, 787. Ware, J. O., and Harrell, D. C. 1944. Agron. J . 36, 976-987. and Harrell, D. C. 1963. Crop Sci. 3, 163-165. Ware, J. 0.. Ware, J. 0.. Jenkins, W. H., and Harrell, D. C. 1943. J. Amer. SOC. Agron. 32, 382-392. Watson, D. J. 1952. Adv. Agron. 4, 101-146. Weaver, D. B., and Weaver, J. B., 1977. Crop Sci. 17, 491499. Weaver, J. B., Jr. 1968. Crop Sci. 8, 598-600. Webster, J. A. 1975. US.,Dep. Agric.. Misc. Publ. 1297. Wessling, W. H. 1958. J. Econ. Entomol. 51, 502-506. White, T. G., and Richmond, T. R. 1963. Crop Sci. 3, 58-63. Wirth, W. 1975. Proc. Tech. Semin. Open-End Spinning, Natl. Cotton Counc., 1975. pp. 12-19. Young, E. F., Jr. 1975. Crop Sci. 15, 59-61. Young, E. F., Jr.. and Murray, J. C. 1966. Crop Sci. 6, 436-438.

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ADVANCES IN AGRONOMY, VOL. 30

THE USE OF PHOSPHATE ROCK FOR DIRECT APPLICATION TO SOILS1 F. E. Khasawneh and E. C. Doll

Division of Agricultural Development, Tennessee Valley Authority, Muscle Shoals, Alabama

...... . . . . . . . . 159 ............................... 161 A. Mineralogy ......................................................... 161 B. Apatitic Rocks ........... .......................

I. Introduction . . . . . . . . . . . . . . . .

11. Mineralogy and Chemistry of Ph

A. Soil Conditions Necessary for Phosphate Rock Dissolution .....

C. Residual Effects of Phosphate Rock D. Partially Acidulated Phosphate Rock. . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

204

I. Introduction

The direct application of phosphate rock (PR) to soils as a source of fertilizer phosphoms (P) is a practice that has been employed with varying degrees of popularity over the years. Numerous experiments have been conducted during the past 100 years or more to determine the most favorable soil and cropping conditions for its use. Nevertheless, according to the 1975 FA0 Annual Fertilizer Review, direct application of PR accounted for only 5.0% of the total world consumption of nearly 24 million metric tons of P205in the 1974-1975 fertilizer year. Of the approximately 1.2 million tons of P,O, applied as PR, 73% was used in the Soviet Union, and about 20% was used in the developing countries, mainly in Latin America and Africa. Most of the remaining 7% was used in Western Europe. These figures do not include the application of about 400,000 IThe following abbreviations are used in the text: PR = phosphate rock, PAPR = partially acidulated phosphate rock, FA = fluorapatite, HA = hydroxyapatite, CA = carbonate apatite or francolite, DCPD=dicalcium phosphate dihydrate, DCPA=dicalcium phosphate anhydrous; SP= superphosphate; OSP = ordinary superphosphate, CSP = concentrated superphosphate, SPE = superphosphate equivalent, RAE = relative agronomic effectiveness, REE = relative economic effectiveness. 159 Copyright @ 1978 by Academic Press, tnc. All rights of reproduclion in any form reserved.

ISBN 0-12~ooO730-4

160

F. E. KHASAWNEH AND E. C. DOLL

tons annually in the People’s Republic of China (Anonymous, 1973), or the use of indigenous sources of PR in many countries for which statistics are not available. In general, experimental results have shown that PR is most effective when used on acid soils that are extremely deficient in P. Lipman et al. (1916) published a brief, but excellent, review of early work to increase the availability of P in PR by “methods that could be used on the farm for increasing the availability of tricalcic-phosphate,” and Rogers et al. (1953) and Russell (1973) have reviewed more recent research in this area. Even when conditions are favorable for the use of PR, maximum yields obtained are nearly always lower than those obtained with soluble P. In addition, the relative effectiveness of PR appears to be unaltered in some cases and markedly decreased in others when liming materials are applied to decrease soil acidity and increase soil calcium levels. Experimental results have been erratic and sometimes conflicting and have led to considerable confusion and disagreement regarding PR. Russell ( 1 973) states that “the fertilizer value of rock phosphate is erratic; it is sometimes ineffectual on acid soils with crops where one would expect it to be suitable. It is a fertilizer of strictly limited value for intensive temperate agriculture, since it cannot maintain a sufficiently high phosphorus concentration in the soil solution for high yields of crops with a high initial phosphorus demand; and it is usually inert in neutral and calcareous soils. It can, however, be suitable for many acid soils in tropical agricultural systems where very high yields are not sought and sulphur is not deficient, because it is the cheapest source of phosphorus. The authors of this chapter contend that most of the confusion and differences in opinion regarding the effectiveness of PR can be resolved if differences in the chemical and mineralogical composition of the various sources of PR are considered and if the factors affecting PR dissolution in soils are quantified by applying known and accepted principles of soil chemistry. In the discussions that follow, it will be shown that, although the source and form of PR are important, its effectiveness in any particular soil is determined largely by three soil factorspH and the concentration of P and Ca in the soil solution. If the level of any one of these factors is not conducive to PR dissolution in the soil, it will be ineffective. Furthermore, changes in the level of any of these factors during the growing season will alter the effectiveness of PR. In addition, differences between crops in their ability to utilize P from PR must be considered; these differences can be related to differences in their demand patterns for P and Ca, to differences in their effect on soil pH, and to the extensiveness of their root systems. No attempt will be made in this discussion to cite the numerous published reports dealing with the use of PR. Rather, we shall attempt tc evaluate systematically the various factors related to the utilization of PR as a source of P for plants. We do not see a need for further extensive field evaluations of PR; rather, the various factors relating to the reactivity of PR’s and the various soil and crop parameters related to PR utilization that will be discussed in the following sec”

PHOSPHATE ROCK IN SOILS

161

tions need to be elucidated and quantified in such a manner as to permit advisory scientists to estimate the probable agronomic effectiveness of a given PR. The data to be presented will show clearly that the use of PR is not suitable for intensive agricultural production, since, to paraphrase Russell (1973), PR cannot maintain a sufficiently high concentration of P in the soil solution for high yields of crops with high P requirements. This is substantiated by the trends in the use of PR in the United States as agricultural production has intensified; in 1951, 16% of the P205used was applied as PR (Rogers er al., 1953), whereas in the 1974-1975 fertilizer year, only 0.2% of the P205used was applied as PR (Food and Agriculture Organization, 1975). However, PR may be a suitable source of P in extensive agricultural systems where suboptimum yields are expected because of limits on additional inputs; in these cases, the relative amounts and costs of PR and soluble P fertilizers required to obtain the desired yield need to be compared. II. Mineralogy and Chemistry of Phosphate Rocks A. MINERALOGY

Phosphate-bearing minerals occur in all geologic settings-sedimentary, metamorphic, and igneous deposits. Deposits from all three classes are mined and beneficiated to obtain PR. Economically, the sedimentary deposits are the most important of the three, with nearly 85% of the PR mined worldwide coming from such deposits (Notholt, 1974). For a discussion on geology, formation, weathering, and other related properties of PR ore bodies, the reader is referred to reviews by Cathcart (1978) and Lehr and Home (1978). This section will be limited to a discussion of the characteristics of these deposits as they relate to PR suitability for direct application. The physical and chemical characteristics of igneous and metamorphic rocks render them quite unreactive and nearly inert for direct application. They are coarsely crystalline substances and do not possess internal surfaces. By contrast, sedimentary PR’s are microcrystalline in nature, and consist of fairly open, loosely consolidated aggregates of microcrystals with a relatively large specific surface area. Igneous rocks often possess a chemical composition that is very close to the theoretical stoichiometric composition of fluorapatite. Furthermore, they generally have less accessory or gangue minerals than sedimentary rocks (Lehr, 1967). As a result of these two factors, chemical analyses usually indicate higher P contents in igneous rocks than in sedimentary rocks. Although a higher P content is a desirable chemical quality factor if the PR is to be acidulated for manufacturing concentrated superphosphate (CSP) or phosphoric acid, it is generally an irrelevant factor if the PR is to be used for direct application. This point will be pursued further in later sections. Sedimentary rocks are composed of microcrystalline carbonate fluorapatites,

I62

F. E. KHASAWNEH AND E. C. DOLL

often also known as francolites, which occur in association with a variety of minerals and other compounds. Considerable amounts of accessory minerals and impurities are removed by beneficiation, but the beneficiated ore retains some of the original impurities. Impurities of commercial PR concentrates consist largely of silica, silicates, alkaline earth carbonates, hydrated oxides of Fe and Al, or combinations of some or all of these substances in varying concentrations. These impurities have a profound influence on the performance of PR used for direct application. Phosphate rocks are also classified according to their mineralogical composition (McClellan and Gremillion, 1978) into three types. In the order of increasing economic importance, they are Fe-A1 phosphates, Ca-Fe-A1 phosphates, and Ca phosphates. The most common mineral groups in the first class are wavellite [A&(PO,h(OH), *5H20],variscite (AIP04*2H20),and strengite (FeP04.2H20). Economically significant deposits of such minerals are found in Senegal, Liberia, Brazil, and Utah. The second class includes principally crandallite [CaAh(PO&(OH), H,O] and millisite [(Na,K)CaA&(PO,),(OH), * 3HzO]. Such minerals are found in the leached zones of Florida deposits and in the C-zone of Christmas Island deposits. The third class consists of the familiar apatitic group of minerals distinguished by a common crystal structure. This structure is exemplified by fluorapatite [Ca,o(P04~Fz] which occurs as such in nature only in few known rare cases. Apatites exhibit a rather wide range in chemical composition, which causes a correspondingly wide range in properties, and which is attributed to extensive isomorphous substitution in the apatitic crystal lattice. Examples of sedimentary apatites are the extensive deposits in North Africa (Senegal, Togo, Morocco, Algeria, and Tunisia), the Middle East (Jordan, Israel, and Egypt), Australia (Queensland), and the United States (Florida, North Carolina, and Idaho). The three classes of PR often occur as a weathering sequence, with Fe and A1 phosphate representing the most intensely weathered and stable end of the sequence, and the apatites representing the least weathered (McClellan and Gremillion, 1978). The discussion that follows in this chapter will be oriented heavily toward sedimentary apatites, largely as a reflection of the economic significance of this type of ore bodies.

B. APATITIC ROCKS

I . Compositional Differences Extensive chemical characterization of a large number of samples collected from about 560 PR’s has been carried out by the Tennessee Valley Authority,

PHOSPHATE ROCK IN SOILS

163

and the data have been periodically reported (Lehr, 1967; McClellan and Lehr, 1969; Lehr and McClellan, 1972). The pertinent parts of these data can be briefly summarized as follows: (1) Isomorphous substitution in the basic fluorapatite structure is the norm, with “true” stoichiometric fluorapatite being exceptionally rare, and limited to few igneous deposits. Partial substitution of nearly all the ionic components in the fluorapatite structure was reported: Ca2+is mostly substituted for by Mgz+and Na+, and to a lesser extent by Sr”, Mn2+, K+, U4+,Fez+, and some rare earth metals. The PO!- tetrahedra are replaced mostly by Cog-, and to a lesser degree by SO’,-, SiO’,-, AsO!-, VOq-, CrOt-, and A10%-.The F- ion is replaced by OH- and C1-. (2) The composition of sedimentary apatites can be closely approximated by their contents of Ca, Mg, Na, P, F, and C. The composition of a representative group of apatites is shown in Table I. (3) Substitution of planar COZ- for tetrahedral PO:- is coupled to additional substitutions. The vacant 0 site is partially filled by F, and the balance of the charge deficit is partially corrected by substitution of monovalent cations, mostly Na for Ca. There is also substitution of Mg for Ca, but this is independent of charge deficit requirements. The COi- for PO:- substitutionprofoundly influences the crystal structure, the physical stability (McClellan and Lehr, 1969), and the chemical stability of apatites. (4) Because the principal substitutions are coupled, natural sedimentary apatites can be represented by the average formula Ca,,-a-bNaaMgb(PO,),-=(CO,),F,+,

The theoretical and observed limit on x is that nl(6-x) be less than or nearly equal to 0.3. Higher substitution disrupts the apatite structure. On the average, y = 0 . 4 ~ and . b, a, andx are interrelated as given below. This compositional series is often called carbonate apatite, or francolite. The two designations are interchangeable. 2 . Effect on Crystalline Properties Results of measuring cell parameters on nearly 500 francolite-bearing PR’s showed that substitution of Cog- F- for PO:- influenced the a and c dimensions of the apatite crystal structure, with a ranging from 9.322 A for highly substituted francolites to 9.376 A for zero substitution (that is, fluorapatite), while the c dimension ranged from 6.877 to 6.900 A, respectively. The standard error of measurement was k0.003 A (McClellan and Gremillion, 1978). These variations are systematic and directly proportional to the degree of substitution. Lehr and McClellan (1972) derived the following regression equations:

+

TABLE I Gross Composition of a Representative Group of Phosphate Rocks, and Composition of the Apatite Component Contained in Them” Source location

Ca

P

F

C

Na

Mg

K

A1

Fe

Si

34.7 34.5 33.9 33.4 30.2 38.7 35.8

13.0 14.1 14.3 14.1 13.4 17.5 15.1

3.5 3.7 3.6 3.2 3.2 3.6 3.4

1.5

0.73 0.50 0.49 0.71 0.30 0.08 0.20

0.33 0.28 0.19 0.22 0.17 0.02 0.38

0.11 0.17 0.12 0.30 0.54 0.02 0.13

0.24 0.40 0.63 0.58 0.74 0.16 0.18

0.48 0.51 1.01 0.31 0.84 0.28 1.82

0.7 1.3 2.4 2.5 4.7 0.6 1.3

Typeb

North Carolina (clastic phosphorite) North Florida (Occidental) Florida Pebble (Polk County) Idaho shale phosphorite Tennessee brown, Columbia India (Jhamar-kotra district)‘ Missouri

S

S

S S S

M 1

1.1

0.9 0.7 0.4 0.2 0.8

Composition of the Apatite Component Ca (I

North Carolina North Florida Florida Pebble Idaho Tennessee India Missouri

(A)

9.322 9.334 9.345 9.356 9.357 9.365 9.373

F

Found” Calculatedd 34.4 34.6 33.9 33.4 30.8 38.8 35.0

34.2 35.0 33.7 32.9 30.9 38.9 34.2

P 13.2 14.1 14.1 14.3 13.4 17.5 15.8

C

Mg

Na

Found Calculated Found Calculated Found Calculated Found Calculated 3.6 3.8 3.8 3.4 3.2 3.6 3.5

4.2 4.1 3.8 3.5 3.2 3.8 3.3

I .4 I .o

1.3 .

1.0 0.5 0.4 0.2 0.1

0.8 0.5 0.4 0.2

1.1

-

0.3 0.2 0.2 0.1 0.1

0.3 0.2 0.2 0. I 0. I

-

-

0.3

0.8 0.5 0.5 0.7 0.2 0. I

0.7 0.5 0.4 0.2 0.2 0. I

0.2

-

‘From Lehr and McClellan (1972). Analysis converted from the oxide to the elemental basis. bS = sedimentary, M = metamorphic, 1 = igneous. CHigh-grade material from block D-zone, Hindustan Zinc Co., Udaipur, India. “Found by chemical analysis of the apatite phase after removal of accessory carbonate minerals by treatment with Silverman’s solution. The calculated data based on the theoretical apatite composition from x-ray data and actual P content from chemical analysis.

165

PHOSPHATE ROCK IN SOILS

-

A

a(obs., by x-ray) = 9.374 - 0.024 6-x a(Na) = 1.327 b(Mg) = 0.515

X -6-x

*

X 6-x

which permits calculation of x (COi- substitution for PO:-) from x-ray data, from which Na and Mg substitution follows. In addition to changing the cell constants of apatite, isomorphous substitution of Cog- for PO!- also decreases the crystallite size (McClellan and Lehr, 1969; LeGeros et al., 1967) and increases the specific surface area of the apatite aggregates (Table 11). A decrease in the crystallite size with increasing substitution indicates that structural incompatibility develops between CO 3- and the POf framework and limits the number of permissible unit-cell repetitions before misfits in the structural units prevent further growth of the individual crystallites. McClellan and Lehr (1969) reported that crystallite sizes ranged from 300 to 2000 A.

3. Accessory Minerals The nature and quantity of accessory minerals that are found in PR have marked influence on their suitability for direct application. The most common accessory minerals are silica, alkaline earth carbonates, layer silicates, Fe and A1 oxides and hydroxides, and evaporites (chlorides and sulfates). There are two basic textures of sedimentary PR-consolidated and unconsolidated. The consolidated rocks are cemented by silica, silicates, carbonates, and/or by oxides of Fe and Al. Each is exemplified by extensive known deposits (McClellan and Gremillion, 1978). Unconsolidated rocks have been concentrated by secondary geologic processes, such as leaching and weathering, and are typified by the land pebble PR of central Florida. The major accessory minerals are present as discrete mineral grains. Accessory carbonate minerals are easily recognized by their rhombic crystals, which distinguish them from carbonate apatites (francolites). Beneficiation usually removes a considerable amount of accessory minerals found in the ore, yet substantial amounts are often retained in the commercial concentrates known as PR. Silica and silicates are largely removed by beneficiation, whereas carbonates are not. For PR intended for fertilizer manufacture, carbonates can be removed by calcining and slaking, but calcining destroys the microcrystalline structure of PR and therefore is not suitable for PR intended for direct application. The oxides

166

F. E. KHASAWNEH AND E. C. DOLL TABLE I1 Effect of C0:- Substitution on Surface Area of Screened Fractions of Selected PR“ Screened fractions, mesh sizes:

Source

X”

North Carolina North Florida Central Florida Idaho Tennessee India Missouri

I .26 0.932 0.845 0.490 0.439 0. I63

- 150 +200

-200 +325

-325 +5pm

Calculated surface areaP

(mW

m2/&

0.048

34.0 20.0 8.2 3.3 17.0 3. I 2.5

36.0 22.0 9.0 2.8 19.0 3.2 7.8

37.0 26.0 9.7 4.5 23.0 3.8 2.2

75.0 39.5 44.0 32.6 32.6 9.4 9.4

“From Lchr and McClellan (1972). “Moles of C 0 3 per mole of apatite, determined chemically. ‘Surface area calculated from crystallite size determined by x-ray methods. dMeasured by the toluene-acetic acid method. Tennessee PR contained large proportions of layer silicates as accessory minerals; hence the large measured surface area.

and hydroxides of Fe and A1 in sedimentary ores are not easy to separate and are retained in the PR. Washing usually reduces contents of accessory chlorides. The effect of these accessory minerals on PR reactivity and on availability indexes of PR will be discussed in later sections. 111. Reactions of Phosphate Rocks in Soils

A. SOIL CONDITIONS NECESSARY FOR PR DISSOLUTION

It has generally been recognized that, when water- and citrate-soluble P fertilizers are applied, the initial reaction products precipitated in soil are metastable and tend to change toward more-stable, less-soluble end products. In neutral and calcareous soils, the ultimate end product is principally hydroxyapatite (HA) and if there is sufficient F in soil, fluoroapatite would represent an even lower state of free energy. So, if soluble phosphates tend to precipitate out as some form of hydroxy- or fluorapatite, then why would carbonate apatite (francolite) dissolve or react in soil in such a manner as to provide P to the soil solution in a form available to plant roots? To be sure, apatitic PR tends to persist in soils, and sometimes for extended periods of time. Published reports indicate that some PR’s persist in their original

PHOSPHATE ROCK IN SOILS

167

form for at least 40 years in some soils. In acid or moderately acid soils, on the other hand, the lowest free energy form of soil P is not apatite but A1 and Fe phosphates. This is the fundamental factor that causes PR to react in certain soils; it also gives the course and direction of PR reactions, although in broad general terms, without specifying intermediate steps or the exact chemical makeup of the end products. The microscale details of this transformation involve dissociation from the apatite surface and reprecipitation of increasingly stable phases of soil P. These processes are essentially a sequence of rate processes, which are greatly influenced by the extensity of surfaces of the dissociating components, and by kinetics of crystal nucleation and growth of the precipitating phases. Obviously, a number of other factors influence these rate processes. The discussion that follows elaborates on all factors involved. 1 . The Driving Force for PR Dissolution

It has generally been recognized that the agronomic effectiveness of PR is higher on acid soil than on neutral or alkaline soils (Peaslee et al., 1962; Ensminger et d.,1967; Barnes and Kamprath, 1975). Over the years, soil acidity has been considered the single most important agent responsible for enhanced availability of P in PR materials. Peaslee et al. (1962) expressly singled out soil pH (vis-a-vis soil pCa) as the most important soil factor in PR dissolution. Ellis et al. ( 1955)observed that oats responded better to PR when it was applied to the soil 1 month prior to liming to pH 7 than when the order of addition was reversed. Graham (1955) and Howe and Graham (1957) showed that the bonding energies for Ca in clay suspensions and in cation exchange resin systems were important factors in PR dissolution. Work by Khasawneh and Engelstad (1975) on the effect of pH in submerged rice soils on the availability of P from PR and by Khasawneh (1977) proved conclusively that a soil’s affinity for Ca is a significant factor, which enhances PR dissolution and the availability of its P to plant growth. The congruent dissolution of apatites will entail the dissociation from the apatite surfaces of the ions Ca2+, Poi-,and F-, and to a lesser extent the isomorphically substituted ions such as Mg2+,Na+, CO:-, and OH-. The PO:ions are quickly protonated to H,PO- and HPOZ-. The driving force for PR dissolution, therefore, must be related to gradients in the chemical potentials of these ions. In order to lay a foundation for this discussion, let us first consider thermodynamically the solubility product of fluorapatite (FA) and its substitution isomorph, francolite. Chaveni and Black (1966) were among the first to do this; they invoked the solubility product principle to give a theoretical discourse on FA and HA solubility and solid solutions of both, and showed how it could be presented in the form of solubility product isotherms. More recently, Chien and Black (1976) and

168

F. E. KHASAWNEH A N D E. C. DOLL

Chien (1977a) discussed the free energy of formation and the free energy of acid dissolution of carbonate apatites (CA), respectively. Data presented by Chien and Black (1976) indicated that the solubility product of five francolites varied with the degree of COi- substitution in the apatite structure. Their data show the following relationship: PKCA = 122.2 - 6 . 3

(1)

where x is the moles of COi- per mole of apatite, and pKcA is the negative logarithm of KcA,the solubility product of CA. This relationship, when extrapolated tox = 0 (that is, FA) gives pKFA = 122.2, which is higher than 119.2 for synthetic FA (McCann, 1968) or 120.86, as measured by Farr and Elmore (1962), but lower than the value measured by Chien and Black (1976) for an igneous FA from Missouri (pKFA= 133.4). It is not our purpose to evaluate these constants critically; so, for the purpose of illustratingcertain points on solubility of francolites, the regression equation given above (Eq. 1) will be used, thus setting p K F A at 122.2. For FA in equilbirium with fluorite (CaFz), we can write pHzP04 + HpCa = 2(pH - HpCa)

+ 1 / 6 ( p K ~-~ ~

K c ~ 6pKz F ~ - 6pK3)

where pKz and pK3 refer to the second and third dissociation constants of &Pod. Values of pKCaF2,pKz, and pK3, taken from Lindsay and Vlek (1977), will give (pHzP04 + HpCa) = 2(pH- HpCa) - 0.82 pHzP04 = 2pH - 1.5pCa - 0.82

(2) (3)

Solubility product isotherms are usually presented according to Eqs. (2) or (3). In Fig. 1, pHzP04is plotted against pH for three values of Ca activities; 1.25 x l C 4 M , 1.25 x l(r3 M , and 1.0 X l C 2 M. For substituted FA, the solubility product depends on the degree of C G substitution, orx, as given in Eq. (1). The empirical formula for CA is Ca,o-a-bNaaMgb(PO4),-=(Co~)=F*+~.4~

where a= 1.327*x/(6-x), b=0.515*x/(6-x), and the apatite has a net positive charge equal to (2.27 - 0 . h ) x/(6 - x ) per formula weight. From this formula, along with Eq. (l), equations analogous to (2) and (3) were derived; these are listed in Table 111. The phosphate potential (pHzP04 + MpCa) is seen to be a function of both the lime potential (pH - 'h pCa) and pCa (Table 111). By contrast, the phosphate potential for FA is a function of only the lime potential, and is independent of pCa, as given by Eq. (2). The equations listed in Table I11 are based on values of (Na) and (Mg) that are assumed to be related to (Ca) in the following manner:

-

169

PHOSPHATE ROCK IN SOILS FA - - , X g O

CA

4.0

5.0

---,

X.1.5

6.0

7.0

8 .O

9.0

PH

FIG. I .

Solubility isotherms of fluorapatite (FA) and a highly substituted carbonate apatite (CA,

x = I .5) in equilibrium with fluorite, as related to pH and pCa. Note that the isotherms of FA and

CA intersect at different pH levels, depending on pCa.

(Mg2+)= 0.25(Ca2+) (Na+) = 0.5(CaZ+) If the activities of Mg2+)and (Na+) were different, only the intercepts of the equations in Table I11 would change. When PR is applied to soil, the activities of Mg and Na are largely governed by the soil itself and are not significantly influenced by Na and Mg from the PR. The above assumptions, therefore, can be easily justified. Solubility product isotherms for francolites in equilibrium with fluorite are shown in Fig. 2 for variable degrees of substitution and levels of solution Ca. Isotherms for hydroxyapatite are shown also for comparison purposes. These

170

F. E. KHASAWNEH AND E. C. DOLL TABLE 111 The Effect of COi- Substitution on Solubility Relationships of FA and CA

pH2P0,

+ '/zpCa=

u(pH - VzpCa) - bpCa

PH,PO, -

apH - bpCa - c

c

X

U

b

C

U

0 0.25 0.50 0.75 1 .OO 1.25

2 2.087 2.182 2.286 2.400 2.626 2.667 2.333

0 0.0135 0.027 0.043 0.060 0.079 0.100 0

0.82 I .33 1.89 2.50 3.17 3.92 4.74 4.83

2.000 2.087 2.182 2.286 2.400 2.526 2.667 2.333

Iso HA

=

b

c

1.500 1.557 1.618 1.686 1.760 1.842 1.933 1.667

0.82 1.33 1.89 2.50 3.17 3.92 4.74 4.83

plots, therefore, indicate that the driving force for PR dissolution consists in the following components: (1) Gradients in pH, where solubility increases with decreasing pH. (2) Gradients in pCa, where solubility increases with decreasing activity of Ca in the soil solution. (3) Gradients in H2P0c activity in the soil solution, where solubility is enhanced if there is a sink to reduce (H2P04-), and hampered if (H2P04-) is at an elevated level. For these three gradients, this is the familiar Le Chatelier principle in action. (4) At pH values below certain levels, solubility increases with increasing Cog- substitution.

The first three factors are soil factors, and the fourth is a PR factor, which determines the reactivity of the PR material. The limitation on the effect of Cogsubstitution on solubility expressed in (4) above comes about as a result of each group of isotherms intersecting at pH levels that seem to depend on pCa (for example, pH 8.42 at pCa 3.9, pH 7.77 at pCa 2.9, pH 7.58 at pCa 2.6, and pH 7.18 at pCa 2.0). At these intersection points, solubility is invariant with respect to the degree of substitution, but at pH values higher than the intersection points the effect of Cog- substitution on solubility is reversed: It decreases with increasing substitution. In other words, there are certain critical levels of pH beyond which the francolites represent forms of apatite that are thermodynamically more stable (lower free energy form) than FA.

171

PHOSPHATE ROCK IN SOILS

At lower pH values, solubilities of francolites increase with x, the number of moles of CO $- per formula weight of apatite, and the lines seem to approach the hydroxyapatite lines. More important, the increasing degree of CO$- substitution seems to bridge the gap between the isotherms of pure HA and pure FA. We should like to emphasize this point because it is a vivid illustration of how isomorphous substitution in naturally occumng minerals may lead to solubility isotherms that for all practical purposes are likely to lie anywhere between two pure mineral species such as FA and HA. Furthermore, there is yet another substitution series involving substitution of OH- for F (fluor-hydroxyapatites), especially in apatite deposits derived from organic origin, such as the Sechura deposit in Peru or the deposits on Curacao Island. The isotherms for this O W series also lie between the FA and HA lines. Quite often analytical soil solution data, when plotted on solubility diagrams, do not fit the isotherms of any known “pure” crystalline compound. This is often cited as proof that there is no known

4

5

6 PH

7

8

I 3

I

I

I

4

5

6

p H - 92 PCa

FIG. 2. The effect of isomorphous substitution of Cog- in the apatite structure and of pCa on solubility isotherms of fluorapatite (FA) and carbonate apatite (CA) in equilibrium with fluorite. Numbers to the left of the isotherms indicate the number of moles of CQ per formula weight of apatite. Isotherms for hydroxyapatite and for variscite in equilibrium with gibbsite are shown for comparison.

172

F. E. KHASAWNEH AND E. C. DOLL

crystalline phase in soil that controls P solubility. The parallellism between the two situations is inescapable. Actually, pure FA and pure HA are quite rare in nature, and isomorphous substitution is the rule rather than the exception (McClellan and Gremillion, 1978). Data points that fall between the HA and FA isotherms may indicate that the crystalline phase is not one of the rare stiochiometric species, but rather a more common isomoxphically substituted species. The data in Fig. 2 represent pH2P04in relation to pH and pCa. The meaning of pH,PO, is not readily apparent, especially since there are other soluble ions and ion pairs, the sum of which constitutes total solution P as would be determined by an analyst. In solution, the P a - ion is protonated to varying degrees, depending on pH, and is also paired with such ions as Ca2+,Mg2+, Zn2+,Fe3+, and A13 Again to illustrate a point, let us assume that only Ca2+ and H+ are present; then the other soluble P-containing ions and ion pairs will consist of HPO$-, PO!-, CaH2P04+,and CaHPO,, and the activities of each are related to pH and pH,PO,. Thus, concentrations of each of these ions and ion pairs can be calculated and summed to give [PT].The results of such calculations are shown in Fig. 3, where [PT]is expressed in parts per million. This brings us to yet another factor, which affects [PT] but not (H,PO:-)ionic strength.,/Par the normally dilute soil solutions, increasing ionic strength leads to’decreasing activity coefficients and, therefore, to increasing concentrations of ionic species, especially the polyvalent ones. The effect of ionic strength is small when compared with the effects of pH or pCa, but it is real nevertheless. This effect is illustrated in Fig. 3B. As a relatively insoluble material, the extensity of the apatite surface per unit weight of PR must be mentioned here The factors enumerated above will determine the total driving force for PR dissolutionper unit surface urea, so naturally the driving force (for dissolution) per unit weight of PR will also be affected by its specific surface area. It was mentioned earlier (Section 11) that isomorphic substitution of COJ- for PO:- leads to smaller crystallite sizes, that sedimentary apatite aggregates are quite porous and possess large internal surfaces, and that specific surface area is highly correlated to COJ- substitution; thus, the larger surface area favorably compounds the positive effect of CO J- substitution on PR reactivity. The data in Fig. 3 give some rather high concentrations of P when pH is between 5.0 and 6 . 5 , a common range, which is compatible with PR use. These levels of [PT1 may never be reached in soil, however, except perhaps on the apatite-soil solution interface; yet these levels of [PT] do represent an upper saturation limit. Should the soil matrix have initially high levels of &PO,-, pH, and/or Ca2+,then PR dissolution will be diminished accordingly. The data can be used to interpret the effect of incongruent dissolution of PR. If the soil matrix is capable of removing H2P04- (such as by the formation of variscite or strengite),

173

PHOSPHATE ROCK IN SOILS

,001

.01

E

-

-

.lo-

9

5!

!?i

1.0 -

10 -

I

I

I

I

I

4

5

6 PH

7

8

5

8 PH

FIG. 3. Solubility isotherms expressed in terms of P concentration (ppm). (A) Fluorapatite (FA) and carbonate apatite (CA, x = I .5) in equilibrium with fluorite as a function of pH and pCa, with ionic strength, p. set at 0.01 M .(B) CA in equilibrium with fluorite as a function of pH and p , with pCa at 3.9.

but not Ca", the H2P04-dissociates from the apatite surface and diffuses away in soil, but the Ca2+remains behind and builds up the apatite surface. The plots in Fig. 3 indicate that, when ambient Ca2+increases, activity of HzP04- and [PT] decrease. The gradient in H2P04- also decreases, which slows down diffusion of H,PO,- toward active precipitation sites, and the process of dissolution is slowed down accordingly. Likewise, the effect of changes in pCa or pH incurred by root surfaces on ambient pH,P04 or [PT]can be quite substantial, where reduced pH and Ca activity are conducive to increased concentration of P from a PR particle within the influence of the root rhizocylinder. 2 . Measurement of PR Dissolution in Soil The extent of PR dissolution has been measured only indirectly, which underscores the difficulty of directly measuring the undissolved fraction for PR and the

174

F. E. KHASAWNEH AND E. C. DOLL

equal difficulty of measuring its “reaction product. Nevertheless, several methods have been employed for that purpose. The principal ones are listed below: ”

(1) Fractionation of soil P, where the Chang and Jackson scheme (1957) or any of its later modifications are used. Increases in ALP and Fe-P fractions over a no-PR treatment are interpreted as reaction products of PR, and increases in the Ca-P fraction are interpreted as due to the persistence of PR in an unreacted form. (2) Dilute acid-N€&F extraction, usually in the manner described by Bray and Kurtz (1945), and commonly referred to as the Bray PI fraction. This extraction predominantly measures Al-P, but also some Ca-P fractions. Unreacted PR in soil would likely contribute an amount of P to Bray PI that remains constant until a substantial part of the PR has dissolved. If zero-time data are included-that is, Bray PI extraction of soil and PR at the time they are first brought together-then changes in Bray PI would be a good method of estimating the extent of PR reaction or Al-P formation. (3) Alkaline extractions of soil P, usually with 0.5 N NaHCO,, more commonly known as the Olsen method (Olsen er af., 1954). Joos and Black (1950) used 1.5% NqCO, as an extractant, and we chose to include their method here because it extracts nearly the same fractions of P as the NaHCO, extractant. These methods of extraction measure reaction products of PR dissolution in soil; that is, they hydrolyze Al-P and Fe-P that have formed, but react little with the unreacted apatites in PR. (4) Extraction with anion exchange resins. (5) Labile P as measured by isotopic exchange. In the latter two methods there is an implied assumption that, when PR dissolves and its P is transformed into Al-P, Fe-P, or whatever, lability of this P increases, and hence measurement by either of the above methods reflects the extractability of PR reaction products. Extractability of P by an anion exchange resin, however, should always take into account the fact that substantial amounts of P are extracted when PR alone is added to an anion exchange resin system (F. E. Khasawneh, unpublished data). Likewise, PR’s possess substantial amounts of isotopically exchangeable P (Olsen, 1952; Car0 and Hill, 1956). If one assumes that partial weathering of the PR particles in soil, as they dissolve and react, does not diminish their contribution to extractable P or to exchangeable P, and if one makes a zero-time measurement, then these two methods may give an indication of the extent of PR reaction in soil. These assumptions have not been shown to be valid experimentally, however, and consequently methods 4 and 5 should be used and interpreted with caution. An interesting comment on methods 4 and 5 is that they are invariably highly

PHOSPHATE ROCK IN SOILS

175

correlated to the availability of P from PR additions. This property, however, should not be equated to measurement of PR reactions in soil. In this connection, 32Phas been used by several investigatorsto measure theA value of soil amended with PR (e.g., Shapiro and Armiger, 1958; Ensminger et al., 1967; Mattingly, 1970). Neutron-irradiated PR, where stable P and Ca are transformed into 32P and 45Ca,respectively, was used by Fried and MacKenzie (1949) and by Murdock and Seay (1955). The A value by definition measures the fertilizer value of PR in terms of a standard fertilizer, such as CSP. Basically, therefore, A value measurements estimate the availability of P in PR for crop growth, but do not measure PR dissolution, per se, in soil. (6) Measurement of changes in soil exchangeable Ca. This method also attempts to measure a reaction product of PR dissolution. It is recalled that francolites in PR dissolve because ambient pH and activities of Ca2+and H2P04- are lower than the saturation level of francolite. The process continues because soil Fe and A1 (exchangeable, or in the form of oxides and hydrated oxides) act as sinks for H2P04-, with the pursuant precipitation of various forms of A1-P and Fe-P. The soil acts also as a sink for the Ca which dissociates from apatite surfaces and becomes part of the exchangeable cations. The Ca2+cannot react with H2P04-, or with combinations of Al, Fe, and H2P04,to form compounds that are less soluble than the initial apatite. There is no place for the Ca except to become an exchangeable cation. Thus, a measurement of changes in exchangeable Ca should give an indication of PR reactions in soil. All the methods enumerated above were described at the outset as being indirect, and they all have limitations. The fractionation scheme of Chang and Jackson has been used by Chu et al. (1962), Robertson et al. (1966), Amberger et al. (1971), Cescas and Tyner (1976), and others. The results of Chu et al. (1962), for example, indicated that PR (unspecified source) reacted with soil to an extent that depended on soil pH, and that increases in the Al-P fraction decreased with soil pH according to a single curvilinear relationship for five soils. Increases in the Fe-P fraction, on the other hand, depended on free Fe oxides in soils, but for a given level of active Fe, the increase in the Fe-P fraction also decreased curvilinearly with soil pH. The formation of Al-P decreased rather drastically at pH between 4.5 and 6.5, and appeared to become negligibly low at pH above 6.5. For Fe-P, its formation appeared to cease at soil pH higher than 5.5 for three soils, and at pH higher than 6.5 for two other soils. Cescas and Tyner (1976) used the Chang and Jackson procedure as modified by Petersen and Corey (1966) to estimate the persistence of Tennessee brown PR in the Morrow Plots in Illinois by measuring the Ca-P fraction in these soils. Certain plots had received 13,200 lb/acre of PR between 1904 and 1919, while others received no fertilizer since the initiation of the experiment in 1876. Addition of PR ceased after 1919, but the plots had been sampled at decade intervals

176

F. E. KHASAWNEH AND E. C. DOLL

between 1923 and 1965. The Ca-P fractions appeared to be a good index of the persistence of PR in soils. The dilute acid-N&F extractant of Bray and Kurtz (1945) (the Bray Pl fraction) was used by Joos and Black (1950), Smith and Grava (1958), Peaslee et al. (1962), Barnes and Kamprath (1975), Cescas and Tyner (1976), and others. Data generally indicate that there is a good correlation between Bray Pl extractable P and plant response from applications of PR. Peaslee et al. (1962) reported that P extracted by anion exchange resins from PR-treated soils was a better index of plant response to PR additions than was Bray Pl extractable P. Cescas and Tyner (1976) also reported that Bray Pl extractable P was inferior to 32Pexchangeable P in PR-treated soils from long-term field trials with PR. Joos and Black (1950) extracted PR-bentonite mixtures (using Tennessee PR) with 1.5% N%C03 solutions and found that the amount of P extracted was affected by the period of incubation of PR-bentonite mixtures and by the pH of the bentonite clay, and only slightly by particle size (150-300 mesh versus <400 mesh). In the incubated series, extractable P decreased nearly tenfold when clay pH increased from 4.6 to 6.6. The more familiar 0.5 M NaHCO, extractant was used by Mattingly (1968) to measure the residual value of Gafsa PR in long-term field experiments, but he did not compare this method with other methods of estimating the extent of PR persistance in soils. Table IV shows some data by Khasawneh (1978) on PR dissolution as measured by changes in exchangeable Ca. The rocks were all -200 mesh (74 pm), and the soil was Mountview silt loam, a typic paleudult, limed to pH 5.0. Dissolution increased with time, and the fraction of the PR that dissolved seemed to decrease with increasing rate of application. Dissolution increased with increasing reactivity of PR materials. The zero-time data represent the extractability of Ca from the various PR sources in neutral N N&OAc which was used in exchangeable Ca determination (10 g of soil three consecutive extractions with 25 ml of N&OAc for 30 minutes). A small but finite amount of Ca is extracted at time zero, especially from the more-reactive North Carolina PR or from rocks that contain free calcite or dolomite such as the Jordanian rock. The process of dissolution is obviously slow, especially for the less-reactive Tennessee PR. A remarkably large number of early field experiments with PR, especially the long-term residual trials, were made with this Tennessee brown PR, which explains why data from such experiments invariably indicated persistence nearly 40 years after application (Cescas and Tyner, 1976). It must be noted here that the procedure of estimating PR dissolution by measuring change in exchangeable Ca suffers from a limitation inherent to all procedures that measure change by difference; that is, it is limited to soils that have a low exchangeable Ca initially. Soils that have a relatively high cation exchange capacity can be acid enough to effect dissolution of PR, yet the initial level of exchangeable Ca may be so high that it becomes experimentally difficult to accurately measure changes in exchangeable Ca by difference.

+

177

PHOSPHATE ROCK IN SOILS TABLE IV Increases in Exchangeable Ca and in Bray P, Attributed to PR Reaction with Soil (Means of Three Replicates) Time elapsed after treatment, days Rate (mg P/kg soil)

Equiv. Ca rate, (rne/100 g)

North Carolina

8.3 33.3 133.3

0.11 0.44 I .76

me Cd100 g soil‘’ 0.02 0.1 I 0.10 0.06 0.23 0.34 0.22 0.67 1.00

El-Hassa (Jordan)

8.3 33.3 133.3

0.11 0.42 1.69

0.06 0.11

8.3 33.3 133.3

0.10 0.39 1.58

8.3 33.3 133.3

0.10 0.39 I .56

PR source

Central Florida

Tennessee

LSD (f = 0.05)

0

-

70

315

0

315

mg P/kg soil“ 0.7 3.0 3.5 12.0 13.4 58.4

0.08 0.08 0.38

0.01 0.19 0.57

0.3 1.2 4.4

1.5 7.3 29.3

0.01

0.01 0.08 0.19

0.07 0.14 0.45

0.2 0.7 2.7

1.6 8.7 29.0

-

-

-

0.01

0.09

0.1 0.4 1.9

0.7 4.1 14.0

-

0.05

0.07 0.25

0.2

“Exchangeable Ca of untreated soil was 1.46 mg per 100 g of soil, and Bray P, of untreated soil was 3.7 mg/kg of soil.

The effect on exchangeable Ca, although never before proposed as a procedure to measure PR dissolution, has been implicitly recognized for quite some time, and the effect has been designated as the “liming effect” of PR. This liming effect, however, is not limited to increasing exchangeable Ca, but is also related to partial neutralization of exchangeable Al. Hammond (1977), for example, measured increases in soil pH and exchangeable Ca and decreases in exchangeable A1 that were attributed to PR reactions in soil. The extent of these changes increased with PR reactivity, with rate of application, and with time. Some of Hammond’s data were recompiled and are shown in Table V. 3 . Kinetics of PR Dissolution

Data on the kinetics of PR dissolution are glaringly scarce, largely owing to the absence of a systematic approach to this subject matter. There are some published reports on PR dissolution in experiments where PR is suspended in a solution and agitated for relatively short periods of time. There are no comparable data for PR dissolution in a soil medium, where particles are stationary with

F. E. KHASAWNEH AND E. C. DOLL

178

TABLE V Increases in Exchangeable Ca and in Bray P, of Soil Treated with PR over the Untreated Soil, Sampled 190 Days after Treatment"** Exchangeable Ca P source

ACSI"

Rate (mg P/kg)

Sechura (Peru)

15

50 100

200

400

Cropped

Uncropped

meq/100 g soil 0.4 0.3 0.7 0.8 1.2 1.3 2.2 2.5

Bray P, cropped mgkg soil 9 17 33 62

North Carolina

20

50 100 200 400

0.4 0.8 1.5 2.5

0.5 0.9 1.7 3. I

Gafsa.(Tunisia)

18

50

0.5 1.2 1.4 2.3

0.5 0.8 1.7 2.8

40 78

0.2 0.5 0.8 1.7

0.3 0.6 I .2 1.9

6 14 31 47

0.4 0.7 I .3 I .8

0.3

0.7 I .2 1.9

7 17 24 28

0.2 0.4 0.7

0.3 0.4 0.7

6 10 20

100

200 400

Central Florida

10

50 100

200 400 Huila (Colombia)

12

50 I00 200

400 Tennessee

5

50 100

200 400

Pesca (Colombia)

10

50 I00 200 400

1.1

1 .o

0.I 0.2

0.2 0.4

0.5 0.9

0.5

0.9

8 17 38 76 9 18

35

5 9 18 30

From Hammond ( 1977). *Soil was a typic haplustox, clayey, kaolinitic, isohypothermic family, and was cropped to Guineagrass, Panicum maximum, in the greenhouse. "Absolute citrate solubility index. 'I

PHOSPHATE ROCK IN SOILS

179

respect to the soil matrix, and where the mode of dissolution is fundamentally different from the shaken flask experiment. There have been a number of longterm field trials worldwide that were originally designed for various objectives but included PR treatments. For example, Cescas and Tyner (1976) analyzed selected samples collected from the Morrow Plots in Illinois. Undoubtedly, other plots could be subjected to similar analyses to obtain invaluable insight into the kinetics of long-term dissolution processes that span years or decades. Basically, PR dissolves in a manner not unlike that of any other sparingly soluble compound applied to soil. Lime is one example, although lime is relatively more soluble than PR. Some published data on lime dissolution should be relevant to the question of PR dissolution. For example, Swartzendruber and Barber (1965) analyzed some of the extensive data of Elphick (1955) to formalize the hypothesis of equal reduction, where it is postulated that the rate of reduction in particle diameter is unaffected by particle size and varies directly with time. Swartzendruber and Barber (1965) showed that this hypothesis can be derived by assuming that the rate of dissolution is directly proportional to the total instantaneous surface area of the dissolving particles, dmldt = k ,

*

S

(4)

where m is the mass of the material that dissolves in time, t, S is the total area of the particle surfaces, and k, is the rate constant. This equation leads to 1 - (1 - /J,)''~= kt

(5)

where p is fractional dissolution of the material, and k is related to k , and to density, and inversely related to the initial diameter of the particles. Basic to Eq. (4) is the absence of concentration gradients as factors that affect the rate of dissolution. Such an omission is permissible if the concentration gradient remains constant, in which case it becomes part of the rate constant k , . In fact, even for the lime data analyzed by Swartzendruber and Barber, they recognized that such a condition is not always satisfied. The proper rate equation, therefore, should be dmldt = k&C,

-C)

where C, is the concentration of the dissolving material at the particle-solution interface, which for all practical purposes is the saturation concentration for the dissolving compound, and C is the concentration of the material in solution. It is interesting to note the variations of Eq. (6) that have been used by different authors. For example, Jurinak et al. (1977) proposed an equation identical to (6) but assumed that S would remain constant (A in their Eq. 2), which is unlikely as the particles dissolve and become smaller, but which is an acceptable approximation in the initial stages of dissolution. In a shaken-flask experiment, they arrive at the following relationship:

180

F. E. KHASAWNEH AND E. C. DOLL

In ( 1

C

- -)

c,

=

-br

where - is proportional to S. As the material dissolves, S L-creases ant k2 decreases, and with longer times the plots of In [ l - CK,] versus r begin to deviate from linearity accordingly. When dissolution is !imited by diffusion across a stagnant liquid layer surrounding the particle, Jurinak er d.(1977) showed that Eq. (6) would lead to the so-called parabolic diffusion law, where c = k3 . t ” 2 (7) In arriving at Eq. (7), the surface factors was assumed to remain constant. An equation similar to (7), namely

c = k,

*

tl’”

(8)

where n is a constant, was used by Chien (1977b) to describe the kinetics of PR dissolution in 1 N NH,OAc (pH 4.8). Plots of log C versus log t for times that ranged up to 3 hours were nearly linear when the rock-solution ratio was 1:100, and curvilinear when the ratio was 1 :2500. The value of n varied from nearly 3 to nearly 6, with no definite trend being apparent between n and the PR source. The value of k3 was related to the reactivity of the PR sources tested. Olsen (1975) empirically suggested an equation similar to (8) where n = 3. The dissolution of PR sources in solutions saturated with EDTA was measured at several intervals during a period of 48 hours. The author reported rate constants that were highly correlated to agronomic performance and to measures of PR reactivity. Curiously, however, Olsen calculated the rate constants from data collected at 7 and 12.5 hours, whereas he could have used regression techniques to employ all the data and to test whether or not the assumption n = 3 was valid. It should be pointed out here that the methods employed by Olsen and by Chien have additional limitations, which severely curtail meaningful extrapolation of their data to PR dissolution in soil. The dissolution of PR releases both Ca and P to the solution phase, and in the method of Olsen, the Ca is sequestered by EDTA, while the P builds up in solution as an acid. As dissolution progresses, the buildup of acidity becomes another factor that accelerates dissolution. Olsen’s data indicated that as much as 29.5 mg of P was dissolved in 24 hours from Curacao PR. That is nearly 1 mmole of P in 100 ml of water, and, if one goes by his reaction (l), that is equal to 2 meq of H+ per 100 ml of water, or an acidity strength of 0.02 N. Obviously, such a situation does not obtain when PR dissolves in soil. Extraction in N b O A c likewise limits the extrapolation of the data to soil situations. The dissolving vector is the mild acidity (pH 4.8), and the Ca and P

PHOSPHATE ROCK IN SOILS

181

ions released to the solution are both soluble. There is no sink for Ca or for P in such a system, and as concentrations of both ions build up in solution, dissolution will be hampered, as evidenced by Chien’s data, which caused him to assume two linear segments of the plots of log C versus log t . It is necessary, therefore, that such data be interpreted with caution. It is obvious from the foregoing discussion that kinetics of PR dissolution in undisturbed soil, or even in the shaken flask, have not been adequately investigated. If one takes into account the loosely consolidated, porous aggregate structure of sedimentary PR particles, the kinetics of their dissolution would have to consider the stagnant layer of solution that bathes the intraparticle surfaces as well as the outermost surface of the aggregate. The solution in this layer can be assumed to become saturated with respect to the solubility product of francolite. The Ca and phosphate ions diffuse away from this layer and down gradients in their respective electrochemical potentials. If the rate of diffusion away from the aggregate surface and into the soil matrix were the limiting factor in PR dissolution, then differences between PR sources and their inherent reactivities would have little influence on the supply of P to plants or on PR dissolution in soil. Experimental evidence is to the contrary, however, and differences in PR reactivity appear to have a substantial effect on PR dissolution in soil. This indicates that the limiting factor in the sequence of events discussed above is diffusion across the stagnant solution layers, both within the particles and on the outside of the particles. The surface factor of Eq. (6) cannot be ignored in any meaningful kinetic investigation of PR dissolution. Furthermore, it appears that there are different gradients for dissolution in a shaken-flask experiment, as compared with an experiment in soil, and that the factors that sustain these gradients are different in the two situations. The obvious conclusion, therefore, is that the kinetics of PR dissolution need to be investigated in soil. The data of Khasawneh (1978), presented in Table IV, give an indication of PR dissolution kinetics in moist soil. The data are not extensive enough, however, to permit calculation of rate constants. On the other hand, Cescas and Tyner (1976) calculated that the annual rate of Ca-P transformation (which could be equated to the rate of PR dissolution) was of the order of 7-1 1 kg of P per hectare (6-10 lb/acre). If one assumes that the PR was 14% P, this rate of dissolution would be equivalent to 50-80 kg of PR per hectare per year. It must be noted that these plots had not received N or K fertilizers, and, if one assumes that crop yield might have been doubled over the years by the use of N and K fertilizers, a conservative estimate, then there would have been a greater stress on the PR to dissolve, and the rate might have been doubled to 100-160 kg of PR per hectare per year. These figures provide rough estimates, especially for residual PR; even in the absence of more precise data, they provide some benchmark values that should be useful. More-reactive PR should dissolve considera-

I82

F. E. KHASAWNEH AND E. C. DOLL

bly faster, but again there are no quantitative data to permit a more precise statement.

B. EFFECT OF ADDITIVES ON PR DISSOLUTION

Numerous studies have been conducted in which the effects of various additives applied with PR have been evaluated. These materials have been either neutral or acid-forming fertilizer substances. The additives that will be discussed in this section consist of N sources, elemental S, and farmyard manure. Although partially acidulated PR materials fit into this category, the acidifying agents constitute a distinct class of additives and will be discussed separately in a later section. Acid-forming N sources tend to increase the dissolution of PR in soil and to enhance the availability of its P to plants. In a greenhouse experiment, Volk (1944) obtained higher yields of sorghum and oats when ammonium sulfate or urea rather than NaN03 was mixed with Tennessee PR. However, yield responses to PR with ammonium sulfate and urea were much lower than with an equivalent amount of P applied as ordinary superphosphate (OSP). Terman et af. (1969) reported that granulating PR with urea or ammonium nitrate resulted in ineffective P fertilizers. Granulating urea with PR did not increase P availability. Acidic materials, such as urea nitrate [CO(NHzk*HNOJ and oxalic acid, granulated with PR increased the availability of P in PR (Terman et af., 1969). However, granulating PR with acidic materials was only slightly more effective than finely divided PR alone. In all cases granulated CSP was much superior to any of the PR mixtures. The idea of mixing elemental S with PR is an old one, predicated on the premise that soil microorganisms, particularly Thiobaciffussp., would oxidize S in the soil to HzS04which would then acidulate the PR in the soil. Lipman and McLean (1918), Lipman et af. (1916), and Waksman and Joffe (1922) composted PR with soil and S and found that appreciable amounts of P were solubilized. Lipman et af. (1921) found in a field experiment with barley that combining sulfur inoculated with Thiobaciffuswith PR resulted in better yields than either PR alone or PR combined with uninoculated S. In a greenhouse study in Florida, Neller (1956) noted that S had a marked effect on solubilizing P from PR, and residual P from PR showed a 13% higher availability when S was added. In a field experiment with forage on the same soil, Neller and Bartlett (1959) noted that both yields and P content of clover and grass were increased, sometimes significantly, on plots that received 300 pounds of P z Q per acre as PR and to which S was applied, as compared with plots that received 600 pounds of P z Q per acre without S. Using 32Pat the conclusion of this experiment did not show any increased residual P availability from PR due to application of S.

PHOSPHATE ROCK IN SOILS

183

A series of greenhouse experiments were conducted in Wisconsin (Kittams and Attoe, 1965; Nimgade, 1969) in which finely ground PR was mixed with molten S, and then crushed and sieved to various particle sizes after solidifying. They stated that recovery of P by ryegrass was inversely related to the particle size of the PR-S fusion, and that -40-mesh granules of both 1: 1 and 2: 1 ratios of PR to S compared favorably with OSP as sources of P. Terman et al. (1964) granulated PR with both S and soil. Inclusions of S in the granules increased the relative effectiveness of granulated PR, and adding soil to the PR-S granules further increased the efficiency of the fertilizer. In no case, however, was the effectiveness more than 56% of that of soluble P (monocalcium phosphate). Additions of elemental S, in order to be economically feasible, should render the PR as effective as when acidulated with an equivalent amount of S as H2SO,. Although the acid is more expensive than elemental S, the acid’s effect on PR is relatively much greater. From an economic standpoint, therefore, the feasibility of PR-S mixtures is questionable. The effect of farmyard manure on PR dissolution was reviewed by Rogers et al. (1953). Although positive interaction of PR-manure mixtures on yields was found in some experiments, the effect is usually slight and within the range of experimental error. From a management point of view, crops that can effectively utilize PR can be used as green manure crops or as animal feed, and thus serve as indirect routes for mobilizing P from PR for subsequent crops that are less effective in their utilization of PR. IV. Agronomic Evaluation of Phosphate Rock for Direct Application

A. EVALUATION OF PR SOURCES

The fundamental principles and practices of comparative evaluation of fertilizer sources have been adequately discussed by several authors (Black and Scott, 1956; White et al., 1956; Terman et al., 1962; Terman and Engelstad, 1976). Source evaluation in these papers was developed along the principles of biological assay methods. The fertilizer sources being compared are assumed to contain differing dilutions of the same compound, and the biological response curves for all sources (yield response curves) are assumed to reach the same limiting value. The internal efficiency of the fertilizer nutrient is assumed to be the same for all sources also, so that, when yield is plotted against nutrient uptake, data points from all sources and all rates fall on a single line. These and other assumptions are discussed in more detail in the papers cited above. These three assumptions were singled out, however, for the purpose of reviewing how well they hold when we attempt to evaluate various sources of PR or when we compare PR with water-soluble sources such as CSP.

184

F. E. KHASAWNEH AND E. C. DOLL

In the first place, sources of PR differ not as a result of containing differing concentrations of the same compound, but because of fundamental chemical and mineralogical differences among their contents of francolite species. There are certain differences that can be attributed to the concentrations of accessory or diluent minerals (see Section II,B), but these differences are less important than the inherent differences among the apatites themselves. Furthermore, it is a common observation that yield maxima attained by increasing rates of PR vary among rock sources, and all are invariably less than the maximum that can be attained with a water-soluble source such as CSP (e.g., Ensminger et al., 1967; Engelstad et a l . , 1974). An example is shown in Fig. 4, with all sources wetscreened to -200+325-mesh size (F. E. Khasawneh, unpublished greenhouse data). Thus, the first two assumptions do not hold in the case of PR source evaluations. The third assumption appears to hold fairly well, as shown in Fig. 5 for the corn data of Fig. 4. Relative agronomic effectiveness (RAE) is usually the most useful parameter when we attempt to evaluate fertilizer sources. For linear response curves, RAE

60[

Maize

ABSOLUTE

- Greenhouse

CIT. SOL. INDEX TSP

NC

20

15 10 6

TN

MO

I

I

I

0

120

240

I

400 P ADDED, M G I P O T

I 960

FIG. 4. Response of maize to -35-mesh triple superphosphate (TSP) and six PR sources on an acid Mountview silt loam of pH 4.8 (1:l soil-water suspension). All PR sources were wet-screened to -200+325 mesh. NC = North Carolina, FL(N) = north Florida, FL(C) = central Florida, ID = Idaho, TN = Tennessee, and MO = Missouri.

185

PHOSPHATE ROCK IN SOILS

0

1‘

0

I

20

I 40

I 60

I 80

I 100

I 120

P UPTAKE. M G / P O T

FIG. 5 . Internal efficiency of P derived from TSP and six PR sources applied at four nonzero rates shown in Fig. 4.

is simply the ratio of the slopes of the rectilinear regression lines that describe experimental response. For Mitscherlich response curves, RAE is equal to the ratio of the computed availability coefficients. Concurrent linear and Mitscherlich models have been used for such computations (White et al., 1956; Engelstad, 1968; Engelstad and Khasawneh, 1969). A common limiting yield maximum is assumed for the Mitscherlich model. Yield response curves with CSP and with PR invariably do not share a common limiting yield (Fig. 4). It is not possible, therefore, to calculate a single RAE value for each source that would not be dependent on the rate used. Yet, in spite of these limitations, investigators might elect to sacrifice precision for the sake of simplicity or practicality. For example, Cooke (1956b) and Ensminger et al. (1967) calculated “superphosphate equivalents” (SPE) of P sources. This method consists of obtaining a complete yield response curve for the CSP standard, using single rates of the other P sources, and of finding (graphically) the rate of CSP that would have given the same yield response as the source being evaluated. The choice of the single rate (of PR, in this case) is purely arbitrary, but usually it has been a high rate, particularly one that is very close to the optimum rate. The rationale for choosing a high rate of PR is both simple and practical: (a) There is little added benefit from higher rates, and (b) the RAE of lower rates is of little interest to the farmer. A farmer is simply interested in

186

F. E. KHASAWNEH AND E. C. DOLL

knowing how much CSP he needs to give him the same yield response as that obtained from PR. Another alternative to the single rate method is to use average yield response for part of the yield curve or for the entire curve. When part of the yield curve is used, it is usually the steeply rising part before the curve begins to level off, and RAE is calculated from average yield responses or from concurrent linear models (Engelstad et al., 1974). The choice of the response surface is entirely arbitrary, and the resulting RAE values should be recognized and used as such. When economic analysis is included in the evaluation procedure, the relative economic effectiveness ( M E ) is calculated, but the process of comparative evaluation is not made easier. 0. P. Engelstad (personal communication, from a paper read in a workshop on PR for direct application held in Haifa, Israel, 1978) described two possibilities. In the first, emphasis is placed on maximizing net returns per hectare; in the second, per fertilizer dollar. In the first case, PR sources usually compare unfavorably with water-soluble sources, and there is a penalty in economic returns resulting from the lower yield potential of PR. In the second case, PR sources appear economically more profitable. This can be deceiving, however, for a farmer thinking primarily of his total annual income; if he elects to use PR, it may be necessary to farm larger acreages to make up for the loss of yield potential associated with PR. However, if his land holdings are small, or if the area under cultivation is limited to family labor, he will find himself restricted to a low annual income. Only use of machinery could increase the area in crop production. But whether machinery is purchased or leased, it represents larger cash inputs, which changes the entire basis of management from maximizing returns per fertilizer dollar to maximizing returns per unit area. The use of PR for direct application seems then restricted to marginal farms where funds are severely limited and risk aversion is of prime importance. The use of 32Pprovides yet another method for evaluating PR sources, both as freshly applied or as residual. For example, Ensminger et al. (1967) measuredA values for various rates of Florida PR using three southeastern soils in greenhouses pots. Their data (Table VI) show that the units of P from PR necessary to give an effect equal to 1 unit of P from OSP varied with soils, with rates of PR, and with liming. In field trials, the same authors reported that ladino clover yields were equivalent with PR at 600 pounds of P2Q per acre to one-fourth this rate as superphosphate (SP) on five soils, and to one-half or one-eighth this rate on two other soils. As will be shown later, agronomic effectiveness varies with the test crop also. It is obvious from the foregoing discussion that it would be futile to seek a single value that expresses the relative agronomic effectiveness of a given PR source, because no such parameter exists. Single-valued RAE numbers are appropriate only if the performance of the fertilizer is not affected by the fertilizer rate, by the soil, or by the crop. Phosphate rocks do not fit this description.

187

PHOSPHATE ROCK IN SOILS TABLE VI Relative Agronomic Effectiveness of PR on Three Soils by the A Value Method“ A values

PR

SP

Tagged Untagged

Wickham fsl Units of P from PWunit of P from SP Cecil Eutaw c. loam clay Unlimed Limed Cecil Eutaw Wickham, unlimed Ib p1205/acre

80 80 80 80 80 80 80 80

40 80

14

40 80 160 320 640

61 10 14 22 57 97

2 72 16 35 58 88 125

I94 233 -

182 172

-

-I 177 177 172 171

I97 202 264 269

-

_

.

-

4.7 4.4 4.5

-

-

2.5 2.1 2.5 3.3 4.6

27.0 20.0 4.6 8.5

“Data collated from Ensminger er al. (1967). ”Superphosphate, 20% p1205. cThese treatments were not included in the reported experiments.

Consequently, any RAE value must necessarily specify the rate, the soil, and the crop.

B. FACTORS AFFECTING AGRONOMIC EFFECTIVENESS OF PR

Discussions in preceding sections indicate that availability of the P in PR is influenced by ( a ) the inherent differences among PR sources, (b) the soil environment to which the PR was applied, and ( c ) the crop for which the PR fertilizer was used.

I . Reactivity of PR Failure to recognize differences among PR sources led to considerable confusion in early work about its fertilizer value. It is now recognized that differences among PR materials are largely explainable on the basis of chemical, crystallographic, and mineralogical composition of the PR concentrate (Sections I1 and In). Car0 and Hill (1956) probably were the first to call attention to the effects of “phosphate-bound carbonates” in PR on the availability of its P for crops. The term “phosphate-bound” was to distinguish this carbonate from accessory cal-

188

F. E. KHASAWNEH AND E. C. DOLL

cite, dolomite, or other alkaline earth carbonates. Crop response data (Armiger and Fried, 1957) were best correlated with bound carbonate and extractability in 2% citric acid (Caro and Hill, 1956). The carbonate was described as latticebound by the process of substitution of Cog- for PO!-. This thesis was further elucidated a decade later by Smith and Lehr (1966) and by the extensive research of the TVA group as discussed earlier (McClellan and Lehr, 1969; Lehr and McClellan, 1972). The relationship between isomorphic substitution in sedimentary apatites and such properties as crystal dimensions, crystallite size, extractability in citric acid or ammonium citrate, and a number of other physical and chemical properties is now well established. a . Measurement of PR Reactivity. A variety of procedures now exist for estimating reactivity of PR. Extensive data also exist for correlating crop response (to PR additions) with citrate solubility of P in PR. Consequently, citrate solubility has become a standard test with which all other laboratory test results are evaluated. Procedures used to measure PR reactivity include chemical extractants, x-ray diffraction methods, infrared (IR) procedures, specific surface, and elemental analysis. Chemical extractants, in addition to the official Association of Official Agricultural Chemists (AOAC, 1970) neutral normal ammonium citrate (NAC), include 2% formic acid (FmA), 2% citric acid (CtA), 1% lactic acid, Na-EDTA, and 32Pexchangeable P (Caro and Hill, 1956; Ensminger et a l . , 1967; McClellan and Gremillion, 1978). Solubility in NAC, CtA, and FmA have been extensively investigated by TVA researchers (Lehr and McClellan, 1972; McClellan and Gremillion, 1978). Some of the salient findings are listed below: (1) Accessory gypsum, calcite, or dolomite consumes a part of the NAC reagent, and the measured solubility is underestimated accordingly. This situation is easily remedied by routinely discarding the first extract and analyzing a subsequent extract of the same sample. (2) The presence of acid-soluble A1 as an accessory phase causes abnormally high P solubility in CtA, but depresses solubility in FmA and NAC. This is also remedied by discarding the first extract. (3) The quantity of P dissolved by NAC is insensitive to variation in PR grade. This can introduce a significant error for PR concentrates of different degrees of beneficiation. To illustrate, assume that we have two hypothetical concentrates, A and B, where A is beneficiated to 100% apatite, whereas B contains accessory silica and is only 80% apatite; otherwise the apatites are identical. Assume also that this particular apatite is 15% P. Extraction of 1 g of each material with NAC according to the AOAC procedure gives the same quantity of P from A as from B. Assume that this quantity is equal to 0.024 g of P. The conventional (also the

I89

PHOSPHATE ROCK IN SOILS

official) method of reporting these results would be to express NAC extractable P as a fraction of total P. Thus, we would report that 0.024/0.15 x 100 = 16% of the P in A is citrate-soluble, and that 0.024/(0.15 X 0.80) X 100 = 20% of the P in B is citrate-soluble. This artifact difference gives a falsely high reading for poor-grade materials, even though the apatite is the same in both cases. To avert this error, Lehr and McClellan (1972) proposed the absolute citrate solubility index (ACSI), for which the quantity of citrate-soluble P is expressed as a fraction of the P concentration of the apatite phase in the PR material rather than of the P concentration in the entire 1-g sample. In our hypothetical example, the apatite composition in either case is 15% P, and the ACSI is 16% in both cases. The definition of conventional citrate solubility and ACSI are as follows: Conventional citrate solubility

=

quantity of P extracted x 100 total P in the PR sample

AOAC citrate-soluble P,O, (g) = Percentage of P,O, in the apatite phase

x 10,000

(4) Solubilities in NAC, CtA, and FmA are all highly intercorrelated, and for a carefully selected population of 40 PR samples, these interrelations were ASI(CtA) = 1.26X ASI(FmA) = 2.42X

+ 7.29

where X is ACSI (McClellan and Gremillion, 1978). The x-ray diffraction procedure for estimating reactivity is predicated on the effect of substitution of COi- for PO!- and other related isomorphic substitutions on the a dimension of the apatite crystal, and also on the direct relationship between isomorphic substitution and citrate solubility. Again, a survey of a large number of PR deposits revealed the following relationships: ACSI ASI, CtA ASI, FmA

= = =

341(9.376 - a ) 429(9.393 - a ) 823(9.376 - a )

Thus, a measurement of the a parameter provides a quick method for estimating PR citrate solubility. It was described earlier that the a parameter also provides an estimate of carbonate, Na, Mg, and F substitution, thus giving a nearly complete descriptive characterization of the apatite phase in a sample. Although the other methods listed above (IR and specific surface area) give measurements that are also related to citrate solubility, the relationships are not as well defined nor as highly correlated as for the x-ray data, particularly because of the effects of accessory minerals on such measurements.

190

F. E. KHASAWNEH AND E. C. W L L

6. Particle Size Effects on Availability of P in PR. Because of the extremely low solubility of PR, it reacts with acid components of soil to release P only in the immediate vicinity of PR particles. Consequently, the greater the degree of contact between PR and soil, the better is crop utilization of P in PR. However, published data indicate that, for sizes C100 mesh (150 pm), the particle size effect is slight to nonexistent in greenhouse and field experiments. For materials coarser than 100 mesh, PR effectiveness declines with increasing particle size. In a series of laboratory and greenhouse studies with both bentonite-PR mixtures and soil-PR mixtures, Joos and Black (1950) reported that the order of decreasing effectiveness of PR was <400 mesh, a commercial grade (87% through 300 mesh), and 150-300 mesh. At pH levels ranging from about 4.5 to 7.0, relative differences in effectiveness of the various-sized PR decreased as the acidity increased in both the clay and the soil mixtures. All PR fractions were more effective as the acidity increased. Armiger and Fried (1958) compared different particle sizes of several of the PR ’s evaluated earlier for relative agronomic effectiveness (Armiger and Fried, 1957). Responses by alfalfa grown on three acid soils were consistently higher with -325-mesh than with - 100+ 150-mesh PR. These differences were smaller than differences among sources, and were even smaller in relation to yield response to P. In an extensive greenhouse pot study in Australia, Alston and Chin (1974) compared various size fractions of Florida and Christmas Island PR’s obtained by differential grinding as sources of P for subterranean clover. Monocalcium phosphate (MCP) produced higher yields than did the PR’s, even with four times as much P from PR. Clover yields (Table VII) with P applications of 11.4-137 mg of P per kilogram of soil increased with fineness of grinding. The favorable effect of finer grinding was less at high than at low P rates. Corn yield and P uptake in pot experiments (Table VIII) indicated no particle size effect among <100-mesh size separates of a highly reactive PR from North Carolina, and a relatively unreactive PR from Tennessee. The size fractions were separated by wet-sieving and by sedimentation for the finer size fractions. The clay size fraction of Tennessee (<2 p m ) appeared to be slightly more effective than the coarser fractions, but, even so, the cost of such fine grinding is prohibitive when measured against gain in effectiveness. Even this ultrafhe grinding was insufficient to make a reactive PR out of an unreactive one. Results from field experiments essentially lead to a similar conclusion. In long-term experiments conducted in Ohio, Salter and Barnes (1935) reported that changing from a coarse (60% through 100 mesh) to a more finely ground (97% through 100 mesh) Tennessee PR failed to show any increase in effectiveness. Rogers et al. (1953) reviewed field results obtained in the United States and concluded that, although finer particles occasionally gave somewhat higher yields than the “commercially ground material” that was readily available, this

191

PHOSPHATE ROCK IN SOILS

TABLE VII Dry Matter Yield of Subterranean Clover in the Greenhouse as Affected by Fineness of Grinding of Christmas Island Phosphate Rock"." Ground material passing through mesh listed (a) Treatment number

10

I 2 3 4 5

98 I00 100 100 100

35

100

Application of P (glpot)

325'

0.04

16 22 27 30 38

3.6 4.6 4.8 5.8 6.1

Fineness of grinding (4) 64 85 92 99 100

42 56 66 75 89

0.12

0.24

0.48

Dry matter yield (glpot)" 7.2 8. I 9.2 10.3 11.3

9.8 10.6 10.7 11.3 11.3

10.5 11.3 11.8 11.9 12.8

"Adapted from Alston and Chin (1974). "Phosphate was mixed with the top 10 cm of soil in each pot. "Equivalent mesh openings are 2, 0.5, 0.152, and 0.044 mm, respectively. dThe no-P pot had a dry matter yield of 0.6 glpot; LSD ( P = 0.05) = 1.5 glpot.

increased availability did not appear to be sufficiently great to merit grinding finer than was needed for about 90% of the material to pass a 100-mesh sieve. Cooke (1956a) summarized a number of field experiments conducted in the United Kingdom in which several sources of PR were compared. He concluded that there was no need for grinding PR more finely than required for 80-90% of the material to pass 100 mesh. In a later summary of over 90 experiments (Cooke and Widdowson, 1959), C300-mesh Gafsa PR was not consistently better than a coarser grade (5040% through < 100 mesh). These results were confirmed in 18 experiments in Wales and the West Midland Region of England (Jones, 1975). At first glance, one might expect substantial effects of particle size on the availability of P in PR; but only with rocks coarser than 100 mesh is particle size effect quite important. Bouldin and Sample (1959) showed that the availability of sparingly soluble P materials in soil was related to the geometric surface area of the fertilizer particles. However, subsequent work with dicalcium phosphate dihydrate (DCPD) indicated that particle size (and geometric surface area) effects leveled off for granules finer than -60 mesh (Bouldin ef al., 1960). The cutoff point for PR appears to be -100 mesh. In the case of PR, however, geometric surface area is only around 5% of total surface area because of the open porous structure of PR particles (Lehr and McClellan, 1972), which are actually loosely consolidated aggregates of much finer crystallites (Fig. 6). Therefore, effects of PR particle size should be interpreted in terms of an alternative hypothesis; Moreno (1959) suggested that the availability of slightly soluble phosphates was a function of the probability of a root contacting a granule, or the soil zone contiguous to and influenced by P fertilizer granules.

192

F. E. KHASAWNEH AND E. C. DOLL

TABLE VIII Effect of PR Particle Size on Dry Matter Yield and Uptake of P by Corn Tops" on Mountview Silt Loam Limed to pH 5.4 Particle size Mesh size" P source

ACSI"

North Carolina PR

19.8

Rate (mg P/pot)

-80+100

-100+200

150 300 600

40 57 72 56 a

55 76 94 75 b

150 300 600

14 16 18 16 a

14 17 19 16 a

42 66 76 61 a

54 80 104 79 bc

15 18 21 18 a

15 21 24 20 ab

x ,I

Tennessee PR

5.1

i

North Carolina PR

19.8

d

150

300 600

xd

Tennessee PR

5.1

150 300 600 id

Microns -200+325

2 0 4

Dry matter yield @/pot) 56 55 73 79 94 98 74 b 78b 14 16 20 17 a

15 19 20 18a

Uptake of P (mg/pot) 54 54 69 75 101 112 75 b 80bc

15 18 28 21 bc

17 24 28 23c

5-20

<2

52 77 103 78b

60 77 95 77b

14

19 24 37 26b

17 18 16a 52 86 113 83 c

56 86 110

16 20 24 20ab

84c 22 29 40 30d

"Average of three replicates; yield of the check treatment was 1 I .6 g/pot, and P uptake was 12 mg/pot. 'Absolute citrate solubility index. "Equivalent mesh openings are: 80 mesh = 177pm. 100 mesh = 149pm, 200 mesh = 7 4 p m , 325 mesh = 44 p m . "Means are compared only with respect to particle size effects; means in a row with different ietters are significantly different at the 5% probability level.

The foregoing discussion points out that grinding PR more finely than is required for 85-90% of the material to pass a 100-mesh siekc is probably not justified. Since extremely fine grinding does not materially alter the PR reactivity, a relatively unreactive source such as Virginia apatite, Missouri, and Tennessee brown PR cannot be converted into a more reactive form simply by fine grinding. The more-reactive sources, however, still need to be finely ground (at least to - 100 mesh) for maximum effectiveness. Particle size effects appear to become less important at high rates of application or in strongly acid soils.

PHOSPHATE ROCK IN SOILS

193

FIG. 6 . (A) A scanning electron micrograph of a PR aggregate from a noncalcined beneficiated concentrate from North Carolina (1OOOX). (B) A stereo photograph of one of the aggregates in A, showing details of its open porous structure (6200X); courtesy of J . R. Lehr and R. M. Scheib, Fundamental Research Branch, Division of Chemical Development, Tennessee Valley Authority.

194

F. E. KHASAWNEH AND E. C. DOLL

2. Soil Factors a. SoilpH. It has generally been recognized that agronomic effectiveness of PR is higher on acid soils than on neutral or alkaline soils (Peaslee et af., 1962; Ensmingeret af., 1967; Barnes and Kamprath, 1975). This relationship has been interpreted as a simple pH effect, in which acidity is the agent responsible for enhanced availability. As was shown earlier, francolite-type apatites are quite unstable at low pH levels, and they release P to react with A1 and Fe in the soil matrix and to form A1 and Fe compounds, which are more stable than apatites at lower pH levels. From a practical point of view, low soil pH develops along with other soil conditions that also affect PR dissolution, such as low exchangeable Ca and high exchangeable Al. The negative effect of excessive soil acidity on the growth of certain crops may override its positive effect on PR dissolution. It is necessary, therefore, to keep a proper perspective on the overall effect of soil acidity on crop response to PR. In field experiments of 2 to 5 years’ duration with PR on seven southeastern soils, liming did not significantly alter the relative effectiveness of PR (Ensminger et af., 1967). Amounts of P extracted by neutral NI&F were less from limed than from unlimed soils treated with equal rates of PR, indicating that liming curtailed reaction of PR with soil, yet P availability was not altered. Greenhouse experiments by Ellis et al. (1955) showed that liming decreased the availability of P in PR. When PR was applied one month prior to liming to pH 7, oat growth was better and P uptake was higher than when the order of application was reversed. Peaslee et al. (1962) also found that the availability of P in PR to sorghum grown on 19 soils decreased drastically with increasing soil pH, reaching nearly zero for soils with pH higher than 6.5. Ensminger et al. (1967) reported that on 13 of 19 soils ladino clover yields were similar with liming to 75% of the lime requirements or without lime. The effect of lime on response to PR was positive on three other soils and decidedly negative on three more soils. These results are not contradictory to the finding of others, but simply underscore the necessity of liming certain soils to obtain growth potentials that will allow response to PR to develop. b. Soil Ca. A soil’s affinity for Ca promotes the dissolution of PR because it provides a sink for the Ca that is released by the congruous dissolution of apatite. For fluorapatites, 10 moles of Ca dissolve for every 6 moles of P that go into solution. A low soil affinity for Ca increases the level of solution Ca at the apatite surface;consequently, the level of H,PO4-/HPO 3- declines according to the solubility product principle. The gradient of H,P04-/HPOi- between the apatite surface and the bulk soil solution declines also, and the process of PR dissolution is slowed accordingly (see Section III,A,3 and Eq. 6). Affinity of a soil for Ca is high when the Ca saturation percentage (fraction of

PHOSPHATE ROCK IN SOILS

I 95

the soil's exchange capacity saturated with Ca) is low; this condition usually occurs when the overall base saturation percentage and pH are low. The effect of Ca gradients on PR dissolution was investigated by Graham (1955) in systems of H-amberlite, H-bentonite, H-Putnam clay, and H-humus, and showed that weathering of P from PR was related to active CaZ+ and active H+ ions in the colloidal systems. More recently, the roles of soil H and soil Ca on PR effectiveness was investigated by Khasawneh (1977) in greenhouse experiments, with corn as the test crop. Mountview silt loam was limed to three levels with either CaCO, or SrCO, , and North Carolina PR was compared with CSP at three nonzero rates. Agronomic effectiveness was computed from the data (Table IX) for the intermediate rate (300 mg of P per pot), as shown in Fig. 7. Liming with equivalent amounts of either CaCO, or SrCO, increased the percentage of base saturation, and hence soil pH, by nearly equal increments. However, liming with CaCO, increased exchangeable Ca and decreased the soil's affinity for Ca. By contrast, liming with SrCO, did not increase exchangeable Ca even though it increased pH and base saturation. The soil's affinity for Ca, therefore, remained as high in SrC0,-limed soil as it was in the unlimed acid soil. The decrease in agronomic effectiveness of PR in the SrCQ-limed series was attributed to increasing soil pH; and the additional reduction in effectiveness with CaC03 was due to a decline in the soil's ability to provide an effective sink for Ca. Another factor closely related to soil pH and Ca is the soil cation exchange TABLE 1X Average Dry Matter Yield of Maize Tops Using Two P Sources, Two Liming Materials, and Three Lime Levels"

SKO,

CaCO, P source

Rate (mg P/pot)

I+,

L

4

L3

L

4

L3

dP0t PR*

150 300 600

64.0 86.5 111.4

62.8 89.9 114.6

40.4 65.3 87.2

16.4 20.6 22.2

57.1 81.3 114.0

56.7 76.3 105.5

38.6 55.1 72.7

CSP

150 300 600

49.5 83.1 118.1

67.8 98.9 127.0

64.3 105.0 127.3

57.1 90.4 131.0

64.0 88.0 120.8

64.6 100.7 127.9

58.1 96.1 117.3

0

9.6

12.7

9.9

8.2

9.9

9.2

8.5

No P

"Averages of three replicates; lime levels, L,, b,and L, represent additions to 18.32, and 60 meq of liming material per kilogram of soil. *North Carolina PR.

F. E. KHASAWNEH AND E. C. DOLL

196 I20

CORRESPONDING SOIL pH LEVELS 71 -

5:2 -

0

10

20

30

40

50

60

RATE OF C0C03 OR SrCO3, ms/kg SOIL

FTG. 7. Relative agronomic effectiveness of North Carolina PR, -200+325 mesh, with CSP (-35 mesh) set at 100 for corn on Mountview silt loam limed with equivalent rates of CaC03 or SrCO, at an equivalent P rate of 300 mg of P per pot.

capacity (CEC). Soils of the same pH may differ in their affinity for Ca because they differ in CEC. This may explain the differential effect of liming on PR effectiveness obtained by Ensminger et al. (1967). A vivid example of the interaction of soil pH and soil Ca on PR effectiveness as a source of P is the common observation that PR effectiveness for paddy rice is related to the initial preflood soil pH and not to the postflood soil pH, which usually is between pH 6 and 6.8 (Engelstad et al., 1974). The pH of acid soils rises sharply after flooding and reaches levels that are mostly related to the bases released by the reducing conditions, to the soil’s cation exchange capacity, and to the equilibrium in solution, which involves the CO%-/HC03-ions. In a series of greenhouse experiments, Khasawneh and Engelstad (1975) showed that PR was substantially more effective at preflood soil pH of 4.8 than at pH 6.0, even though the pH of both soils was above 6.0 after flooding. This effect was observed when PR was preincubated with the acid soil prior to flooding as well as when PR was added to the soil at the time of flooding without prior incubation. The effect may be explained on the basis of the soil’s affinity for Ca: Reducing conditions in flooded acid soil release Fe 2+ and Mn 2+, which become exchange-

PHOSPHATE ROCK IN SOILS

197

able cations, and thus raise the percentage of base saturation and soil pH. The Ca saturation, however, remains low at the elevated soil pH levels, and thus affinity of the flooded soil for Ca remains as high as for the initially acid soil. c. Soil P . The level of soil P, as expressed by the activity of H2P04- or by the phosphate potential, pH2P04 !hpCa, plays a role in PR dissolution analogous to that played by the level of soil Ca2+.The soil matrix should provide a positive gradient in the electrochemical potential of both Ca2+ and H2P04- to ensure the congruous dissolution of PR. If the soil is supersaturated with respect to the particular apatite in PR, the rock will neither dissolve nor significantly participate in supplying P to plant roots. From a practical point of view, moderately fertile soils with a relatively high soil solution concentration of P can derive little or no benefit from additions of PR. As an effective P fertilizer, PR is limited to soils that are severely to moderately deficient in P, but it has little or no value in soils of medium to high P status. d. Other Soil Fucrors. Additional soil factors include soil texture, soil organic matter, and placement methods. Texture indirectly incorporates effects of soil clays on CEC-pH relationships and on the ability of the soil to provide a sink for P. Light-textured soils and sands are not good sinks for P or Ca, and P may leach downward beyond the root zone. Under such conditions impaired solubility becomes an advantage, and PR’s are currently being evaluated for use in such situations, especially in forest stands ( G . W. Bengtson, Tennessee Valley Authority, personal communications). Effects of soil organic matter are probably twofold. The first is immediate and is related to bonding of Ca and providing an effective sink for Ca. The second effect is slow and indirect, since soil organic matter is a good index of the overall fertility status of mineral soils. Inorganic P released from PR can be incorporated into the organic pool of soil P, thus providing an indirect route of releasing P from PR from which plants obtain their requirement for P by mineralization. Placement effects are actually an extension of the particle size effects; hence PR placement should ensure thorough mixing in the rooting zone. It is no accident, therefore, that nearly all published reports on PR have used one method of PR application-namely , broadcasting of the finely ground material followed by incorporation. In greenhouse pot experiments, the method has been similarthorough mixing with soil. This method of placement is considered most appropriate, since it affords the widest distribution of PR in the upper rooting zone of the soil and permits the largest extent of contact between plant roots and PR particles. Placement methods that localize PR sources have been shown to limit their effectiveness (Terman er ul., 1964; Alston and Chin, 1974). Under field situations, broadcasting of ground PR is a rather dusty and difficult method of spreading. Dustiness is also exacerbated by preference for finer grinding. In addition, ground PR cannot be bulk-blended with other granular N and K fertilizers because of segregation problems. Two alternative approaches are cur-

+

198

F. E. KHASAWNEH AND E. C. DOLL

rently under investigation. The first, developed primarily by TVA, consists in formulating water suspensions of finely ground PR, which also may contain dissolved or suspended N and K fertilizers. Stable suspensions containing as much as 60% PR by weight have been made, and the technology appears to be quite simple and does not require complex equipment (Tennessee Valley Authority, 1976). The product has not been evaluated in field experiments, however, nor has the stability of suspensions been tested under varied handling and storage conditions. A second alternative to the handling and application of PR is by granulating finely ground PR with a water-soluble salt binder, so that the granule will slake down to fine particles when wetted. This concept has been pursued vigorously by a few companies, and such products are already on the international market. However, there is no information on the agronomic performance of such granular PR except for test data by proprietory companies. Granulation of PR has been shown repeatedly to be counterproductive for raw crops if the granule size is as large as the accepted size range for water-soluble fertilizers (-6+ 14 mesh). Granulation of <200- or <300-mesh PR into so-called minigranules,
3 . Plant Factors Truog (19 16) was probably the first to recognize that crops vary greatly in their ability to utilize P from PR under different soil conditions. He attributed this variability to differences in crop demand for Ca. Cook (1935) compared oats, corn, millet, and buckwheat grown in sand culture enriched with PR and containing bentonite or soil organic matter saturated with either H or Ca. He reported that oats, corn, and millet used PR effectively only in the presence of H-saturated bentonite or organic matter, while buckwheat utilized P in the presence of either H- or Ca-saturated exchange material. Experiments by Fried and MacKenzie (1949) and by Murdock and Seay (1955) with neutron-irradiated PR confirmed differences among crops in their ability to derive P and Ca from PR. For example, the latter authors reported 23-30% of the P in red clover but only 13-15% of the P in wheat to be derived from PR. The 32P/45Caratio ranged from 3.3 to 4.4 in wheat and from 1.1 to 1.9 in red clover in soils treated with PR. Thus, clover not only derived a high proportion of its P from PR, but also derived a higher proportion of its Ca from PR. Differences among crops must be related to their demand patterns for both Ca

PHOSPHATE ROCK IN SOILS

199

and P, and to how these demand patterns alter the composition of the soil solution at the root-soil interface. Cooke (1956a) postulated that crops with well-developed fibrous roots are best suited to utilize P from PR. In an extensive series of greenhouse experiments, he reported that a PR from Morocco was equivalent to SP for radishes, about half as equivalent for swedes, rape, and buckwheat, and of little value for mustard, clover, ryegrass, timothy, wheat, barley, rye, and lettuce. Additional listings were given by Dean and Fried (1953) and by Rogers et al. (1953); lupins, buckwheat, clover, mustard, Swiss chard, rape, and cabbage were listed as efficient users of PR, whereas cotton, cowpeas, and most cereals were listed as inefficient. Perhaps the unifying parameter in PR utilization is the relative growth rate of a plant species and its direct effect on setting the demand patterns for both Ca and P. Fast-growing plants will need a high rate of accumulation of P within the plant to maintain this growth rate. If the plant has an extensive root system, then the P demand per unit length of root is less than for a root system of limited length and extensity. Again, for a given level of P intake per unit length of root, the concentration of P in solution needs to be above a certain value, which is determined by the kinetics of P uptake for that particular species. If the PR cannot maintain such a concentration in solution, then the rate of P absorption per unit of root will decline, and the relative growth rate will decline accordingly. In a series of greenhouse experiments, F. E. Khasawneh (unpublished data) measured the relative growth rate of corn grown on a Mountview silt loam fertilized with three rates of four PR’s and powdered DCPA (dicalcium phosphate, anhydrous). Results indicated that the relative growth rate of corn was related to the concentration of P that these sources could maintain in soil, and all the data points for all sources and rates could be described by a single curvilinear relationship (Fig. 8). The extensity of root elongation as a factor in P nutrition has been confirmed by Khasawneh and Copeland (1973) and by Newman and Andrews (1973). Different crop species have different rooting habits, which are largely genetically determined, but which also can be significantly altered by subsoil acidity, subsoil compactness, drainage, and pathological agents. Mycorrhizal associations are yet another aspect of how the extensity of root ramification into the soil can be altered in such a way as to avail the root system of a larger probability of contacting or being physically close to a PR particle so that it can derive more of its P from PR. Tinker (1975) examined this possibility and concluded that mycorrhizal associations alone cannot explain differences among crops in their ability to use PR. It is more likely, therefore, that all the factors enumerated above contribute to these differences. Whatever the cause@), crops do vary in their ability to utilize PR, and these differences contribute to their relative agronomic effectiveness. In summation, it should be emphasized that a given PR does not have a unique

F. E. KHASAWNEH AND E. C. DOLL

200 0.20

5

-

0.15 -

P

? C

zm

0.10 -

o DCPA 0 TENNESSEE D CENTRAL FLORIDA I NORTH CAROLINA A EL-HASA(JOR0AN) A CHECK

W

2

5

OD5

-

(L W

I

01 0

PR PR PR

PR.

A I 10

I 20

I

30

I 40

I

50

I 60

I

70

I

80

P CONCENTRATION IN I:I SOIL-WATER EXTRACTS.ppb

FIG. 8. Relative growth rate of corn grown on Mountview silt loam fertilizer with three nonzero rates of DCPA and of PR from four sources as a function of the P concentration that these P sources were able to maintain in the soil.

relative agronomic effectiveness associated with it, but it does possess a unique reactivity, which can be measured in a variety of ways. The relative agronomic effectiveness of a PR depends on three distinctly independent sets of factors: (a) the inherent reactivity of the rock, (6) the soil factors, and (c) the plant factors. The interaction of these sets of factors may result in a reactive PR’s being nearly as effective as SP, or in its being nearly inert.

C. RESIDUAL EFFECTS OF PR

The preceding discussion concerning agronomic effectiveness of PR has dealt mainly with its initial effectiveness. However, as was presented in the discussion of PR dissolution in soils, PR has been shown to persist in some soils for at least 40 years. Therefore, the residual effects of PR are of considerable practical interest. In an experiment with rice in Thailand, Engelstad er al. (1974) evaluated the residual effects of various rates of both CSP and several sources of PR applied to rice by growing a second crop of rice without added P, except that CSP was applied to an extra set of check plots for the second crop to provide a comparison with fresh application. They concluded that (a) the general superiority of CSP (fresh and residual) over all sources of PR persisted through the second crop; (6) a relationship between citrate solubility of P in PR and crop 1 response was

PHOSPHATE ROCK IN SOILS

20 1

largely obscured for crop 2; and ( c ) the residual effects of most PR’s were substantial (Missouri PR was ineffective both initially and residually). Hammond (1977) conducted a similar experiment with field beans in Colombia. Yields of the second crop of beans (grown to evaluate the residual effects of CSP and PR applied to the first crop) showed a marked residual response to all PR’s, but an even greater residual effect of CSP at the same rate of P. Citrate solubility of P in PR was related to yields of both bean crops, but relative differences were smaller for crop 2 than for crop 1. Doll et al. (1960) compared initial applications of PR and OSP in a 3-year rotation of corn, wheat, and hay. Initially, higher yields were obtained with CSP, but yields of the second wheat crop (fifth cropping year) were higher with PR applied to supply twice as much P as in CSP. Ensminger et al. (1967) summarized a number of regional experiments in southeastern United States and concluded that residual effects of PR were less or no better than that of half as much P from OSP. In Australia, sorghum was grown for 7 years on plots (pH 6.5) that received various initial rates of OSP and PR. Initially, OSP was more effective than PR, but after 7 years the residual value of OSP was only 8% of the initial value, as compared with 60-70% of that for PR (Amdt and McIntyre, 1963). Ensminger and Pearson (1 957) used 32Pto determine A values in field experiments in which OSP and PR had been applied for 15 years in Alabama and then discontinued for 5 years. On a Greenville ffne sandy loam (pH 5.6-6.1), OSP had a greater residual value than PR applied at twice the rate of P. On Decatur silt loam (pH 5.4-5.6), PR and OSP applied at the same rate of P had about the same residual availability. In similar experiments in Iowa, to which PR had been applied to soils of pH 5.7-6.3 for 8-39 years, Webb and Pesek (1954) reported that the residual effects of PR were less than those of OSP when PR was applied at equal or higher rates of P. On a soil testing pH 8.0, PR was an ineffective source of P. In Minnesota, Caldwell et al. (1956) noted very little residual availability of PR applied to a soil at pH 6.0. In rotation experiments conducted over a 30-year period in Ohio, Salter and Barnes (1935) reported that the efficiency of PR was about 40% of that of OSP on unlimed plots for grain crops and clover. On limed plots, the efficiency of PR dropped below 10%. In Arkansas, twice as much P from PR as from OSP was applied for corn, oats, and hay grown in rotation over a 30-year period (McLean et al., 1952). After 10 years, corn yields were about equal for OSP and PR, but wheat yields with PR were less for most of the 30 years. The annual yields of the three crops were about equal on OSP and PR plots after 30 years. Doll et al. (1960) reported the results of two rotation experiments in Kentucky conducted for 39 and 45 years on which four and three times as much P had been applied as PR, as was applied as OSP. At the conclusion of the experiment, corn yields were higher with PR, but wheat yields were higher with OSP. In several early

202

F. E. KHASAWNEH AND E. C. DOLL

long-time rotation experiments summarized by Rogers et al. (1953), PR and SP were each usually compared at only one rate, with PR applied at the same weight of P as OSP, or more frequently, in an amount estimated to be equal in value to the amount of OSP applied. Thus, from two to four times,as much P was usually applied as PR. At the same time, rates of fertilizer used were low, and yields of all crops were much lower than those currently being produced. Therefore, these old experiments give valuable information concerning the relative persistence of PR in soils, but little or no information on the relative effectiveness of PR for the production of maximum, or near maximum, yields. It has commonly been assumed that the residual effects of PR are greater than those of soluble P fertilizers; however, the results presented here do not confirm this assumption. Results indicate that PR will persist for long periods of time, as would be expected fro,m dissolution of PR, discussed in Section II1,A. It appears that the residual effects of soluble P fertilizers are greater than those from PR in the first 3 or 4 years after application when equal amounts of P are applied. However, it should also be noted that less than optimum yields were obtained in most of these experiments.

D. PARTIALLY ACIDULATED PR

A considerable number of investigations, largely in greenhouse pots, have been conducted in which PR has been partially acidulated by the use of various acids before being applied to the soil, or in which varying amounts of SP have been granulated with PR. In Ohio, McLean and his co-workers have obtained generally favorable results with partially acidulated, fine PR (PAPR). McLean and Wheeler (1964) and McLean et al. (1965) reported that PAPR of 10-20% partial acidulation was equal to 100% acidulated PR for corn seedlings and alfalfa in growth chamber experiments. In field experiments in Ohio, in which significant yield responses to P were obtained, McLean and Logan (1970) concluded that yields with fine 20% acidulated PR were higher than or equal to yields with 100% acidulated PR (superphosphate) in 46 of 53 experiments. They attributed the effectiveness of the 20% acidulated materials to the relatively high P fixation tendencies and the high levels of exchangeable aluminum in their Ohio soils. McLean and Ssali (1977) used partially acidulated PR in a greenhouse experiment with millet and alfalfa on two Oxisols from Uganda and an oxidic Ultisol from Tennessee. Yields obtained with CSP were higher than those obtained with 20% acidulated PR for both crops and on all three soils. They stated that the results obtained with the more highly weathered Uganda and Tennessee soils were different from those previously obtained with Ohio soils, and attributed the different behavior to the lower levels of exchangeable aluminum in the more highly weathered soils.

PHOSPHATE ROCK IN SOILS

203

A series of greenhouse experiments was conducted at TVA using granulated materials prepared either by partially acidulating PR or by granulating mixtures of PR and OSP. Terman er al. (1964) reported that relative yields with 25% and 50% acidulated materials were approximately 25% and 50% of the yields obtained with OSP. Relative yields with granular PR were very little better than those with no P. Additional greenhouse experiments with corn were conducted by Terman and Allen (1967) to evaluate the effectiveness of PR acidulated to varying degrees with &Po4 or mixed with CSP or OSP. Effectiveness of P in the granular fertilizers was closely related to their content of water-soluble P. The authors stated that economies resulting from the use of underacidulated PR could be approximated by using reduced rates of SP. Similar results were obtained by Ashby et al. (1966), but there was little difference between 50% and 100% acidulation levels. Total P recovery was highly correlated with the percentage of available P in the fertilizer. Mixing the granules with the soil gave higher yields and P uptake than band placement. Misra and Panda (1969) and Panda and Misra (1970) reported satisfactory results in pot experiments when PR was 50% acidulated at soil pH above 5.6. Products acidulated with &Po4 were superior to those acidulated with HNO,, probably because of the higher water solubility of P with H3P04. In Virginia, Lutz (1971, 1973) conducted field experiments in which 20% acidulated PR (with H3Po4) was compared with CSP as sources of P for corn, alfalfa, and orchardgrass; their results are in agreement with the greenhouse results of Terman and Allen (1967). Published reports relative to the effectiveness of PAPR are thus conflicting. Most of the differences in results can be attributed to differences in the form of PAPR used (powdered versus granulated), to differences in acids used for acidulation, to differences in responsiveness of soils used for testing the fertilizer, and to differences in rate of P application. The method of adding the acid to the PR and subsequent aging determines the chemical nature of the acidulated material. A 100% acidulation yields monocalcium phosphates, whereas lesser acidulation may result in mono- and dicalcium phosphate phases that are either well distributed or in small pockets, depending on the method of mixing and handling of the mixture. The dicalcium phosphate phase is as effective as the monocalcium phosphate when in powdered form, and its effectiveness declines with granulation (Bouldin et al., 1960). Partially acidulated PR is usually superior to unacidulated PR; but partial acidulation does not seem to increase the effectiveness of the unacidulated portion of the PR. Murdock and Seay (1955) concluded in a greenhouse experiment that small amounts of OSP applied with relatively large amounts of PR increased the uptake of P from PR, but that larger amounts of OSP tended to decrease the uptake of P from PR. This underscores the important effects of P rates on such comparisons. At low rates, the results of Murdock and Seay are in agreement with the results of McLean and his co-workers in Ohio. At

204

F. E. KHASAWNEH AND E. C. DOLL

high rates, however, their results agree with those of Terman and his associates. It has been proposed that a small amount of soluble P on a severely P-deficient soil will stimulate root growth and allow the plant to utilize applied PR more effectively. However, unpublished results by Carlos Valverde and his coworkers in Peru (La Molina Agricultural Experiment Station, Lima, Peru, personal communication) do not substantiate this view. Low rates of banded SP superimposed on various rates of broadcast PR did not increase the utilization of P from PR by potatoes, although there was a slight tendency to increase PR effectiveness at low rates of PR. The available data indicate that there are situations where partially acidulated PR may be an effective P fertilizer, but there are other situations where an amount of SP equivalent to the available (citrate-soluble) portion of the partially acidulated PR may be just as effective and even more economical. This is an area where more field research may be needed. REFERENCES Alston, A. M., and Chin, K. W. 1974. Aust. J. Exp. Agric. Anim. Husb. 14, 649-655. Amberger, A., Sommer, G., and Gutser, R. 1971. Landwirtsch. Forsch. 24, 260-271. Anonymous. 1973. Phosphorus Potassium 18, 19-23. Armiger, W. H., and Fried, M. 1957. Soil Sci. SOC.Am., Proc. 21, 183-188. Armiger, W. H., and Fried, M. 1958.1. Agric. Food Chem. 6, 539-543. Amdt, W., and Mclntyre, G. A. 1963. Aust. J. Agric. Res. 14, 785-195. Ashby, D. L . , Fenster, W. E., and Attoe, 0. S. 1966. Agron. J. 58, 621-625. Association of Official Agricultural Chemists. 1970. “Official Methods of Analysis,” 1 Ith ed., p. 15. AOAC, Washington, DC. Barnes, J. S., and Kamprath, E. J. 1975. N.C.. Agric. Exp. Stn., Tech. Bull. 229. Black, C. A., and Scott, C. 0. 1956. SoilSci. Soc. Am., Proc. 20, 176-179. Bouldin, D. R., and Sample, E. C. 1959. Soil Sci. Soc. Am., Proc. 23, 276-281. Bouldin, D. R., DeMent, J. D., and Sample, E. C. 1960. J. Agric. Food Chem. 8, 470-474. Bray, R. H., and Kurtz, L. T. 1945. Soil Sci. 59, 39-45. Caldwell, A. C., Hustrulid, A., and Hammers, F. L. 1956. Soil Sci. Soc. Am., Proc. 20, 25-28. Caro, J . H., and Hill, W. L. 1956. J. Agric. Food Chem. 4, 684-687. Cathcart, J . B. 1979. In “The Role of Phosphorus in Agriculture” (F. E. Khasawneh, E. C. Sample, and E. J. Kamprath, eds.), Chapter 2. Soil Sci. SOC.Am., Madison, Wisconsin (in press). Cescas, M. P., and Tyner, E. H. 1976. Ann. Agron. 27, 891-924. Chang, S. C., and Jackson, M. L. 1957. Soil Sci. 84, 133-144. Chaveni, J . G., and Black, C. A. 1966. Iowa State J . Sci. 41(1), 77-95. Chien, S. H . 1977a. Soil Sci. 123, 117-121. Chien, S. H. 1977b. Soil Sci. Soc. Am. J . 41, 656-657. Chien, S. H . , and Black, C. A. 1976. SoilSci. SOC.Am. J. 40, 234-239. Chu, C. R., Moschler, W. W., and Thomas, G. W. 1962. Soil Sci. Soc. Am., Proc. 26, 476-478. Cook, R. L. 1935. J. Am. Soc. Agron. 27, 297-311. Cooke, G. W . 1956a. Emp. J . Exp. Agric. 24, 295-306. Cooke, G. W. 1956b. J. Agric. Sci. 48, 74-103. Cooke, G. W., and Widdowson, F. V. 1959. J . Agric. Sci. 53, 46-63.

’

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205

Dean, L. A,, and Fried, M. 1953. In “Soil and Fertilizer Phosphorus in Crop Nutrition” (W. H. Pierre and A. G. Norman eds.), Vol. 4, pp. 189-242. Academic Press, New York. Doll, E. C., Miller, H. F., and Freeman, J. R. 1960. Agron. J. 52, 247-250. Ellis, R., Jr., Quader, M. A., and Truog, E. 1955. Soil Sci. SOC. Am., Proc. 19, 484-487. Elphick, B. L. 1955. N . 2. J . Sci. Technol., Sect. A 37, 156-173. Engelstad, 0.P. 1968. Agron. J. 60, 327-329. Engelstad, 0. P., and Khasawneh, F. E. 1969. Agron. J. 61, 473-474. Engelstad, 0.P., Jugsujinda, A., and DeDatta, S. K. 1974. Soil Sci. SOC.Am., Proc. 38, 524-529. Ensminger, L. E., and Pearson, R. W. 1957. Soil Sci. SOC. Am., Proc. 21, 80-84. Ensminger, L. E., Pearson, R. W., and Armiger, W. H. 1967. U.S., Dep. Agric. ARS 41-125. Farr, T. D., and Elmore, K. L. 1962. J. Phys. Chem. 66, 315-318. Food and Agriculture Organization. 1973. “Annual Fertilizer Review. ” FAO, Rome. Food and Agriculture Organization. 1975. “Annual Fertilizer Review. ” FAO, Rome. Fried, M.. and MacKenzie, A. J . 1949. Soil Sci. SOC.Am. Proc. 14, 266-231. Graham, E. R. 1955. Soil Sci. SOC.Am., Proc. 19, 26-29. Hammond, L. L. 1977. Ph.D. Thesis, Michigan State University, East Lansing. Howe, D. O., and Graham, E. R. 1957. Soil Sci. SOC. Am., Proc. 21, 25-28. Jones, E. 1975. J. Soil Sci. 26, 66-73. Joos, L. L . , and Black, C. A. 1950. Soil Sci. SOC. Am., Proc. 15, 69-75. Jurinak, J. J . , Whitmore, J . C., and Wagenet, R. J . 1977. Soil Sci. SOC. Am. J. 41, 721-724. Khasawneh, F. E. 1977. Agric. Conf. Muslim Sci., I s t , 1977. Khasawneh, F. E. 1978. Soil Sci. 126 (in press). Khasawneh, F. E., and Copeland, J . P. 1973. Soil Sci. SOC. Am., Proc. 37, 250-254. Khasawneh, F. E., and Engelstad, 0. P. 1975. Annu. Meet., South. Br. Am. SOC. Agron., 1975. Kittams, H. A,, and Attoe, 0. S. 1965. Agron. J . 57, 331-334. LeGeros, R. Z . , Trautz, 0. R.,LeGeros, J . P., Klein, E., and Shirra, W. P. 1967. Science 155, 1409-141 I . Lehr, J . R. 1967. Proc. 17rh Annu. Meet. Fert. lnd. Round Table pp. 61-67. Lehr, J. R., and Hoare, J . 1979. In “The Role of Phosphorus in Agriculture” (F. E. Khasawneh, and E. C. Sample, E. J. Kamprath, eds.), Chapter 4. Soil Sci. SOC.Am., Madison, Wisconsin (in press). Lehr, J. R., and McClellan, G. H. 1972. Natl. Fert. Dev. Cent.. Bull. Y-43. TVA, Muscle Shoals, Ala. Lindsay, W. L., and Vlek, P. L. G. 1977. I n “Minerals in Soil Environments” (J. B. Dixon and S. B. Weed, eds.), Chapter 17, pp. 639-672. Soil Sci. SOC.Am., Madison, Wisconsin. Lipman, J. G., and McClean, H. C. 1918. Soil Sci. 5, 243-250. Lipman, J. G., McLean, H. C., and Lent, H. C. 1916. Soil Sci. 2, 499-538. Lipman, J. G., Blair, A. W., Martin, W. H., and Beckwith, C. S. 1921. Soil Sci. 11, 87-92. Lutz, J . A. 1971. Agron. J. 63, 919-922. Lutz, J . A. 1973. Agron. J. 65, 286-289. McCann, H. G. 1968. Arch. Oral Biol. 13, 987-1001. McLean, E. 0.. and Logan, T . S. 1970. Soil Sci. SOC.Am., Proc. 34, 907-91 1. McLean, E. 0.. and Ssali, H. 1977. Soil Sci. 123, 155-164. McLean, E. O., and Wheeler, R. W. 1964. Soil Sci. SOC. Am., Proc. 28, 545-550. McLean E. O., Brown, D. A,, and Hawkins, C. A. 1952. Arkansas, Agric. Exp. Sm., Bull. 528. McLean, E. O.,Wheeler, R. W., and Watson, J. D. 1965. SoilSci. SOC. Am., Proc. 29, 625-628. McClellan, G. H., and Gremillion, L. R. 1979. In “The Role of Phosphorus in Agriculture” (F. E. Khasawneh, E. C. Sample, and E. J . Kamprath, eds.), Chapter 3. Soil Sci. SOC.Am., Madison, Wisconsin (in press). McClellan, G. H.,and Lehr. J. R. 1969. Am. Mineral. 54, 1374-1391. Mattingly, G. E. G. 1968. J. Agric. Sci. 70, 139-156.

206

F. E. KHASAWNEH AND E. C. DOLL

Mattingly, G. E. G. 1970. J. Agric. Sci. 75, 413418. Misra, V. K., and Panda, N. 1969. Indian J. Agric. Sci. 39, 353-361. Moreno, E. C. 1959. Soil Sci. Soc. Am., Proc. 23, 326-327. Murdock, J. T., and Seay, W. A. 1955. Soil Sci. SOC.Am., Proc. 19, 199-203. Neller, J . R. 1956. Soil Sci. 82, 129-134. Neller, J. R., and Bartlett, F. D. 1959. Soil Sci. 88, 331-335. Newman, E. I . , and Andrews, R. E. 1973. Plant Soil 38, 49-69. Nimgade, N. M. 1969. Trans. In!. Congr. Soil Sci.. 9th. 1968 Vol. 2, pp. 765-774. Notholt, A. J. G. 1974. Proc. Ind. Miner. Int. Congr., 1st. 1974 pp. 104-120. Olsen, R. A. 1975. Soil Sci. Soc. Am., Proc. 39, 634-639. Olsen, S. R. 1952. J. Phys. Chem. 56, 630-632. Olsen, S. R., Cole, C. V., Watanabe, F. S., and Dean, L. A. 1954. U . S . , Dep. Agric., Circ. 939. Panda, N., and Misra, V. K. 1970. Plant Soil 33, 225-234. Peaslee, D. E., Anderson, C. A., Burns, G. R., and Black, C. A. 1962. SoilSci. Soc. Am., Proc. 26, 566-570. Peterson, G. W., and Corey, R. B. 1966. Soil Sci. Soc. Am., Proc. 30, 563-565. Robertson, W. K.. Thompson, L. G., Jr., and Hutton. C. E. 1966. Soil Sci. Sor. Am., Proc. 30, 446450.

Rogers, H. T., Pearson. R. W., and Ensminger, L. E. 1953. In “Soil and Fertilizer Phosphorus in Crop Nutrition” (W. H. Pierre and A. G. Norman, eds.) Vol. 4, pp. 189-242. Academic Press, New York. Russell, E. W. 1973. “Soil Conditions and Plant Growth,” loth ed., pp. 587-588. Longman Group, Ltd., London. Salter, R. M., and Barnes, E. E. 1935. Ohio, Agric. Exp. Sin.. Bull. 553. Shapiro, R. E., and Armiger, W. H. 1958. J. Agric. Food Chem. 6, 453455. Smith, F. W., and Grava, J. 1958. Soil Sci. 86, 313-318. Smith, J. P., and Lehr, J. R. 1966. J. Agric. Food Chem. 14, 342-349. Swartzendruber, D., and Barber, S . A. 1965. Soil Sci. 100, 287-291. Tennessee Valley Authority. 1976. “New Developments in Fertilizer Technology,’’ I Ith Demonstration, Natl. Fert. Dev. Cent., Bull. Y-107,pp. 70-74. TVA, Muscle Shoals, Ala. Terman, G. L., and Allen, S. E. 1967. J . Agric. Food Chem. 15, 354-358. Terman, G. L., and Engelstad, 0. P. 1976. Natl. Fert. Dev. Cent., Bull. Y-21. TVA, Muscle Shoals, Ala. Terman, G. L. Bouldin, D. R., and Webb, J. R. 1962. Adv. Agron. 14, 265-319. Terman, G. L., Moreno, E. C., and Osborn, G. 1964. Soil Sci. Soc. Am., Proc. 28, 104-107. Terman, G. L., Kilmer, V. J., and Allen, S. E. 1969. Fert. News 14, 4 1 4 5 . Tinker, P. B. 1975. In “Endomycorrhizas” (F. E. Sanders, B. Mosse, and P. B. Tinker, eds.), pp. 353-371. Academic Press, New York. Truog, E. 1916. Wis.,Agric. Exp. Sin., Res. Bull. 41. Volk, G. W. 1944. J. Am. Soc. Agron. 36, 46-56. Waksman, S. A., and Joffe, J. S. 1922. J . Biol. Chem. 50, 35-45. Webb, J . R., and Pesek, J. T. 1954. Soil Sci. SOC.Am., Proc. 18, 448453. White, R. F., Kempthorne, O., Black, C. A., and Webb, J. R. 1956. SoilSci. SOC.Am., Proc. 20, 179-186.

ADVANCES IN AGRONOMY, VOL. 30

PRODUCTION OF SOLASODINE FOR THE PHARMACEUTICAL INDUSTRY Jay D. Mann Applied Biochemistry Division, Department of Scientific a n d Industrial Research, Lincoln, New Zealand

1. Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. Solasodine-Containing Species of Solanurn .........................

111.

IV.

V.

VI.

A. Poroporo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0. Solanuin khasiunuin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Other Potentially Useful Species ....................................... Chemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Biochemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Biosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Turnover . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Degradative Pathways Isolation and Determination A. Extraction. . . . . . . . . . . . . . B. Assay . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Agronomy of Poroporo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Seed Germination .......................... ...... B. Soil Preparation, Planping Distances, Etc. ................................ C. Growth of Poroporo .................................. D. Harvesting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

........... ..................... VII. VIII.

...................... ....................................... .................................................

207 209 209 215 216 217 22 1 22 I 224 225 226 226 228 229 230 23 1 233 235 236 231 238 240 240

I. Perspective

Diosgenin is the most important source of raw material for the synthesis of steroid drugs (Applezweig, 1962, 1969). Supplies of diosgenin are ultimately limited (Martin, 1972), although recent fluctuations in supply have had social and political rather than agricultural causes. A search for alternative raw materials has been motivated by various reasons, including the aforementioned restrictions of diosgenin supply, unwillingness to rely solely on one supplier, and in many cases a desire to use internal production to conserve foreign exchange. Solasodine, which is chemically very close to diosgenin, can effectively serve as a replacement for that material. In the first 207 Copyright @ 1978 by Academic Press. Inc. All rights of reproduction in any form reserved.

ISBN 0-12-wO730-4

208

JAY D.

MA"

section of this chapter an attempt is made to survey the economic aspects of production of steroid raw material, including alternative sources of supply. Production of steroid drugs is a large-scale industry (Applezweig, 1962, 1969). In 1967, total world consumption of steroid precursors was loo0 tons, two-thirds of which came from diosgenin, and the remaining one-third from a variety of miscellaneous sources. The latter included plant products such as solasodine, yamogenin, hecogenin, and stigmasterol; animal products such as bile acids; and a small amount made by total synthesis from simpler organic chemicals. The cost of diosgenin and its substitutes has fluctuated widely in recent years, largely because of difficulties in the Mexican supply of diosgenin. The dried yam root (barbasco) rose in price from 24 cents per kilogram before 1975 to $5.60 in 1976 (Anonymous, 1977). At a concentration in the root of about 5%, this corresponds to a price ranging between $5 and $1 12 per kilogram in siru. Extraction costs have to be added on to these figures: In 1969 purified diosgenin cost approximately $16 per kilogram (Applezweig, 1969). The latest price for barbasco is $2.66 per kilogram, corresponding to more than $50 per kilogram of unextracted diosgenin. The high prices for Mexican diosgenin have had rather little effect on the selling prices of the greatly modified chemicals ultimately sold to the consumer. The costs of drug production arise mostly from the cost of equipment, research, and registration; the raw material expenses are relatively minor. Diosgenin was the first raw material source to be used for high-volume production (Djerassi, 1966), because it was available in a readily purified form and at sufficiently high concentrations in a tuber that was cheaply collected rather than cultivated. This led to a very low price for diosgenin. As that price has now increased, alternative steroid sources have become competitive (Anonymous, 1977). Solasodine is one such alternative. Two other steroidal alkaloids that could become available in large quantities are tomatidine and solanidine, from wastes of tomato and potato growing, respectively. Unfortunately, neither of these materials is well suited to chemical conversion to steroid drugs, although an enzymatic conversion of tomatidine to allopregnenolone has been described (Heftmann and Schwimmer, 1972). Hecogenin, a by-product from sisal hemp production, and stigmasterol from vegetable oils have been used as commercial precursors. Hecogenin has been in limited supply, but forthcoming Brazilian production of paper from sisal may make large quantities available in two years (Anonymous, 1977). Cholesterol from wool grease and sitosterol from soy oil have been used to make diuretic and contraceptive drugs by microbiological fermentation; these processes have been so successful that diosgenin may no longer be required for this portion of the market (Anonymous, 1977). It is not widely recognized that antifertility drugs do not constitute the main end use of steroid drugs. Only 5% of total steroid production goes into fertility control drugs; however, these have a disproportionately high unit value, so that

PRODUCTION OF SOLASODINE

209

such sales amount to roughly 25% of steroid sales. The' greater portion of steroid drug production, 95%, is aimed at lower-cost corticosteroids, which are used in the treatment of arthritis, skin inflammation, etc. To raw material producers, this pattern of utilization is important because it suggests that changes in the use of steroid contraceptives will have no particular impact on the continued need for steroid precursors. Solasodine, as a nitrogen analogue of diosgenin, seems to be in a strong competitive position with diosgenin itself. Indeed, solasodine derived from Solanum laciniaturn is reported to be the sole source of cortisone and progesterone in the USSR (Alekseenko et al., 1976b; but cf. Applezweig, 1969). In India, S. khasianum and certain other species are being cultivated for the local production of solasodine used by the Indian pharmaceutical industry. Commercial production of solasodine from S. aviculare is under way in New Zealand, with 1000 hectares planned for 1981. Extensive reports have been published from Hungary, and preliminary trials of solasodine production were reported from Australia, Bulgaria, Czeckoslovakia, China, New Zealand, Poland, Rumania, and Yugoslavia (Schreiber, 1968). Experimental plantings of S. marginarum are being tried in Ecuador. Despite this degree of interest, much of the literature in the field has been scattered, with language and availability acting as barriers to restrict access. This review is intended to summarize the present state of knowledge of solasodine-bearingplants. II. Solasodine-Containing Species of Solanurn

There are nearly one hundred different Solanum species reported to contain solasodine to one degree or another (Table I). Only a handful of species, however, have been considered for commercial production of solasodine. Of this handful, S. aviculare, S. khasianum, and S . laciniatum are the main candidates.

A. POROPORA (S. aviculare AND S. laciniaturn)

The New Zealand Maoris used the wordporoporo to describe both S. aviculare and S . laciniatum, since the two species are difficult to distinguish by means of vegetative characteristics. This review will follow the suggestion by Thomson (1976a) that the term poroporo be retained as a combined form when either species could be meant. There has, in fact, been considerable confusion in the identification of poroporo species. For a number of years, Hungarian workers cultivated what was thought to be S. aviculare. Mathe et al. (1964) eventually showed that these plants, derived from New Zealand-supplied seeds, were actually S. luciniarurn. It

210

JAY D. M A " TABLE I Solasodine-Bearing Species of Solanum Organs Species

S. aburiloides

(Griseb.) Bitt. et Lillo S. aculeatissium Jacq. S . americanum Mill. S. alarum Moench S . armarum R. Br. S. arundo (Mattei) (S. diplacanthum) S . asrroires Forst f. S . arriplicifolium

Gill. ex. Nees S. arropurpureum Schrank S. auricularum Ait. (S. mauritianum) S. aviculare Forst f. S . boerhaviaefolium Sendt. S . boerhaavii Thell. S . capsiciforme

(Domin) Baylis S. carolinense L. S. chlorocarpum Spenn. S. ciliatum Lam S. cornurum Lam. S. curripes Bitt. S . cyananthum Dun. in D.C. S. depilatum Kitag S. douglasii Dun. in D.C.

(%, dry weight)"

Leaves

0.01 -0.03

Schreiber, 1963

Fruits

2-3

Fruits Leaves Fruits

0.2 0.3

Verbist and Monnet, 1976; Kadkade and Rolz, 1977 Briggs ct al.. 1961 Schreiber, 1963 Schreiber, 1963 M. Saleh. 1973

Leaves Fruit Leaves Fruit Leaves

0.3 0.6 I 0.5 0.1

Schreiber, 1963

Leaves 0.5 Fruit 1.7 All pans

Schreiber, 1963

Leaves Fruit Leaves Fruit Leaves Fruit Leaves Leaves Fruits Leaves

S . dulcamara L. S . eleagnifoliurn Cav.

Fruit Fruit Leaves Leaves Fruit Leaves Fruit

S. euacanrhum Phil.

-

S.flavum Kitas

Leaves Fruits Fruits Leaves

S.fircarum L. S. gigantewn Jacq.

Referenceb

0.2 0.2 0.06 0.02 0.0Ic 0.06

0.2 0.6 0.1 0.01"

0.1 0

2-3

0.8 0.9 0.3

Schreiber, 1963 Schreiber. 1963

Kuhn and Low, 1955 Briggs er al., 1961 Schreiber, 1958, 1963 Schreiber, 1963 Lewis and Liljegren, 1970 Schreiber, 1963 Schreiber, 1963 Briggs er al., 1961 Saleh and Ahmed, 1973; Schreiber, I963 Schreiber, 1963 Rizk and Abou-Zed, 1970 Saleh and Ahmed, 1973 Schreiber. 1963 Schreiber. 1963 Ammal and Viswanathan, 1974; Harrison, 1976; Kaul and Zutschi, 1973 Herben, 1975 Schreiber. 1958 Briggs er al., 1961 Schreiber, 1963

21 1

PRODUCTION OF SOLASODINE TABLE I (continued) Organs Species S . gracile Otto ex W. Baxt.

S. guineense Lam. S . haernarocarpum hort.

S . hartwegii Benth. S . hererodoxum Dun. S . heierophyllum Balb.

S. hirsutissimum S . humile Bernh. ex Willd. S. incanum L.

S. indicum L. S . inopinum Ewan S . integrifolium Poir. S . inierandinum Bitt. S . jasminoides Paxt. S . judaicum S. jubatum Willd.

S . juvenale S . kieseriizkii S . khasianum Clarke var. Chatterjeanum Sen Gupta (S. viarum Dun.) S. laciniarum Ait.

S . linearifolium Gerasimenko,, S . lorentzii

S. lureum Mill. S . lyocarpum

S. macranrhum Dun. S . macrocarpum L.

S. mammosum L. S. marginatum L. f.

S. maritimum Meyer ex Nees S. melanorerasum Willd.

(%, dry weight)"

Leaves Fruit Leaves Fruit Leaves Fruit Leaves

0.07" 0.7

Schreiber. 1958, 1963

0.1 0.1 0.1

Schreiber, 1963

0.2 0.2

Leaves Fruit Fruit Leaves Fruit

Reference*

0.6 0.6 1.0

0.7

4

Fruit and stems I Fruit Fruit 0.1 Fruit 0.1 Aerial parts Fruit 2.2 Leaves 0 Fruit Aerial parts 5 Fruit

Leaves Fruit Stems Leaves Fruit Tops Leaves Fruit Fruit Fruit Leaves Fruit Leaves Fruit Leaves Fruit

1-3.8 3.6 0.1-0.3 0.14' 0.83

0.1-0.5 0.7-2.3

Leaves Fruit

0.1 0.3

0.5 0.8

0 0.2 0

2

Schreiber, 1963 Schreiber, 1963 Saleh and Ahmed, 1973 Schreiber, 1963 Perez-Medina et al., I964 Schreiber. 1958. 1963 Ammal and Viswanathan. 1974; Zaitschek and Segal, 1972 Herbert, 1973 Perez-Medina er al.. 1964 Briggs er al., I96 I Briggs ei a/., I96 I Jain and Sharma, 1977 Harrison, 1976 Perez-Medina ei al., 1964 Herbert, 1975 Herbert, 1973 Maiti ei al.. 1964

Briggs et al., 1961

Lewis and Liljegren, 1970 Herbert, 1975 Schreiber, 1963 Herbert, 1973 Willaman and Schubert. 1961 Schreiber. 1963 Perez-Medina ei al.. 1964; Upadhyay er al., 1969 Perez-Medina et a/., 1964; Schreiber, 1963 Harrison, I976 Schreiber, 1963 (continued)

212

JAY D. M A ”

TABLE I (continued) Organs Species

S . melongena L. S . memphiricum J. F. Gmel. S . miniarum Bernh. ex Willd. S . monis Hgl. S. nigrum L. S . niridibaccarum Bitt. S . nodijlorum Jacq. S. ochroleucum Bast.

S . oleraceum S. otronis Hylander S. palinacanthum Dun. in D.C. S. panduraeforme Drage S . paranense Dusen S . persicum Willd. S.pinnarum Cav. S . platanifolium Sims

S.pseudomeum L. S . pseudopersicum S . pyracanthum Jacq.

S . pyrerifolium S. quinquangulare Willd S . quitoense Lam. S . rosrrarum Dun. S . roxburghii Dun. S. saponaceum Dun

S . sarachoides Sendt. S . schimperianum Hochst. S. schulresii Opiz S. simile F. von Muell. S . sinaicum Boiss. S . sodomaeum L.

S . surattense S . symonii Hj. Eichler

(%, dry weight)”

Fruit Leaves Fruit Leaves Fruit

0.2 0.7 I 0.5

Leaves

0.6

Leaves Fruit Leaves Fruit

0.3 0.2 0.6 0.6

Leaves Fruit Leaves 0.07 Fruit 0 “Large quantity” Leaves All parts Fruit 1.9 Fruit Leaves Fruit Tops Fruit Tops

0.2 0. I

Tops Fruit Tops Fruit Fruit

0.03 0.4 0.03 0.01 -0.09 0.3

Leaves Fruit

0.64c 0.76

-

Bud Leaves Fruit Leaves Fruit

0.9 0.02

0.9

Reference* Schreiber, 1963 Schreiber. 1963 Schreiber, 1968; Willaman and Schubert, 1961 Schreiber, 1968 Schreiber, 1963 Schreiber, 1968 Schreiber, 1963; Willaman and Schubert, 1961 Schreiber, 1963 Harrison, 1976 Schreiber, 1963 Herbert, 1973 Willaman and Schubert, 1961 Schreiber, 1963 Novruzov and Aslanov, 1975 Ursua and Cassels, 1972 Bhatnager, 1974; Puri and Bhatnagar, I975 Saleh and Ahmed, 1973 Aslanov, 1975 Schreiber, 1963 Herben, 1975 Perez-Medina er al., 1964 Saleh and Ahmed. 1973; Schreiber, 1963 M. Saleh, 1963 Briggs et a / ., 1961 Schreiber, 1958 Briggs et al., 196I Coune and Denoel, 1975 Schreiber, 1968 Lewis and Liljegren, 1970; Briggs and Cambie. 1958 Schreiber, 1963 Schreiber, 1963

1.0

1.9 0.2’

0.18

Herbert, 1973 Lewis and Liljegren, 1970

213

PRODUCTION O F SOLASODINE TABLE I (continued) Organs Species

S . romatillo Phil. f.

S. tomentosum L. S. rorvum Sw. S. rrachycyphyum Bitter

S . rranscaucasicum S. rrijlorum Nutt. S. trilobarum S. umbellarum Mill. S . venosum

S. verbascifolium L. S. vescum F. von Muell S . villosum Lam. S . warscewiczii Hort. ex Lambertye S. wrightii Benth. S . xanthocarpum Schrad. et Wendl. (S.aculeatissimum?) S. xanthocarpum Koenen Cesrrum parqui L'Herit. Cestrum purpureum

(%, dry weight)"

Leaves Leaves Fruit Leaves Fruit

1 .o

0.1 0.7 3.2

Leaves Fruit Fruit

3.5 I .5

Leaves Fruit Leaves Leaves Fruit

0.2 0.4 1.6 0.20' 0.14

Leaves Fruit Leaves Fruit Fruit

I .o I .o

3

Leaves

0.7

Reference* Schreiber, 1963 Schreiber, 1963 Fayez and Saleh, 1967b Perez-Medina et a!.. 1964 Herbert, 1974 Schreiber, 1963 Ammal and Viswanathan, 1974 Dopke et al., 1976; Perez-Medina et al.. 1964 Perez-Medina et 01.. 1964 Schreiber. 1963 Briggs rt al., 1961; Lewis and Liljegren, 1970; Matveenkoeral.. I975 Schreiber. 1963 Schreiber. 1963 Fayez and Saleh. 1967a Schreiber, 1963 Schreiber, 1963 Schreiber. 1963 Herbert, I974

"Solasodine values on a dry-weight basis unless otherwise specified; values for fruits cited by Schreiber (1968) are all unripe fruits. *Authorities. where cited, are those given by the original author. 'Fresh-weight basis. dFree solasodine aglycone isolated from this species.

seems likely that a similar confusion afflicted Russian workers, who probably obtained their seed via Hungary. Sastri (1 969) indicated that S. aviculare was the Russian drug plant, yet the figures given for solasodine concentration were quite low for S. aviculare and were consistent with those for S. laciniatum. A number of taxonomic keys are now available to identify S. aviculare, S. laciniatum, and the relatedS. simile and S. vescum (Baylis, 1963, 1966; Bulfin, 1969; Foldesi, 1965; Imre et a l . , 1964). These have been summarized in Table 11. Solunum laciniatum is in the Archaeosolanum group. In favorable climates it is a hardy, short-lived perennial, with a natural range extending from the southern tip of New Zealand (463'2"s) to as far north as Adelaide (35"s) (Baylis,

214

JAY D. MANN TABLE I1 Identification of S. aviculare and S. Iuciniarum" Character Height (m) Stem color Leaf veins Flower: Color Diameter (cm) Corolla lobes Stigma color Fruit: Size (mm) Color (ripe) Seed length (mm) Stone cells in fruit Chromosome number (n)

S. uvicdare

S. laciniatum

1-3 Green or red Red anthocyanin

1-3 Red Green

Light lavender, sometimes white u p to 3.5 Distinct and pointed White

Dark blue-purple u p to 5 Indistinct, notched at tip Lilac

20 X 15 Bright orange Less than 2 Not obvious 23

25 x 20 Pale lemon yellow More than 2 Prominent, large 46

"After Baylis (1963); Bulfin (1969); Mathe and Foldesi (1965).

1966). Rainfall in its range is between 60 and 150 cm a year. The chromosome number of S. luciniutum is 2n = 92. Solunum simonii, with the same chromosome number, cannot be crossed with S. luciniutum (Baylis, 1954). Solunum uviculure is, in comparison with S. luciniutum, smaller, more frosttender, and more resistant to virus infection. Its range extends from the New Guinea Highlands of 1300-2700 m in elevation, through Eastern Australia, to coastal New Zealand locations near Kaikoura (42%"S) (Baylis, 1966). A few plants have been found in sheltered pockets on Banks Peninsula, in Canterbury, New Zealand, at 45"s (D. J. Davies, personal communication). The chromosome number of S. uviculure is 2n = 46. Accordingly, this species cannot be hybridized with S. luciniutum unless some ploidy manipulation is utilized. Solasodine is found in all parts of poroporo plants. Younger leaves and fruits contain most of the solasodine (Foldesi and Svab, 1969; Foldesi et ul., 1969; Lancaster and Mann, 1975; Marav'eva et ul., 1969). The small amount of solasodine found in stems is said to be concentrated in the bark parenchyma; the leaf alkaloid is found in mesophyll cells (Moskaleva and Goncharova, 1963). Solunum uviculure produces less total dry matter per hectare than does S. luciniutum, but the former species has a higher concentration of solasodine. Where winters are sufficiently mild to permit its cultivation as a perennial, S. uviculure offers both higher solasodine concentrations and better disease resistance than S. luciniutum. Fruit production from S. uviculure is not important for alkaloid processing, since the solasodine concentration is not much higher than in

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215

the leaves, and the plants fruit sparsely. This was not recognized when S. aviculare was apparently ruled out as a commercial crop for Georgia (United States) on the grounds of being too late fruiting (Massey, 1967)! Solanum laciniatum is the preferred species when annual cultivation is necessary. Both leaves and fruits may contribute to economic yield. Higher production of dry matter, but lower solasodine concentrations, is obtained from S . laciniatum.

B. Solarium khasianum This species is a bushy, thorny leaved plant, grown either as an annual or as a short-lived perennial in India (Kammathy er al., 1971). The leaves contain only traces of solasodine, and the fruits, which resemble small green tomatoes, are the commercial product. About 10% of the fruit dry weight is in an outer pericycle and p e r i c q barriers that divide the fruit into several hollow locules. The locules contain numerous small seeds covered with a slimy mucilage; solasodine glycoalkaloids are present almost exclusively in this mucilage (Saini, 1966). Alkaloid concentrations do not decrease with increasing fruit ripeness (Khanna and Murty, 1972). The location of the glycoalkaloid in the extracellular mucilage may protect against the loss of solasodine that commonly occurs in other species during fruit ripening, since in most other species the alkaloid is intracellular. Murty (1976) found no correlation between solasodine concentration and fruit size or fruit weight. The best variety was reported to be Chaterjeanum (Maiti er al., 1964). At least two reports, however, have implicitly suggested that S. khasianurn var. chatterjeanum is actually s. viarum Dun. (Kammathy er al., 1971; Datta er al., 1973). Since S . viarum is native to South America, it may be that a plant introduced into India was confused with the native species. In any event, the use of the name S . khasianum has been retained by most Indian authors. The solasodine concentrations in the fruit of S. khasianum range from 2.5 to 5.4% on a dry-weight basis (Maiti et al., 1964; Saini et al., 1965; Saini and Biswas, 1967). However, the spines are quite vicious and constitute a significant limitation to extensive cultivation of the species. The sampling method of Saini and Biswas (1967) was described as follows: “It is not possible . . . to approach each and every plant in the field for harvesting the fruits. In between the rows, passage was made with the help of bamboo sticks. Serious attempts have been made to reduce spininess. High doses of gibberellic acid resulted in elongated plants with soft, almost spineless leaves; fruit development was not mentioned (Chakraverty and Basu, 1973). Spineless polyploids were obtained with colchicine or gamma irradiation (Bhatt, 1975). These tended, unfortunately, to have very poor fruiting ability. Continued breeding of few-spined mutants was reported by Bhatt to result in better fertility in later generations. ”

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Success in production of a spineless yet fertile mutant of S. khasianum has been reported by Murty and Abraham (1975). Profuse fruit production, with undetermined solasodine concentration, is claimed. The actual extent of commercial S. khasianum cultivation in India is not known. Apparently, sufficient seeds are available as a by-product to have stimulated a study of seed oils (Parimoo and Baruah, 1975). The seed fat contained 60% linoleic acid esters, with lesser quantities of oleic and palmitic esters. A mosaic disease, which lowers solasodine concentrations, has been troublesome (Naqvi and Mahmood, 1975; Rangaraju and Chenulu, 1975; Sastry et al., 1974).

C. OTHER POTENTIALLY USEFUL SPECIES

The foregoing paragraphs have indicated that solasodine can be produced either from leaves or from fruits. Using fruits may be advantageous in terms of easier chemical purification, but this can be nullified by rapid loss of solasodine during fruit ripening. In most Solanurn species, ripe fruits have no alkaloid (Schreiber, 1963). A small number of species, however, retain significant amounts of solasodine in ripe fruits. Solanurn khasianurn is the best known of this group. Other species include S. aculeatissimum (Kadkade and Rolz, 1977); S. eleagnifoliurn and S . trilobaturn (Ammal and Viswanathan, 1974);S. giganteurn, S. torvum, and S . xanthocarpum (Krishnappa and Chennaveeraiah, 1975); S. platanifoliurn (Puri and Bhatnagar, 1975); and S. marginatum and S . rnamrnosurn (Perez-Medina et al., 1964). Solasodine concentrations of 2% or better, on a dry-weight basis, are reported for these species. The property of retaining alkaloid during ripening provides a significant agronomic advantage by minimizing the need for precise timing of harvest operations. Localization of glycoalkaloid in an extracellular mucilage rather than intracellularly seems to confer added stability in these species. For instance, Perez-Medina et al. (1964) reported that the small amount of greenish liquid inside the pericarp of ripe S. rnamrnosurn fruits contains 18-20% glycoalkaloid. (Fruits of this species have been used in Peru as a rat poison.) Similarly, two-thirds of the alkaloids of S. marginatum fruit are in the mucilage around the seeds, and one-third in solid tissue (K. E. Blyth and J. D. Mann, unpublished work). Teleker al. (1977) have proposed cultivation of S. marginatum in the lowland tropics. Yields of 32.5 kg/ha were obtained, with the prospect of better yields from modified agronomic techniques and strain selection. Severe loss of solasodine during ripening of fruit means that weekly hand harvesting from the thorny plants would be required. The bitter, inedible fruits of S. incanum, a perennial of the Lower Jordan and Dead Sea, were shown to contain about 2% solasodine (Zaitschek and Segal, 1972). A variety of this species from North Kerala, India, was found to have

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217

3.8-4.8% alkaloid (Ammal and Viswanathan, 1974). This variety was being used as an oral contraceptive by a local tribe. Solanum aculeatissimum (mostly called S . xanthocarpum) from Nagpur, India, and from Nepal produces fruit with 1% solasodine (Tupkari et a l . , 1969; Verbist and Monnet, 1974a). In France, these plants reportedly had fruits with 34.6% solasodine (Verbist and Monnet, 1974b). Sparse fruiting was associated with this high concentration, however, for yields of only 3.35 kg of solasodine per hectare were calculated (Verbist and Monnet, 1975a). It is not clear whether the plants first described as S. xanrhocarpum and later corrected to S. aculeatissimum (Verbist and Monnet, 1976) are the same as the S. xanthocarpum plants tested by Schreiber (1963). Natural product chemists are not generally noted for their taxonomic skills. Confirmation of solasodine from S. aculeatissimum has come from Kadkade and Rolz (1977). There do not seem to be any species other than S. aviculare and S . laciniafum worth considering for foliar production of solasodine. An alternative steroidal alkaloid, tomatidenal, can, however, be converted to 16-D even more smoothly than solasodine (Schreiber, 1974). Tomatidenol glycoalkaloids can be obtained from certain strains of S. dulcamara (Boll, 1962; Rasmussen and Boll, 1958). This species has several chemotypes of chemovariants (Willuhn, 1967). Some otherwise identical types of S. dulcamara produce predominantly soladulcidine tetraglycosides (Willuhn, 1966, 1969a), whereas others synthesize predominantly solasodine compounds. A study of the Hungarian varieties of S. dulcamara showed that most were soladulcidine or solasodine types, with a few tomatidenol types in northem Hungary (Mathe and Matht, 1972). Commercial cultivation of tomatidenol-forming types of S. dulcamara would require some readily visible phenotypic marker’s being incorporated so that fields of the crop could be rogued free of soladulcidine-containing plants. It is likely that contamination of the crude tomatidenol with soladulcidine would present problems during chemical processing. Contamination with solasodine would be less troublesome, since the two are stereoisomers. Regardless of the alkaloid type found in the vegetative organs, fruits of all types contain predominantly solasodine (Willuhn, 1967). This phenomenon suggests that solasodine glycoalkaloids may play a specific role in fruits. Protection against insects seems unlikely to be that role, since soladulcidine tetraglycoside is more toxic to insects than are the triglycosides (Boll, 1962). 111. Chemistry

The following treatment is not intended to replace the complete description of Schreiber (1968) but to summarize this confusing field for botanically oriented readers. The steroids look so much alike in their ring structures that the small but

JAY D. MANN

218

cnlical differences are hard to appreciate. Some pertinent steroidal compounds are summarized in Fig. 1. The most important differences arise from the possible unsaturation between bonds 5 and 6 (A5),the orientation of the F ring (for example, tomatidenol versus solasodine), and the presence or absence of oxygen in ring E. The close structural similarity between steroidal alkaloids and corresponding nitrogen-free sterols is evident in Fig. I . For commercial drug production, it is important to have the A5 linkage. Hence, diosgenin, solasodine, tomatidenol, and yamogenin would all be suitable,

Tgogmin:X=O Solasodine: X=NH Dio8genin : X=O

Tomatid-5-en01 : X=NH Yamogenin :X=O

Ho

CHI I

Ho

dP

Neotigogenin: X=O

/ Ho

Solanidice

16-Dehydropregnendone ("16- 0")

Norethynodrel

Betamethasone

FIG. 1. Structures of pertinent steroidal compounds.

PRODUCTION OF SOLASODINE

219

whereas neotigogenin, soladulcidine, tigonenin, and tomatidine would not. Of equal importance is the ease of removing the F and most of the E ring to form 16-D. The usual route is via acetylation and oxidation. Whereas conversion of diosgenin to 16-dehydropregnenolone is about 50%, solasodine gives about 65% yield (Harrison, 1976). Alkaloids of the solanidine type cannot undergo this facile conversion. Two (out of many) steroid drugs are shown in Fig. 1. Norethynodrel is a typical fertility control agent, being 1 %nor (Djerassi, 1966). Betamethasone exemplifies the corticosteroid group, having oxidized substituents on carbon 20. The structure of solasodine was first correctly described by Bell and Briggs (1942). Solasodine was isolated from a number of Solanum species (Bell et al., 1942; Briggs and Cambie, 1958; Briggs et af., 1961). Schreiber has been especially active in this field of chemistry, and a comprehensive review by him (1968) should be consulted. Recent chemical and biochemical investigations have been summarized by Schreiber (1974). An annual series of reviews on alkaloid chemistry provides continuing coverage of the literature in this field (Harrison, 1976; Herbert, 1973, 1974, 1975). Solasodine has not been isolated in significant quantities as the free steroid, except ins. cyananthum (Rizk and Abou-Zied, 1970). Instead, it is found with a series of sugar residues attached to the oxygen at C-3. Triglycosides (with three sugar residues) are by far the most common forms. Solasonine, consisting of solasodine linked with a mole each of glucose, galactose, and rhamnose, was the first glycoalkaloid identified (Bnggs et al., 1942, 1963; Kuhn and Low, 1955). The glycoside linkages have been summarized diagrammatically in Fig. 2. It will be noted that solasodine is a member of a solatriose group of compounds, in which the same trisaccharide moiety is found with a variety of different aglycones attached. Solamargine is the predominant glycoalkaloid in most species (Briggs et al., 1952, 1975; Briggs and Brooker, 1953). As shown in Fig. 2, solamargine is but one member of a chacotriose series of glycosides. It is especially noteworthy that dioscin, a common glycoside of diosgenin, has the same sugar structure as solamargine. This argues for a high degree of evolutionary stability and enzymatic specificity on the part of the glycosidating enzymes. Small quantities of diglycosides and monoglycosides have been isolated from Solanum leaves and fruits. (The monoglycosides are omitted from Fig. 2 but comprise derivatives with either galactose or glucose.) These traces of lower glycosides may represent glycoalkaloids en route to the triglycosides, or they may be formed from enzymatic attack on the triglycosides during extractions or tissue ageing. In the other direction, at least five tetraglycosides are known to occur. A Mexican wild potato contains a demissine tetraglycoside (demissidine is a 5,6saturated solanidine). Another tetraglycoside contains soladulcidine as the al-

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JAY D. M A "

Glycosides of solatriose series

Aglycone

Glycosides of chacotriose series

(a) Diglycosides

R = solasodine R = solanidine R = tomatidenol

Glu p(1+3)-Gal p(1+3)-R p -solasonine p-solanine 8-solamarine

a(1+2) or Rhm a(l+4)-Glu p ( 1-+3)-R P-solamargine p-chaconine y-solamarine

(b) Triglycosides

R R R R

= = = =

solasodine solanidine tomatidenol diosgenin

Rham a (1+2), Glu p (l+3)Gal+ (1+3)R solasonine solanine a-solamarine

-

Rham a ( 1+2), Rham a(1-4) Glu-(I+3)R solamargine a-chaconine p-solamarine dioscin

(c) Tetruglycosides

R

R

=

=

solasodine

soladulcidine

R = tomatidine R = tomatidenol

Rham a(1+2), Glup'(l-t2)-Glu P(1+3)-Galp(1+3)-R solaradixine X YP(1-3) ~ Glu p ( I + 2 ) h u p ( 1+3)-Galp(1+3)-R soladulcidine tetraoside a-tomatine -

Arab-Rham Rham-Glu-R

-

soladulcamarine

FIG. 2. Relationships among glycosides of steroidal compounds. Abbreviations: Glu glucose, Gal = o-galactose, Xyl = D-xylose, Rham = L-rhamnose, Arab = L-arabinose.

= D-

kaloid, with a sugar portion consisting of solatnose (glucose-galactoserhamnose) plus a D-xylose. Both demissine and the soladulcidine tetraoside are toxic or repellent to larvae of the Colorado potato beetle (Boll, 1962; Petrotschenko, 1957). Tomatine, from tomato leaves, is also in the xylosesolatriose series, with tomatidine as aglycone moiety; this tetraglycoside also shows toxicity to the Colorado potato beetle (Roddick, 1974). Tetraglycosides have been described that belong to the chacotriose (rhamnose-glucose-rhamnose) series. Soladulcamarine, from some varieties of S.dulcamara, is in this group (Rasmussen and Boll, 1958). A solasodine compound, P-solanigrin, with two moles of rhamnose, one of glucose, and one of galactose, is probably a chacotriose derivative, but the sequence of sugars is not known (Schreiber, 1968). Solanigrin was the main glycoalkaloid in S . boerhaviaefolium and S . gracile (Schreiber, 1958). A tetraglycoside derivative

PRODUCTION OF SOLASODINE

22 1

of solasodine had also been reported by Briggs and Brooker (1958), but this claim was later withdrawn (Briggs et al., 1961). Nevertheless, three higher glycosides of solasodine were isolated from roots of S. laciniatum by Bite and co-workers (1970a; Bite and Shabana, 1972). One compound, solaradixine, consists of solasonine with an additional P-D-glucose residue. Solashabanine is formed from solasonine with two additional glucoses, whereas solaradinine is similar with three additional glucose units. The higher glycosides, starting from the triglycoside level, are more watersoluble than the lower homologues. During prolonged storage of leaves some sugar residues may be enzymatically lost (Syhora et al., 1962). This will result in lower levels of acid-extractable glycoalkaloid, yet total solasodine might not be altered, as shown by extraction with organic solvents. Solvent extraction has its own drawbacks, however. Triglycosides have the ability to precipitate with cholesterol even in alcoholic solutions. This is potentially useful for purification, but it cannot be used with the aglycone. Finally, it is clear that at least some tetraglycosides have insecticidal activity not shown by triglycoside homologues. Whether the still higher homologues-solaradixine, solashabanine, and solaradinine-have similar biological properties is not known.

IV. Biochemistry

A. BIOSYNTHESIS

Biosynthesis of the spirosolane alkaloids such as solasodine is intimately associated with the biosynthesis of spirostane steroids having the same ring stmcture. The insertion of nitrogen into the alkaloids occurs quite late in the biogenetic pathway. It is common to find both solasodine and diosgenin or chlorogenin in the same plants (Fayez and Saleh, 1967b; Saleh, 1974; Saleh and Ahmed, 1973). The ratio between diosgenin and solasodine in leaves ofS. laciniatum has a restricted range between 1:7 and 1:16 (Panina and Madaeva, 1967). The generally accepted pathway for steroid biosynthesis in plants is outlined in Fig. 3. The starting point is acetyl-CoA, which is converted to cholesterol via a mevalonic acid pathway. A series of hypothetical reactions as shown in Fig. 3 (after Kaneko et al., 1976) leads through known compounds to a key intermediate teinemine. Teinemine can then be cyclized in a number of ways to produce either the two stereoisomers, solasodine and tomatidenol, or else solanidine. Experimental evidence for this hypothetical pathway consists almost entirely in demonstrationsthat labeled procursors can be converted to the anticipated final

222

JAY

0 3[CH3&-SCoAI

Acetyl CoA

D. MANN

-

?H HOCH2-CHp-C- CH2-CooH CH3

Mevalonic Acid.

[OI

Solasdine

'

Teinemine

Tomatidenol

Etioline

Solanidine

FIG.3. A possible pathway for steroid biosynthesis in plants, modified from Kaneko er al. ( 1976).

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223

products (Roddick, 1974; Schreiber, 1974). The ring carbons of the steroid structure solasodine ought to be derived from either the methyl or the carboxyl carbons of acetic acid. Careful degradations after administration of radioactively labeled acetic or mevalonic acid toS. faciniatum plants have confirmed the localization of the radioactivity in the anticipated carbons of solasodine (Guseva and Paseshnichenko, 1962; Guseva et af., 1961). Similarly, labeled cycloartenol and lanosterol were converted to solanidin, tomatidine, and solanocapsin by suitable plant species (Ripperger et al., 1971). Cholesterol or a closely related sterol is believed to lie between cycloartenol and the steroidal alkaloids. Heftmann et af. (1967) demonstrated that leaves of Lycopersicon pimpineffifofiummetabolized labeled cholesterol to tomatidine. Tschesche and Peistert (1975) found that both 20-hydroxycholestero1and 20aminodihydrodiosgenin were converted to solanidine. Studies with tritiumlabeled intermediates showed that the hydroxyl group postulated at C-26 or C-27 could be replaced directly with nitrogen without the formation of a C-26 keto intcmediate (Tschesche et a f . , 1976). These results are consistent with the scherne postulated. Nitrogen is first inserted, according to this scheme, at some level after dormantinone, presumably through intermediate formation of a Schiff base. L-Arginine was twenty times as efficient as ammonium ion in supplying nitrogen for synthesis of solanidine in Veratrum grandzj7orum (Kaneko et al., 1976). Tissue culture studies have yielded only limited information to date. Sofanum faciniarum tissue cultures produced steroids rather than alkaloids (Vagujfalvi et a f . , 1971). Tissue cultures of S . xanrhocarpum synthesized solasodine when 2,4-D rather than IAA was used as the auxin (Heble et af., 1968, 1971). When suspension cultures of S. xanthocarpurn were supplemented with cholesterol, twenty times as much solasodine was produced (Khanna and Manot, 1976). This agrees well with the hypothetical pathway of Fig. 2. The intracellular site of alkaloid biosynthesis is not known. Isolated chloroplasts of greening potato tuber peels were capable of synthesizing solanidine (Ramaswamy er af., 1976). No comparable studies seem to have been performed with leaf chloroplasts. If the broad outlines of aglycone synthesis can be discerned, the route for glycoside attachment is shrouded in mystery. Labeled solasodine aglycone was converted to solamargine and solasonine when administered to stem sections of S. faciniatum (Liljegren, 1971). An enzyme preparation was obtained from the leaves that could convert solasodine + UDP-glucose to glucosidyl solasodine. Presumably there also exists an enzyme to form galactosidyl solasodine. Solasodine aglycone is so insoluble, however, that it is difficult to understand why glycosidation (and an increased solubility) should await this late step in synthesis. Perhaps the glycosidating enzymes are relatively nonspecific and would be capable of using steroid intermediates on the level of cycloartenol or

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JAY D. M A ”

cholesterol. Alternatively, the demonstrated enzymes may serve a scavengingrole to prevent undesirable intracellular precipitation of any solasodine that might be formed from glycosidase attack on the glycoalkaloids. Steroidal alkaloids are atypical, or “alcaloida imperfecta” (Roddick, 1974), because the nitrogen is added very late in their biogenesis, in contrast to ordinary alkaloids derived in most cases from amino acids. The steroidal alkaloids are a product of “high-carbohydrate” rather than “high-nitrogen’’ conditions (Nowacki et al., 1975). The response to nitrogen fertilization is unusual and can be accounted for if carbohydrate supplies are rate-limiting in glycoakaloid biosynthesis. The concentrations of solasodine in poroporo leaves remained quite constant over a range of levels of nitrogen fertilization. With higher rates, leaf growth was stimulated and total solasodine per plant increased (Crush, 1973). Similarly, Nowacki et al. (1975) found that, although the concentration of glycoalkaloids in the tops of potato plants diminished with higher rates of nitrogen fertilization, total alkaloid per plant increased. In contrast, the “highnitrogen” alkaloids of Nicotiana and Datura were found in much higher concentrations in leaves of nitrogen-fertilized plants (Nowacki et al., 1975). Carbohydrate levels can be diminished by shading leaves. This treatment severely inhibited solasodine production by S . laciniatum (Bernath et al., 1976). During growth, leaf glucose and leaf solasodine concentrations showed a positive correlation of r = 0.80 (Moursi and Ahmed, 1973b). On the other hand, there were no obvious correlations between sugar levels and alkaloid concentrations in the fruits (Moursi and Ahmed, 1973a).

B. TURNOVER

A number of alkaloids show surprisingly high turnover rates (Floss et al., 1974). No estimation of turnover for the glycoalkaloids of Solanurn is available; however, changes in the relative proportions of solasonine, solamargine, and related glycosides indicate a time scale on the order of weeks rather than days (Lancaster et al., 1977; Moursi and Ahmed, 1973b). In addition, changes in the solasodine content of leaves are well established. Young, fully expanded leaves contain the maximum concentrations of solasodine. The older leaves have lower concentrations (Murav’eva et al., 1969; Foldesi et al., 1969; Moursi and Ahmed, 1973b). Although Moursi and Ahmed (1973b) considered that lower concentrations in older leaves resulted from dilution with veins and other “inert” leaf parts, Lancaster et al. (1977) showed that the absolute quantity of solasodine per leaf decreased in older leaves. The customary explanation of such concentration patterns is that the alkaloid is synthesized in young, growing leaves and subsequently destroyed in older leaves. This hypothesis was confirmed by following alkaloid concentrations in selected individual leaves sampled by leaf punches.

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225

The low alkaloid concentrations of older (but still fully green) leaves was a result of alkaloid loss rather than early restrictions to alkaloid synthesis (J. E. Lancaster, unpublished work). Rapid loss of solasodine could be artificially induced by spraying plants of S. luciniurum with a mixture of actidione and ethephon. The mature leaves turned from green to bright yellow and lost half their solasodine within 8 days (J. D. Mann and K. E. Blyth, unpublished work). Solasodine in poroporo fruits disappears as the fruits ripen (Moursi and Ahmed 1973a). The ripe fruits were used for jam-making by the early European settlers in New Zealand. Tomatine in tomato fruits also disappears during ripening (Roddick, 1974). Since the alkaloid was almost exclusively in the supernatant fraction after centrifugation of tomato extracts, it was regarded as a vacuolar constituent (Roddick, 1976).

C. DEGRADATIVE PATHWAYS

Specific glycosidases isolated from sprouting potatoes were shown to attack solasonine and solamargine (Petrotschenko, 1957). These were used in the study of the glycoside structures (Guseva and Paseshnichenko, 1958). When solasonine was the substrate, one mole of rhamnose was removed to form “Psolasonine”; next a mole of glucose was split to leave “y-solasodine” (that is, galactosidyl solasodine). Finally, the solasodine-galactose link was severed. Enzymatic hydrolysis of solamargine gave less clear-cut results. Free solasodine appeared very early, and no “y-solamargine” (that is, glucosidyl solasodine) was found. A rhamnose-glucose-solasodine compound, called “P solamargine,” was found in the enzymatic hydrolyzate, and was also isolated from leaves of S. uviculure. Guseva and Paseshnichenko (1958) suggested that enzymatic attack on ‘‘p -solamargine” resulted in removal of glucose-rhamnose as a disaccharide rather than two stepwise removals. There is apparently no published study on glycoalkaloid hydrolysis using enzymes from poroporo rather than potato, although Liljegren (1971) mentioned unpublished work. Syhoraer af. (1962) found that approximately three-fourths of the glycoalkaloid in excised leaves was lost during storage for 1 week at 20°C; the original content of solasodine was still present, as shown by extraction with methanol. After 2 weeks of storage, significant losses of solasodine aglycone had occurred. Thus, initial degradation of glycoalkaloid involves cleavage of sugars without attack on the alkaloid rings, but later the alkaloid itself is modified. The fate of the catabolized solasodine moiety is not known. In studies of tomatidine breakdown (Roddick, 1974), a 23-hydroxy derivative, pimpinellidine, has been implicated. A later step would be 3-P-hydroxy-5apregn- 16-en-20-oneglycoside, in which the E and F rings have been removed, with at least some sugars retained (Heftmann and Schwimmer, 1972).

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JAY D. MANN

In the intact plant, export of solasodine glycosides is a possible but unproved explanation for the losses in alkaloid during the maturation or aging of various plant organs. For instance, roots of S . laciniatum acquire solasodine during a period when leaf levels are decreasing (Lancaster and Mann, 1975). Subsequent studies, however, have given no evidence for transport of solasodine within the plant; in fact, excised roots were found to be capable of synthesizing solasodine from mevalonic acid (J. E. Lancaster, personal communication). Similarly, when Willuhn (1969b) made reciprocal grafts between solasodine-type and tomatidinenol-type S . dulcamara, there was no evidence for transport of alkaloids to either leaves or fruits. V. Isolation and Determination of Solasodine A . EXTRACTION

A comprehensive review of extraction methods published recently by Weston (1976) should be referred to for details of the methods described in this section. A Russian reference (Lakova et al., 1975) might also be useful. An apparently simple way to extract the glycoalkaloids is to obtain a juice exudate by chopping and expressing cell sap in a way similar to that used by Pine for leaf-protein preparation. Unfortunately, most of the liquid obtained in this manner arises from stems rather than leaves (Tashbulatov and Martynov, 1973) and hence contains little solasodine. Crushing methods result in only 60% yields (Martynov and Sklizov, 1974); this was ascribed to a binding of alkaloid onto cellular material. Experience in our laboratory has shown that solasodine and its glycoalkaloids are firmly bound even on such surfaces as slightly etched glassware. Enzymatic breakdown, too, may be partly responsible for low yields. A critical chopping size below 0.5 cm caused considerable losses of solasodine (Tashbulatov and Martynov, 1973). Such chopping would liberate hydrolytic or oxidative enzymes affecting solasodine. Thus, it is necessary to extract the glycoalkaloid-containing tissue with external solvents, typically in a 1O:l or 15:l ratio of extractant to tissue. It would be very convenient to be able to perform this extraction on fresh, undried tissue, since the cost of drying leaves and stems can represent a large portion of the total cost of extraction. Unfortunately, most fresh-tissue extraction methods are proprietary secrets. If fresh tissue is extracted, then the factory must be large enough to handle relatively large quantities of leaves arriving at the factory gate when harvest conditions are right. This is more of a problem with annual harvesting of S . laciniatum than for the perennial cultivation of S . aviculare, since repeated

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cuttings can be scheduled at convenient intervals. Tempting as it might be to consider cold storage of fresh tissue, such storage, even at temperatures below freezing, leads to solasodine losses over periods of 2 or 3 months (Retezeanu and Constantinescu, 1963). Similarly, when fruits of S. aculeatissimum were frozen extractable solasodine content was significantly less than with freshly extracted fruit (Verbist and Monnet, 1975b). If incoming tissue is dried, then extracting equipment can be scaled down to the right size to process the summer's harvest over the full calendar year. Drying generally involves some sort of flowing hot-air process, since stagnant heaps of leaves lose solasodine. Leaf temperatures must be maintained somewhere below 80" or 90°C, as prolonged drying at temperatures above 110°C can cause significant alkaloid loss (J. E. Lancaster, unpublished data). The leaves lose water rapidly, the stems slowly. It is not uncommon for seemingly dry material to come out of the equipment and then, during the next day or so, turn into a soggy mass as the moisture from the interior of the stems diffuses out into the dry leaf fragments. Mechanical separation of stems from leaves can be attempted on partly dried samples; this can lead to some energy-saving, since not all the moisture of the valueless stems need be removed. Engineering solutions to these requirements are straight-forward but expensive. The actual process of extraction can be with either alcohol or aqueous acids. Alcohol extracts yield more total solasodine but are significantly more contaminated with pigments and resins. Losses during purification of the alcohol extracts can result in overall yields comparable to those of aqueous extraction methods. Aqueous acids used are commonly 1-2% sulfuric acid, or 3-5% acetic acid. Szilagyi and Tetenyi (1967) found identical results from 2% solutions of acetic, oxalic, citric, or tartaric acid. Extraction periods are typically 24 hours at 20"C, although 15 minutes in 5% acetic acid at 100°C did not cause any loss of glycosides (Ananichev and Loshkarev, 1969). Dilute sulfuric acid at 50°-60"C has been used with extraction times of 2 hours. One method for extraction of diosgenin from yams is to hydrolyze the tubers in siru without prior extraction of the diosgenin glycosides (Applezweig, 1962). A similar process has been patented for extraction of Solanum alkaloids (Lohen and Sollins). The acidified pulp is hydrolyzed at 125"-135"C for 1-5 hours. After neutralizing, the filter cake is extracted with petroleum ether or hexane in a Soxhlet apparatus. It is not clear how these two solvents are supposed to be capable of extracting solasodine, since the alkaloid is insoluble in them. An interestingin siru hydrolysis has been described by Panina et al. (1975a,b). The fresh plant material (one part) is added to three parts of isopropanal; then hydrochloric acid is added to 3 or 4%, and the mixture is refluxed for 5 hours. Originally, calcium hydroxide was added to neutralize and precipitate solasodine, and then solasodine was extracted from the precipitate with xylol. In a

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modified version, the acid hydrolyzate, still with the plant pulp, is neutralized with sodium hydroxide, and then solasodine is extracted from this with at least two-thirds volume of xylol at a temperature of 50°-55"C. Both the volume and the temperature are important. An alcohol-water solution of acetic acid is then utilized to remove solasodine from the xylol fraction. Recoveries of 85-90% of total solasodine are claimed. In methods where glycoalkaloids are first extracted intact it is then necessary to hydrolyze them. An undesirable side reaction during hydrolysis leads to A3solasodiene, by removal of the C-3 hydroxyl group. To minimize solasodiene formation, the hydrolysis is carried out under reflux with alcohol-water mixtures, using hydrochloric or sulfuric acid. Solasodine aglycone is insoluble in water, and the alcohol helps keep it in solution. After hydrolysis, alcohol is distilled off, and the mixture is made alkaline. Solasodine precipitates and can be removed as a solid or extracted into benzene, chloroform, or xylol. Subsequent extraction of the organic solvent with aqueous phosphoric acid (Brutko, 1966) or aqueous acetic acid (Weston, 1976) removes solasodine into the acid, while the solasodiene impurity stays in the organic solvent. This cleanup is built into the Panina method described above.

B. ASSAY

Agronomic and genetic work on solasodine production would be facilitated by a quick, moderately accurate assay for solasodine content. Decisions regarding the timing of harvests or the selection of individual plants for propagation need almost immediate or one-day service. The need is for a fast method, even if it is imprecise and nonspecific. Unfortunately, despite the remarkably large number of methods cited in literature, most prove to be slow and relatively nonspecific. A wide range of methods for a single compound often signals the absence of one really satisfactory technique. In almost all the assay methods, extraction of the alkaloid from a weighed and, most important, truly representative tissue sample is one of the more tedious and time-consuming steps, and one perhaps least suited to full automation. A sampling of the methods available to the analyst is very briefly summarized in Table 111. (Note: A greatly expanded description of assay methods can be provided by the author and will be kept on file at the Library, Botany Division, DSIR, Private Bag, Christchurch, New Zealand). In our laboratory we employ a colorimetric method modified to have most manipulations contained within a single Pyrex glass tube that serves for both hydrolysis and centrifugation. Gas chromatography offers a useful alternative if suitable equipment is available. Automatic injectors and digital integrators would almost certainly be needed for production-scale analyses.

229

PRODUCTION OF SOLASODINE TABLE I11 Methods of Assay of Solasodine Type

Range

Reference

Gravimetric determination Nonaqueous titration

100 mg upward

Dye binding

10-100 p g

Ion exchange Marquis reagent (acid-formaldehyde) Nephelometry Thin-layer chromatography (antimony trichloride spray) Electrophoresis Columns (HPLC) Gas-liquid chromatography

? 20-200 pg

Bell and Briggs, 1942 Bite ef al., 1970 ; Valovich. 1964. 1965; Hardman and Williams, 1976 Birner, 1969; Balcar and Zalecka, 1962; Lancaster and Mann, 1975 Andreeva and Romanchuk, 1970 Ananichev and Loshkarev, 1969; Guseva et al., 1965; Khanna and Murty, 1972 Guseva et al., 1965 Sofowora and Hardman, I974

Gram quantities? 0.2-1 pg

Fungal growth inhibition

?

1-2 rng

0.2-1.6 mg 2-50 p g ?

Saber et al., 1965 Hunter et al.. I976 T. Mason, private communication; Herb et al., 1975 Mathe and Foldesi, 1965

VI. Agronomy of Poroporo

Although there exists a considerable amount of literature dealing with cultivation of S. laciniatum, almost nothing is written about S. aviculare. To a large extent results from one species can be applied to the other, if the greater frosttenderness and slower growth rate of S. aviculare are kept in mind. Despite extensive preliminary tests in many parts of the world (Schreiber, 1968), long-term studies seem to have been restricted to Hungary, Russia, and New Zealand. A comprehensive summary of Hungarian results is provided in the publication by Mathe and Foldesi (1965). Many of the statements made in this review are, unless specific reference elsewhere is cited, derived from the Mathe and Foldesi compilation. The same information is generally repeated in separate papers in Herba Hungarica; these references have been cited when possible, since the journal is more widely available than the 1965 volume. It is rumored that the Hungarian solasodine production has been discontinued as being noneconomic. Russian publications concerning commercial production are somewhat limited (Davtyan and Babakhanyan, 1974; Kiselev and Stotskii, 1975). At least one paper (Tupkari et al., 1969) described cultivation of S. aviculare, but it seems likely that S. laciniatum was meant. The overall significance of solasodine to the Russian steroid drug industry is not clear. Alekseenko e f al. (1976b) stated that S . laciniatum was the sole source of cortisone and progesterone in the USSR, but

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Applezweig (1969) reported Russian purchases of diosgenin-derived intermediates from the West. Other East European countries have tested Solanum species, apparently with little success. Certainly, a Czechoslovakian report calling for pot culture of the plants would not encourage large-scale trials (Stary and Kybal, 1961). Lack of publications does not necessarily indicate absence of field trials, since commercial secrecy and the common habit of making photocopied reports for local circulation discourage formal publication. Only three short, noncomprehensive notes (Fawkner, 1974; Fryer, 1972; Palmer, 1977) have arisen from extensive field trials in New Zealand. There are a number of points about which considerable confusion has existed: 1. Solanum aviculare versus S . laciniatum. The taxonomic difficulties with these two species have already been discussed. Nonflowering plants are extremely hard to differentiate unless plants of both species are growing alongside for comparison. 2. Glycoalkaloid yields versus solasodine yields. In some of the literature, yields are stated in terms of percentage of glycoalkaloid. Since the molecular weight of the trisaccharide glycoalkaloids is nearly double that of the aglycone solasodine, this can result in false optimism as to the marketable yields of solasodine, particularly from nonchemically trained administrators. I have attempted to bring all such estimates down to earth by using only the solasodine concentrations. 3. Solasonine is a common description of the glycoalkaloid present, yet in almost all cases solamargine is found, by chromatographic methods, to be the predominant alkaloid. The use of solasonine is an historical accident arising from the work of Briggs et al. (1942), who isolated solasonine first, and then described solamargine later (Briggs et al., 1952). Use of the term “solasonine” ought to be restricted to the triglycoside of solasodine containing glucose, galactose, and rhamnose, and ought not to be used interchangeably with “solasodine glycosides,” since the latter term also includes solamargine. The older literature tends to blur this distinction, which may be academic at present but might become important were it to be found that one or the other triglycoside has different hemolytic or pesticidal properties.

A. SEED GERMINATION

The seeds of S. laciniatum are quite small, with diameters about 2 mm, and a mean weight of 1 ?hg per loo0 seeds. Those of S . aviculare are larger. Germination and early seedling establishment are very troublesome. In some years, direct

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seeding results in good stands, but this is unreliable, and complete failure is not uncommon. At present, transplants seem to be the only way to guarantee a reasonable stand. Efforts to accelerate seed germination show a notable lack of consistency. Earlier results were summarized by Foldesi (in Mathe and Foldesi, 1965). The optimum germination temperature is fluctuating either between 12"and 25"C, or else between 25" and 30°C. The latter optimum has been confirmed by Fawkner (1974). In the work described by Foldesi there was either no response to light or else only a slight improvement (85% versus 68%). Both species of poroporo, however, have been found by N. G. Porter (personal communication) to show good response to light. In general, the state of ripeness of the fruit from which seeds are obtained makes little difference to seed germination, unless very immature fruit are used (Sudiatso and Wilson, 1974). Fawkner (1974) found better germination, however, by using orange-ripe fruit. Sudiatso and Wilson (1974) found that leaching seeds with water did not improve germination, but Fawkner (1974) reported improvement with either 5 days in tap water with S. luciniutum or 9 days in 30°C water with S. uviculure. The rate of seedling emergence, rather than total percentage germination, was improved in Fawkner's tests, and subsequent seedling growth was inferior to that of nonleached controls. Steeping in aqueous solutions of gibberellic acid was stimulatory if done for 9 days but no longer (Sudiatso and Wilson, 1974). Porter and Gilmore (1976) showed that 1 mM solutions of gibberellic acid made up either in acetone or water could improve germination. When the acetone solution was used, the seeds could subsequently be stored dry without loss of the beneficial effects of the hormone treatment. Only seed of S. luciniutum, not S. uviculure, showed a gibberellic acid response. Porter and Gilmore found that germination tests using filter paper or blotting paper gave entirely different results from tests using soil as a germination medium. It takes up to 6 weeks for seeds to germinate, with a further 40-50 days in cold frames or glasshouses for seedlings to reach transplanting size. (Sofunurnuviculure seed may germinate faster than S. luciniutum.) Although the Hungarians accepted the extra costs of transplanting, apparently in Russia some success was had by directly drilling S. luciniatum seeds; it took 65-80 days for the plants to reach a height of 30-40 cm.

B. SOIL PREPARATION, PLANTING DISTANCES,

ETC.

A reasonable range of soil types is tolerated by poroporo. Growth starts sooner in easily warmed loose soils than in heavy soils (Bernath and Foldesi, 1971). Adequate moisture is important, with 20-25 cm of rain during the growing

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season if winter rainfall has been adequate. Baylis (1966) suggests a total yearly water requirement of 60 cm. Fertilizing with superphosphate at planting time has not been shown to improve yield. There is a definite response to added nitrogen, although low and high rates of nitrogen supplementation do not give especially different responses (Bemath arid Foldesi, 1972; Crush, 1973). There has only rarely been a response to added phosphorus and potassium, and then only in drought years (Foldesi, 1964). Although initial Russian and Hungarian practice involved using complete nitrogen-phosphorus-potassium mixtures, probably as “insurance, ” it was later stated that 400-500 kg of potassium nitrate per hectare was sufficient (Mathe and Foldesi, 1965). The foregoing results pertain to annual cultivation of S. laciniatum. It is possible that in perennial cultivation of S. aviculare nitrogen alone will not suffice, particularly in phosphate-poor New Zealand soils. Responses to boron and manganese were found in Russia (Kvitaishvili, 1967). Weed control has been a serious problem, since the young plants are very slow in their initial growth. Treflan (trifluralin) has been successful in Hungary (Foldesi and Svab, 1969), while Sencor (metribuzon) is recommended in New Zealand. Napropamide [N,N-diethyl-2-(1-naphthyloxy)-propionamide] is registered in New Zealand for experimental control of annual grasses and broadleaf weeds in poroporo. Resistant perennials can be very troublesome in S . aviculare plantations. There is a surprising degree of uniformity in recommended planting distances. In Poland, 0.24 m2 per plant was recommended (Golez, 1964). Hungarian practice is 0.25-0.33 & per plant (about 13,000 plants per acre). Wide spacings of 2.4 m2 per plant reduced overall alkaloid yield (Bemath and Tetenyi, 1973). Standard spacing in New Zealand has been 0.3 m3 per plant. The only exception to this range is a report by K. S. M. Sastry et al. (1973), who allowed over 1 & per plant. It seems likely that this wide spacing was intended for hand harvesting of leaves. A circular-density trial (Nelder scheme) in New Zealand showed that somewhat higher yields could be obtained by very dense planting, with only 0.04 & per plant (D. J. Davies, personal communication). This high density would not be economically practical, since the improved yield would not cover the added cost of transplanting additional seedlings. Under special circumstances where land area rather than costs were limiting, high-density planting might be advantageous. Density has no effect on leaf solasodine concentration (J. D. Mann and D. J. Davies, unpublished). There does not seem to be any comparable density recommendation for S . aviculare. Under a perennial system of cultivation, even low-density plantings will eventually cover the ground, although early yields in the first year of growth probably could be improved by denser plantings.

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C. GROWTH OF POROPORO

Considerable attention has been paid to changes in alkaloid levels during the growth ofS. laciniatum (Golez, 1964; Foldesiet al., 1969); Moursi and Ahmed, 1973b; Lancaster and Mann, 1975). When all leaves on the plants are bulked, analyses show that young plants contain relatively low levels of solasodine. Around the middle of summer a sudden burst of alkaloid synthesis begins, with a maximum concentration reported during the period of mass flowering (in Europe). In autumn, there is a slow decrease in solasodine concentrations. These figures are subject to considerable fluctuation according to the ratio of young to old leaves, since the former contain higher concentrations. Even when leaf maturity is taken into account, there is an overall decrease in solasodine concentration at the end of the growing season (Lancaster and Mann, 1975). This drop in concentration has been ascribed to lower temperatures rather than to internal physiological changes in the plants (Marav’eva et al., 1969). When plants were covered with transparent plastic film that raised the mean air temperatures by 6” or 7”C, solasodine concentrations was raised 5-6%. The autumnal decrease in solasodine concentrations could be stopped or reversed by the plastic film (Bernath and Foldesi, 1974). The opposite effect of warmer temperatures was found, however, in a growth chamber experiment (Mann et al., 1978). At higher temperatures total vegetative growth was improved; total solasodine contents were not much altered, compared with those at cooler growing conditions, so overall solasodine concentrations tended to fall. Aslanov and Ismailov (1971) reported elevated “amides” at 40°C, compared to those at 25”-32°C. The latter range was the highest tested by Mann et al. It is possible that at 40°C the plants were subject to drought stress. Severe drought stress increased solasodine concentrations but lowered total yields in the aforementioned growth chamber study (Mann et al., 1978). This would seem to confirm two published reports in which prolonged drought increased alkaloid concentration (Balcar-Skrzydlendsi and Zalecka, 1964a; Sinicin, 1963). A small field study in New Zealand, where stress was mild, did not confirm any higher concentrations (Mann et al., 1978). A remarkable example of temperature sensitivity is claimed by BalcarZkrzydlewska and Zalecka (1964b). Solasodine concentrations rose during the day and decreased at night. This phenomenon was noted during one year’s testing but not during another. Experience in our laboratory suggests that such great sampling error exists in poroporo that exceedingly careful statistical workup is needed for this type of study. One would in fact expect lower alkaloid concentrations at the end of the day if sufficient starch has accumulated to dilute out a more stable pool of alkaloid. Several attempts have been made to increase solasodine yields by chemical

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treatment of poroporo. Several combinations of gibberellic acid with CCC were tested by El-Antably er u f . (1975). The results were mixed, except that all gibberellic acid treatments decreased dry matter production relative to that in controls. The incorporation of labeled precursors into potato sprout glycoalkaloids was reduced by aminoside (Alar), ethephon (Ethrel), and telone (Jadhav er a f . , 1973). Field trials with aminoside and ethephon, however, did not show any reduction in solasodine concentration of either poroporo species (Mann and Lancaster, 1976). In the latter study, twenty growth regulators and herbicides were tested. A number lowered solasodine concentrations, but none succeeded in raising it. One report (Shokova and Paravyan, 1969) claimed improved solasodine concentrations by spraying S . luciniarum leaves with 0.001% nicotinic acid. Confirmation of this finding would be very desirable. Diseases and pests can be quite destructive. In Europe the Colorado beetle (Leprinorursa decemfineata) is the main pest (Studzinki and Mikolajewica, 1975). This is fortunately absent in New Zealand. A significant New Zealand problem is the eggplant caterpillar (Scefoides cordalis), which acts as a stem borer. It is controlled with lindane emulsion. Foldesi and Svab (1964) also reported minor problems with attacks on leaves by aphis, colembolae (Phyfforretra spp.), and snout weevil (Pussafidium maxiflosum F.), known in New Zealand as the green vegetable weevil. Root systems were attacked by ants, grass grubs (Mefolontha spp.), black cutworms (Agroris spp.), and wire worms (Agriores spp.). Phytophthora late blight is the main microbiological problem, with five types of virus diseases also known. Thomson (1976b) has found cucumber mosaic virus and potato virus Y common in New Zealand S . faciniatum. A recent finding is that root-knot nematode (Mefoidogynehapfa)can be a very important pest (F. Wood, unpublished data). Infestation may be widespread without any obvious symptom's. The nematode has a wide host range, including clovers, S . nigrum, potatoes, and tomatoes. The proper timing for harvesting is vexing. As the season wears on, total solasodine concentration tends to drop, but total dry matter (mostly of stems) and total solasodine per hectare increase, except in late autumn. Higher solasodine concentrations are desirable to minimize extraction costs, but this can involve multiple cutting. Uramowa (1965) showed that cuts could be made at 35- to 45-day intervals, obtaining higher solasodine concentrations but with total alkaloid production not quite as high as frDm a single late harvest. The extra costs of multiple harvesting then have to be balanced against the higher concentration of alkaloid. If S . aviculare is to be grown as a perennial crop, then multiple cuttings are obviously necessary, if only to prevent excessive formation of woody stem tissue. Against the cost of harvesting, savings in planting costs by use of a perennial system can be balanced.

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235

To a large extent, leaves provide the bulk of solasodine formed per hectare, but significant quantities are also found in berries. Solasodine concentration in S. laciniaturn berries is two- or threefold higher than in leaves. Since this can raise the overall concentration significantly, Hungarian workers have placed much emphasis on the factors affecting berry production. Solanum laciniatum flowering is not under photoperiodic control (Baylis, 1968). The species may, therefore, be thermoperiodic rather than photoperiodic. In Hungary, cool, rainy conditions after flowering led to early fruit abortion and strong vegetative growth. On the other hand, dry, warm periods after flowering were well suited to fruit production. Changes in mean temperatures of 1" or 2°C had significant effects on fruit production (Foldesi and Bernath, 1968; Bernath and Foldesi, 1969; Bernath, 1970, 1971). Foldesi et al. (1969) suggested that, over a reasonable range of weather conditions, total solasodine production from a given land area may be quite constant, although its proportion in the leaves and fruits may vary considerably. Between 30 and 53% of solasodine was in fruit, 46-57% in leaves, with total yields in Hungary of up to 55 kg of solasodine per hectare. In some years few berries were produced, but luxuriant leaf growth compensated for this fact. In one year, where drought was a problem, total yield was only 18.6 kg per solasodine per hectare, but 75% of that yield was accounted for in the fruit.

D. HARVESTING

Details on commercial harvest methods are hard to obtain. Where labor costs are not significant, hand picking of leaves and fruits can be carried out, with the advantage that nearly valueless stems are eliminated right at the beginning. Machine cutting is common, however, with the slight problem that a large proportion of stems are included. Very young stems contain solasodine in the thin green cortex (Moskaleva and Goncharova, 1963). The main difficulty with inclusion of stems in the harvest, aside from their bulk, is that, if a machine drying operation is to follow, up to half the energy needed for drying is spent in removing moisture from worthless stems. A distracting but probably not serious problem with stems is that, when harvested material is piled into trucks or trailers, the weight of plant material forces a great deal of liquid out. This loss of liquid suggests at first that a great deal of solasodine glycoalkaloid is being wasted, but in fact the origin from stem juice means that only negligible quantities of solasodine are lost. There is general agreement that, if leaves are kept in piles with poor air movement and possible self-heating, significant solasodine losses will occur through enzymatic or microbiological processes (Panina et a l . , 1974). On the other hand, a number of Russian publications have appeared to suggest

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that postharvest increases of solasodine content can be obtained. Labeled mevalonic acid can be incorporated into solasodine by excised leaves. Conversion to solasodine was 4% in leaves kept supplied with water, and 4.4-5.4% in wilted leaves (Guseva et a!., 1973a,b). In another study, drying at temperatures above 30°C with low humidity and good aeration resulted in 5 4 7 % increases in solasodine (Panina et al., 1974). In the first 24 hours of drying, solamargine increased and solasonine decreased. By 72 hours this pattern had been reversed, with an overall increase of 9-20% total solasodine (Moiseev et al., 1970). It must be pointed out, however, that inspection of the actual data, where the publications are available, suggests quite a wide range of results from year to year and location to location. In any event, the possibility of achieving these slow drying conditions without fermentation does not seem likely with large commercial quantities of poroporo leaves. Even the Russian authors seem to agree that processing of harvested leaves without undue delay is important.

E. PLANT SELECTION AND BREEDING

There is very little evidence that breeding (as contrasted with plant selection) has had much success in improving solasodine production either in higher yields per unit area of land or in higher alkaloid concentrations. The many agronomic factors affecting solasodine concentration make it difficult to identify promising plants as individuals. Attempts to select high alkaloid-producing lines of S . laciniatum have not been very impressive. Baylis (1966) predicted this failure, since he regarded the species as being quite uniform throughout its distribution. Gerasimenko (1971) claimed that the Australian and Tasmanian forms of the species had higher solasodine concentrations than, for instance, the New Zealand forms. On the other hand, Matveenko et al. (1975) found that all forms of S. laciniatum were much the same, with 1.5-1.8% solasodine. Moreover, selection of parents with high levels did not give consistent elevations in alkaloid concentrations in the next generation. Even more discouraging results were obtained in Hungary (Szabady and Tetenyi, 1974). For three years, the highest yielding plants of gamma-irradiated plants were selected for seed production. Unselected controls were also carried along. In two years out of three, the mean solasodine concentrations in the selections were somewhat lower than in the unselected controls. There were large differences in year-to-year levels of solasodine production, but both selected and unselected lines showed essentially identical responses. The foregoing statements do not mean that any randomly selected wild line of poroporo can be used commercially. The ability of a given line to prosper under agronomic conditions can vary enormously. Under perennial cultivation, in particular, up to 95% loss of certain lines of plants can occur (Palmer, 1977). It is

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not clear whether these losses are caused by disease or inability to withstand harvesting. There is one recent publication regarding selection of S. aviculare (Komeva and Matveenko, 1975). This species is of interest only in regions where winters are sufficiently mild to permit its cultivation as a perennial. Under these conditions, S. aviculare offers the advantage of vegetation with solasodine concentrations of 2% or better, although total dry matter production per hectare is less than forS. laciniatum. Korneva and Matveenko (1975) distinguished five botanical varieties of S. aviculare, with solasodine concentrations ranging from a low of 1.5% to a high of 2.6%. They also reported that S. laciniatum ranged from 1.4 to 6% solasodine. (No S. laciniatum having 6% solasodine has ever been analyzed in New Zealand, to my knowledge.) It is an obvious approach to try to cross S. laciniatum with S . aviculare in an effort to obtain the high dry-matter production of the former together with the higher solasodine concentrations of the latter. Baylis (1963) showed that direct crosses were not successful. This was anticipated, since the basic chromosome number of S. aviculare is 23, whereas that of S. laciniatum is 46. Appropriate juggling with chromosome numbers is required. It seems that tetraploids of S. aviculare somewhat resemble those of S. laciniatum (Korneva and Balakhanova, 1973). Such autotetraploids could be crossed with S. laciniarum. The second generation of such hybrids showed segregation of the alkaloid-producing traits, since the solasodine concentrations ranged from 0.62 to 2.8% (Matveenkoet al., 1975). Alternatively, haploids of S. laciniatum can be made. Alekseenko et al. (1976b) indicate that the chloroplast number guard cells of the second and third true leaves can be used to distinguish between haploids and diploids. These crosses between S. aviculare and S . laciniatum may result eventually in considerable improvement in the economics of solasodine production. It will be necessary to ensure that the virus resistance of S. aviculare is maintained in the ultimate selections. Growth chamber studies (Mann et al., 1978) showed that S. aviculare grew slower than did S. laciniatum even in warmer conditions and was more susceptible to water stress than was S. laciniatum. It seems possible that only its disease resistance is responsible for the survival of S. aviculare.

F. YIELDS

It will not be surprising that figures for yields of solasodine are, in general, either unreliable estimates from small-plot tests, or else cannot be published here because they are proprietary and confidential. In the early 1960s, Hungarian workers obtained 10-15 kg/ha from S. laciniatum, while Russian yields were claimed to be threefold greater (Mathe and

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D. MANN

Foldesi, 1965). In some of the trials described by Foldesi et al. (1969) yields were up to 65 kg/ha. Other Hungarian reports are up to 80 kg/ha. Solanum laciniatum trials in the South Island of New Zealand averaged about 70 kg/ha-after elimination of the numerous tests in which germination, establishment, or growth were very poor. The maximum yield in Canterbury was 96.6 kg/ha in a sheltered location with good soil. One trial in Central Otago (a region with warmer summers and milder winds then most of the South Island) produced 180 kg/ha in a favorable year. Small-plots trials of S. aviculare in the Auckland region gave estimates of 89-197 kgha the first year, and 190-356 kgha subsequently (Palmer, 1977). These results may be unduly high. A small-plot trial in Gisborne suggested S. aviculare yields of at least 100 kg/ha in the first year. Figures for S. khasianum yields are even sketchier. Saini et al. (1965) estimated a potential of 40 kg/ha, but without actual trials. In Auckland, New Zealand, an estimate of 431 kglha was obtained (Palmer, 1977), but this again seems very high. Although S. aculeatissimum (mostly as S . xanthocarpum) was mooted as a potential solasodine plant, less than 4 kg/ha was obtained in France (Verbist and Monnet, 1975a). Fruit yields in Nepal are higher, but solasodine concentration was lower. VII. Medical Aspects of the Glycoalkaloids

Most of the interest in solasodine-bearing plants is due to their potential conversion of solasodine to synthetic drugs. There is, however, some biological activity of the original glycosides as such. Poropora leaves were used by the New Zealand Maoris to make poultices for skin disorders. Partial confirmation of this use comes from Kamyszek (1974), who successfully treated a fungal skin disease in rodents, Trichophyton mentagrophytes, with an aerosol preparation of solasonine and solamargine mixture. Later, a related dermatomycosis in cattle, caused by Trichophyton verrucoccum, was cured with preparations of 21% crude poroporo glycoalkaloids, smeared three to nine times on the affected areas (Kamyszek et a l . , 1975). Veterinary opinion seems to be that there are many possible remedies for this disease. Oral ingestion of poroporo glycosides is not generally regarded as dangerous, since poor absorption and rapid detoxification is thought to limit the hazard (Connor, 1977). The glycosides are cholinesteraseinhibitors. Symptoms of acute toxicity are depressed nervous system activity, followed by failure of the heart and of the respiratory system. A study of cumulative properties (Shashkinaet al., 1974) showed that oral ingestion by rodents of relatively low doses (between

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1.25% and 10% of the L B O )resulted in changes in glycogen content of the liver and in increased number of leukocytes in the blood. Dystrophic and necrobiotic changes were found in the liver, kidneys, and brain. (The extent and seriousness of these changes are not described in the abstract.) The LDsn for intraperitoneal injection ranged from 103 mg/kg for guinea pigs to 898 mg/kg for mice. For comparison, oral LBO of aspirin is approximately 350 mg/kg in humans. There is a possibility that the solasodine glycoalkaloids might directly interfere with reproduction. A high-solasodine strain of S . incanum first came to the attention of Ammal and Viswanathan (1974) when local tribes were found to be using the fruit for birth-control purposes. There is no evidence to show whether solasodine or some other compound in the fruit was acting as a contraceptive or abortifacient agent, nor, for that matter, whether the use of the fruit for this purpose was really effective. On the other hand, subsequent studies (Keeler et al., 1976; Young et a l . , 1976) suggest that solasodine aglycone might damage fetuses if given at sufficiently high doses. Golden hamsters, pregnant for 7 or 8 days (at the primitive streakheural plate stages) were force-fed aqueous suspensions of solasodine at rates from 1184 to 1628 mg/kg or else tomatidine or diosgenin at 2664 mg/kg. Out of 115 solasodine-treated hamsters, 10 died from apparent overdosage and 21 were found to have totally resorbed their litters by the next week. There was one overdose death from diosgenin feeding, and none from tomatidine or water control. Resorption incidence was also very low with tomatidine or diosgenin feeding. There were approximately 10 offspring per litter in the control and tomatidine- or diosgenin-treated dams, but litter size after solasodine treatment ranged from 3 to 10, with an average of 1.6 resorptions per viable litter. More disturbing still, between 5 and 15% of the offspring from solasodinetreated dams had teratogenic symptoms such as spina bifida and exencephaly. In this type of test, solanidine is not teratogenic. On the other hand, even though the doses administered are extremely high, corresponding to more than 60 gm of solasodine per human female, there is a suggestion here that solasodineproducing factories should take care to restrict exposure of women of childbearing age to possible ingestion of the alkaloid. About the only risky situation would be during the handling or grinding of dry leaf material. This produces a dust with quite an unpleasant acrid odor, and it is most unlikely that any one would remain in contact with it. Proper air filtering is obviously called for, however, if Solanum leaf dust is being produced. Finally, mention must be made of solaplumbin, a solasodine derivative claimed to have anticancer activity (Singh et a l . , 1974). The sugar linkages to solasodine are unusual in this compound, which is derived from a Nicotiana species, so that there is no implication of any such favorable effects from solasonine or solamargine.

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Although details are shrouded by commercial secrecy, there is little doubt that production of solasodine is under way in a number of locations throughout the world. In the long term, solasodine or some other replacement for diosgenin must become of increasing importance to the pharmaceutical industry. There is, however, a closer relationship between the farmer and the drug producer than is usual for other crops, since either the solasodine-bearing plants are grown under contract, or else the drug company itself has taken responsibility for cultivation of the crop. Freelance production of these plants would be a dubious farming practice; we are not yet at the stage of having “solasodine futures” traded on the grain exchange. REFERENCES Alekseenko, L. F., Laptev, Yu. P., and Shain, S. S. 1976a. Genetika 12, 50-58. Alekseenko, L. F., Shain, S. S.,and Laptev, Yu. P. 1976b. Eesti NSY T e d Akad. Toim.. Biol. 25, 157-159; Biol. Abstr. 63, 27447 (1900). Alekseenko, L . F., Shain, S. S.,and Laptev, Yu. P. 1977. Ref. Zh. 11, 55 and 255., Plant Breed. Abstr. 47, 4545. (1900). Ammal, E. K. J . , and Viswanathan, T. V. 1974. Curr. Sci. 43, 378. Ananichev, A. V., and Loshkarev, P. M. 1969. Tr. Vses. Nauchno Issled. Inst. Lek. Rast. 15, 487; Chem. Abstr. 75, 52849b (1972). Andreeva, L. G., and Romanchuk, M. A. 1970. Khim.-Farm. Zh. 4, 43-45; Chem. Abstr. 73, 132298 (1970). Anonymous. 1977. Chem. Week June 29, 49-50. Applezweig, N. 1962. “Steroid Drugs.” McGraw-Hill, New York. Applezweig, N. 1969. Chem. Week May 17, 58-72. Aslanov, S. M. 1975. Khim. Prir. Soedin. 2, 264-265. Aslanov, S. M., and Ismailov, N. M. 1971. Rastit Syr’e Azerb. pp. 96-104. Balcar, E., and Zalecka, M. 1962. B i d . Inst. Rod. Lecz. 8, 90-77; Chem. Abstr. 59, 2593e (1963). Balcar-Skrzydlewska. E., and Zalecka, M. 1964a. B i d . Inst. R o d . L e a . 10, 159-171; Hort. Abstr. 36, 5266 (1966). Balcar-Skrzydlewska, E., and Zalecka, M. 1964b. B i d . Inst. R o d . Lecz. 10, 172-186 (1964); Chem. Absrr. 63, 16767 (1965). Baylis, G. T. S. 1954. Trans. R . SOC. N.Z. 82, 639-643. Baylis, G. T. S. 1963. Aust. J . Bot. 11, 168-177. Baylis, G. T. S. 1966. Herba Hung. 5, 283-287. Baylis, G. T. S. 1968. N.Z.J . Bot. 6, 221-225. Bell, R. C., and Briggs, L. H. 1942. J. Chem. SOC. 145, 1-2. Bell, T. C., Briggs, L. H., and Carroll, J. J . 1942. J . Chem. SOC.145, 12-15. Bernath, J . 1970. Herba Hung. 9, 35-47. Bernath, J . 1971. Herba Hung. 10, 21-32. Bernath, J . , and Foldesi, D. 1969. Herba Hung. 8, 107-112. Bernath, J . , and Foldesi, D. 1971. Herba Hung. 11, 55-66. Bemath, J . , and Foldesi, D. 1972. Herba Hung. 11, 61-71. Bernath, J . , and Foldesi, D. 1974. Herba Hung. 13, 37-43.

PRODUCTION OF SOLASODINE

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Bernath, J., and Tetenyi, P. 1973. Herba Hung. 12, 17-28. Bernath, J., Tetenyi, P., Horvath, I., and Zambo, 1. 1976. Herba Hung. 15, 43-53. Bhatt, B. 1975. Curr. Sci. 44, 677-678. Bhatnagar, J. K. 1974. Lloydia 37, 318. Birner, J. 1969. J . Pharm. Sci. 58, 258-259. Bite. P., and Shabana, M. M. 1972. Acta Chim. Acad. Sci. Hung. 37, 361-362. Eite, P., Shabana, M. M., Jokay, L., and Pongracz-Sterk, L. 1970a. Acta Chim. Acad. Sci. Hung. 63, 343-352. Bite, P., Mago-Karacsony, E., Rettegi, T., and Uskert, A. 1970b. Acta Chim. Acad. Sci. Hung. 64, 199-201. Boll, P. M. 1962. Acta Chem. Scand. 16, 1819-1820. Briggs, L. H., and Brooker, G. 1953. J . Chem. Soc. pp. 2833-2834. Briggs. L. H., and Brooker, E. G. 1958. J. Chem. Soc. pp. 1419-1421. Briggs. L. H.,and Cambie, R. C. 1958. J. Chem. SOC. pp. 1422-1425. Briggs, L. H., Newbold, R. B., and Stace, N . E. 1942. J. Chem. SOC. pp. 2-12. Briggs, L. H., Brooker, E. G., Harvey, W. E., and Odell, A. L. 1952. J. Chem. Soc. pp. 35873591. Briggs, L. H., Cambie, R. C., and Hoare, J. L. 1961. J. Chem. Soc. pp. 46454649, Briggs, L. H., Cambie, R. C., and Hoare, J. L. 1963. J. Chem. SOC. pp. 2848-2853. Briggs, L. H., Cambie. R. C., and Hyslop. D. M. 1975. J . Chem. SOC.. Perkin Trans. I 23, 2455-2457. Brutko, L. I. 1966. Khim. Prir. Soedin. 2, 442-443. Chem. Abstr. 66, 98454 (1900). Bulfin, M. J. A. 1969. Can. But. Soc. J. 2, 13-14. Chakraverty, R. K., and Basu, 1973. Sci. Cult. 39, 134; Hortic. Abstr. 44, 2759 (1974). Connor, H. E. 1977. “Poisonous Plants of New Zealand,” Bull. 99. DSIR, Wellington, New Zealand. Coune, C., and Denoel, A. 1975. Plant. Med. Phytorher. 9, 14-20. Crush, J. R. 1973. N . Z . J. Exp. Agric. 1, 187-190. Datta, A , , Pal, G. D., Bhattacharya, P., and Chakraverty, R. E. 1973. Bull. Bor. Sum. India 15, 177-181. Davtyan, G. S., and Babakhanyan, M. A. 1974. Biol. Z h . Arm. 27, 14-18. Djerassi, C. 1966. Science 151, 1055-1061. Dopke. W., Kimenex, V . , and Hess, U. 1976. Pharmazie 31, 488. El-Antably, H. M. M., Ahrned, S. S., and Eid, N. M. A. 1975. Pharmazie 30, 397-399. Fawkner, J. J. 1974. Int. Plant Propagation SOC. Proc. 24, 331-334. Fayez, M. B. E., and Saleh, A. A. 1967a. Phytochemistry 6, 433436. Fayez, M. B. E. and Saleh, A. A. 1967b. Planta Med. 15, 430433. Floss, H. G., Robbers, J. E., and Heinstein, P. F. 1974. I n “Metabolism and Regulation of Secondary Plant Products” (V. 0. Runeckles and E. E. Conn, eds.), pp. 141-178. Academic Press, New York. Foldesi, D. 1964. Herbu Hung. 3, 235-253. Foldesi, D. 1965. Hcrba Hung. 4, 63-73. Foldesi, D.. and Bernath, J . 1968. Herba Hung. 7, 105-1 19. Foldesi, D., and Svab, J. 1964. Herba Hung. 3, 439. Foldesi, D., and Svab. J. 1969. Herba Hung. 8, 81-92. Foldesi, D., Lang, T., and Kovacs, T. 1969. Herba Hung. 8, 49-61. Fryer, R. F. 1972. Proc. Agron. SOC. N . Z . 2 , 73-84. Gerasimenko, 1. I. 1971. Rastit. Resur. 7, 363-371. Golez, L. 1964. Herba Pol. 10, 187-192. Guseva, A. R., and Paseshnichenko, V. A. 1958. Biochemistry (Engl. Transl.) 23, 525-527.

242

JAY D. MANN

Guseva, A. R., and Paseshnichenko, V. A. 1962.Biochemisrry (Engl. Transl.) 27, 721-726. Guseva, A. R., Paseshnichenko, V. A,, and Borikhina, M. G. 1961.Biochemisrry (Engl. Transl.) 26, 631-635. Guseva, A. R., Paseshnichenko, V. A., Borikhina, M. G., and Moiseev, R. K. 1965.Biochemistry (Engl. Transl.) 30, 224-228. Guseva, A. R.,Paseshnichenko, V. A., and Borikhina, M. G. 1973a.Prikl. Biokhim. Mikrobiol. 9, 117-1 19;Biol. Absrr. 56, 5783 (1973). Guseva, A. R., Paseshnichenko, V. A., and Borikhina, M. G. 1973b.Prikl. Biokhim. Mikrobiol. 9, 764-767. Hardman, R., and Williams, T. G. 1976.PIanra Med. 29, 61-71. Harrison, D. M. 1976.Alkaloids (London) 6, 285-295. Heble, M. R., Narayanaswami, S., and Chandha, M. S. 1968.Natunvissenschafren 7, 350. Heble, M. R., Narayanaswami, S., and Chandha, M. S. 1971.Phyrochemistry 10, 2393-2394. Heftmann, E., and Schwimmer, S. 1972.Phyrochemisrry 11, 2783-2787. Heftmann, E.,Lieber, E. R., and Bennett, R. D. 1967.Phyrochemisrry 6, 225-229. Herb, S. F., Fitzpatrick, T. J., and Osman, S. F. 1975.J . Agric. Food Chem. 23, 520-523. Herbert, R. B. 1973.Alkaloids (London) 3, 279-291. Herbert, R. B. 1974.Alkaloids (London) 4, 383-394. Herbert, R. B. 1975.Alkaloids (London) 5, 256-260. Hunter, I. R., Walden, M. K., Wagner, J. R.,and Heftman, E. 1976.J. Chromarogr. 119,223-226. Imre, M., Dezso, F., Zoltanne, S., Sandome, S., and Peter, T. 1964.Herba Hung. 3, 295-305. Jadhav, S. J., Salunkhe, D. K., Wyse, R. E., and Alvi, R. R. 1973.J. Food Sci. 38, 435455. Jain, S. C., and Sharma, G. L. 1977.Planfa Med. 31, 212-213. Kadkade, P. G., and Rolz, C. 1977.Lloydia 40, 217. Kammathy, R. V., Chaudhuri, Rai, H. N., and Kayal, R. N. 1971.Bull. Bor. Surv. Indian 12, 224-235. Kamyszek, F. 1974.Zwierzera Lab. 11, 57-64.Biol. Absf. 61, 8739 (1976). Kamyszek, F., Dudzinski, A., and Cogolewski, L. 1975.Herba Pol. 21, 79-87. Kaneko, K., Tanaka, M. W., and Mitsuhashi, H. 1976.Phyrochemisrry 15, 1391-93. Kaul, B. L., and Zutshi, U. 1973.Indian J . Phurm. 35, 94-96;Hortic. Absrr. 44, 3461 (1974). Keeler, R. F., Young, S., and Brown, D. 1976.Res. Commun. Chem. Parhol. Pharmacol. 13, 723-730. Khanna, K. R., and Murty, A. S. 1972.Planfa Med. 21, 182-187. Khanna, P., and Manot, S. K. 1976.Indian J. Exp. Biol. 14, 631-633. Kiselev, V. P., and Stotskii, S. K. 1975.Izv. Akad. Nauk Tadzh. SSR, Old. Biol. Nauk 2, 93-95; Horric. Absrr. 47, 86 (1977). Komeva, E. I., and Balakhanova, F. G. 1973.Generiku 9, 1390-1396;Biores Index 12, 16965 ( 1 976). Komeva, E. I., and Matveenko, L. F. 1975.Ref. Zh. 11, 55-259;Plant Breed. Absrr. 47, 4551 ( 1 977). Krishnappa, D.G., and Chennaveeraiah, M. S. 1975.Proc.IndianSci. Congr.. 62nd, IY75 p. 121. Kuhn, R.,and Low, I. 1955. Chem. Ber. 88, 289-294. Kvitaishvili, L. V. 1967.Soobshch. Akad. Nauk Gruz. SSR 47, 607-612;Biol. Absrr. 49, 118489 (1968). Lakova, M. T.,Zelinskaya, L. G., Mikhailova, I. I., and Rosanov, L. G. 1975.Khim-Farm. Zh. 9, 24-27. Lancaster, J. E., and Mann. J. D. 1975.N.Z. J . Agric. Res. 18, 139-144. Lancaster, J. E., Mann, J. D., and Blyth, K. E. 1977.N . 2. J . Agric. Res. 20, 395-399. Lewis, D. C., and Liljegren, D. R. 1970.Phytochemistry 9, 2193-2195.

PRODUCTION O F SOLASODINE

243

Liljegren, D. R. 1971. Phyrochemisrry 10, 3061-3064. Lohen, B., and Sollins, I. V. 1970. U.S. Patent 3,510,400. Maiti, P. C., Mookerjae, S.,Mathew, R., and Henry, A. V. 1964. Curr. Sci. 33, 730. Mann, J . D., and Lancaster, J . E. 1976. N.Z. J . Exp. Agric. 4, 347-350. Mann, J. D. et 01. 1978. In preparation. Marav’eva, V. I., Kondratenko, P. T., and Brink, N. P. 1969.Rasr. Resur. 5 , 187-190; Chem. Abst. 72, 714 (1970). Martin, F. W . 1972. Planr Foods Hum. Nurr. 2, 139-143. Martynov, Yu. F., and Sklizov, V. G. 1974. Farmarsi.ya (Moscow) 23, 15-20. Massey, J . H. 1967. Univ. Ga., Res. Bull. 7. Mathe, I., and Foldesi, D. 1965. ”The medicinal “Csucsor” Solanum laciniarum Ait,” Cultivated Flora of Hungary, Vol. 5 , Booklet 17. Academic Edition, Budapest. MathC, I., and Mathe, I., Jr. 1972. Herba Hung. 11, 5-12. Mathe, I., Foldesi. D., Szabo. E., and Tetenyi, P . 1964. Herba Hung. 3, 305. Matveenko, L. F., Korneva, E. I., and Kondratenko, T. P. T. 1975. Dokl. Vses. Akad. Skh. Nauk 1, 12., Biol. Absrr. 61, 56 (1973). Moiseev, R. K., Klyphev, L. K. and Guseva, A. R. 1970. Tr. Inst. Bot.. Akad. Nauk Kaz. SSR 28, 215-225; Chem. Absrr. 73, 127830 (1970). Moskaleva, V. E., and Goncharova, E. V. 1963. Bot. Zh. (Leningrad) 48, 1208-1210; Hortic. Abstr. 34, 5427 (1964). Moursi, M. A,. and Ahmed, S . S . 1973a. Pharmazie 28, 58-61. Moursi, M. A,, and Ahmed, S. S . 1973b. Pharmazie 28, 62-64. Murav’eva, V. I., Kondratenko, P. T., and Brink, N. P. 1969. Rastir. Resur. 5 , 187-190; Chem. Absrr. 72, 714 (1970). Murty, A. S. 1976. Curr. Sci. 45, 314. Murty, U. R., and Abraham, K. 1975. Cum. Sci. 19, 718-719. Naqvi, S. Q. A , , and Mahmood, K. 1975. Proc. Indian Sci. Congr., 62nd, I975 pp. 59-60. Novruzov, E. N., and Aslanov, S. M. 1975. Izv. Akad. Nauk Az. SSR, Ser. Biol. Nauk 2, 33-36; Biol. Absrr. 61, 30750 (1976). Nowacki, E., Jurzysta, M., and Gorski, P. 1975. Bull. Acad. Pol. Sci. 23, 219-225. Palmer, J . A. 1977. N.Z. J. Horric. 1, 18-21. Panina, V. V., and Madaeva, 0. S. 1967. Khim.-Farm.Zh. 1, 37-38; Biol. Absrr. 50,4596 (1969). Panina, V. V., Dem’yanova, G. M., Kuzovkova, R. I., Strelkovich, R . P., Denisova, G. A., and Avilova, 0. P . 1974. Rastir. Resur. 10, 386-389. Panina, V. V., Barashkov, S. G.. and Dem’yanova, G. M. 1975a. Khim.-Farm. Zh. 9, 58-60; Chem. Absrr. 84, 88804 (1976). Panina, V. V., Copobetskii, L. Sh., Dem’yanova, G. M.. and Babanova, A. V. 1975b. Khim.Farm. Zh. 9, 107-108. Parimoo, P., and Baruah, R . N. 1975. J . Am. Oil. Chem. SOC.52, 357. Perez-Medina, L. A,, Travecedo, E., and Devia, J. E. 1964. Planta Med. 4, 478-487. Petrotschenko, E. I. 1957. Abh. Dsch. Akad. Wiss. Berlin, Kl. Chem., Geol. Biol. pp. 158-165. Porter, N. G., and Gilmore, H. M. 1976. N.Z. J. Exp. Agric. 4, 343-345. Pun, R. K., and Bhatnagar, J. B. 1975. Phyrochemistry 14, 2096. Ramaswamy, N . K., Behere, A. G., and Nair, P. M. 1976. Eur. J . Biochem. 67, 275-282. Rangaraju, R., and Chenula, V. V. 1975. Acfa Phytoparhol. Acad. Sci. Hung. 10, 237-243. Rasmussen, H.B., and Boll, P. M. 1958. Acra Chem. Scand. 12, 802-806. Retezeanu, M., and Constantinescu, C. 1963.Lucr. Grad. Bot. Eucuresti 2, 677-681;Horric. Absrr. 36, 1635 (1966). Ripperger, H., Moritz ,W. M., and Schreiber, K. 1971. Phytochemisrry 10, 2699-2704.

244

JAY D. MANN

Rizk, A. M., and Abou-Zied, E. N. 1970. Planta Med. 18, 347-349. Roddick, J . G. 1974. Phytochemistry 13, 9-25. Roddick, J . G. 1976. Phytochemisrry 15, 475-477. Saber, A. H., Balbaa, S. I., and Zaky, A. Y. 1965. Planta Med. 13, 104-1 16. Saini, A. D. 1966. Indian J . Plant Physiol. 9, 600. Saini, A. D., and Biswas, R. C. 1967. lndiun J . Plant Physiol. 10, 36-43. Saini, A. D., Mukherjee, M . , and Biswas, R. C. 1965. Indian J . Plant Physiol. 8, 102-1 12. Saleh, A. A. 1974. Planta Mrd. 26, 4 0 4 4 . Saleh, M. 1973. Planta Med. 23, 377-378. Saleh, M., and Ahmed, S. S . 1973. Qual. Plant. Muter. Veg. 22, 133-136. Sastry, K. S., Sastry, K. S. M., and Singh, S. J. 1974. Indian Phytopathol. 27, 316-321. Sastry, K . S. M., Pandotra, V. R., Thakur, R. N., and Gupta, J . H. 1973. Mysore J. Agric. Sci. 7, 192- 197. Schreiber, K. 1958. PIanra Med. 6, 435-439. Schreiber, K . 1963. Kulturpflanze 11, 451-501. Schreiber. K. 1968. In “The Alkaloids Chemistry and Physiology” (R. M. F. Manski. Ed.).10, 1-192. Schreiber, K. 1974. Biochem. SOC. Trans. 2, 1-15. Shashkina, L.F., Ryndina, S.F., and Starkov, M. V. 1974. Farmakol. Toksikol. 37, 719-722;BioI. Abstr. 60, 5745 (1975). Shokova, R. I., and Paravyan, A. V. 1969. Tr. Bor. Sadov. Akad. Nauk Kaz. SSR 11, 188-25. Singh, S . , Kanna, N. M., and Dhar, M. M. 1974. Phytochemistry 15, 2020-2022. Sinicin, G.S. 1963. Tr. Inst. Bot., Akad. Nauk Kaz. SSR 17, 153-158;Hort. Abstr. 35, 6371 (1965). Sofowora, E. A., and Hardman, R. 1974. Planta Med. 25, 22-27. S t a y , F., and Kybal, J . 1961. Tagungsber.. Bot. Akad. Landwirtschaftswiss. Berlin 27, 193-198; Chem. Abstr. 60, 16213 (1964). Studzinki, D. D., and Mikolajewica, M. 1975. Herba Pol. 21, 210-219; Biol. Absrr. 62, 25007 ( 1976). Sudiatso, I. S., and Wilson, D. R. 1974. N.Z. J . Agric. Res. 17, 4 5 5 4 5 8 . Syhora, K., Cekan, Z., Hennanef, S., and Trojanek, J. 1962. Planta Med. 10, 318-326. Szabady, J . , and Tetenyi. J. 1974. Herba Hung. 13, 45-50. Tashbulatov, A., and Martynov, Yu F. 1973. Ref. Zh. 6, 233-239. Telek, L., Delphin, H., and Cabanillas, E. 1977. Econ. Bot. 31, 120-128. Thomson, A. D. 1976a. Crop. Res. News, Dep. Sci. Ind. Res.. N.Z. 18, 10. Thomson, A. D. 1976b. N . Z . J . Agric. Res. 19, 521-527. Tschesche, R., and Peistert, G. 1975. Phytochemistry 14, 435-438. Tschesche, R., Goossens, R., and Topfer, A. 1976. Phytochemistry 15, 1387-1389. Tupkari, S. V., Saoji, A. N . , and Deshmukh, V. K. 1969. Pluntu Med. 22, 184-187. Upadhyay, D. N . , Shukla, A. K., and Singh, K. K. 1969. Indian J . Pharm. 38, 52-53. Uramowa, B. 1965. Herba Pol. 11, 162-169; Hortic. Abstr. 37, 1583 (1967). Ursua, A., and Cassels. B. K. 1972. Phytochemistry 11, 3548-49. Vagujfalvi, D., Maroti, M., and Tetenyi, P. 1971. Phytochemistry 10, 1389-1390. Valovich, N . A. 1964. Herba Hung. 3, 439. Valovich, N. A. 1965. Med. Prom. SSSR 19, 45-48. Verbist, J . F., and Monnet, R. 1974a. Plant. Med. Phytother. 8, 263-268. Verbist, J . F . , and Monnet, R. 1974b. Plant. Med. Phytother. 8, 269-280. Verbist, J . F., and Monnet, R. 1975a. Plant. Med. Phytother. 9, 59-68. Verbist, J . F., and Monnet, R. 1975b. Plant. Med. Phytorher. 9, 69-71. Verbist, J. F., and Monnet, R. 1976. Plant. Med. Phytother. 10, 54-55. Weston, R. J . 1976. J. Appl. Chem. & Biotechnol. 26, 657-666.

PRODUCTION OF SOLASODINE Willaman, J . J . , and Schubert, B. G . 1961. U . S . , Dep. Agric.. Tech. Bull. 1234. Willuhn, G . 1966. PIunrn Med. 14, 408-420. Willuhn, G . 1967. Plarira Med. 15, 58-73. Willuhn, G. 1969a. Planra Med. 16, 4 6 2 4 6 6 . Willuhn, G. 1969b. Eer. Dtsch. Bot. Ges. 82, 657-663. Young, S . , Keeler, R. F., and Brown, D. 1976. Terarology 13, 41A. Zaitschek. D. V . , and Segal, R . 1972. Lloydia 35, 192.

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ADVANCES IN AGRONOMY, VOL. 30

TECHNICAL CLASSIFICATION SYSTEM FOR SOIL SURVEY INTERPRETATION Lindo J. Bartelli School of Forestry and Wood Products, Michigan Technological University, Houghton, Michigan

I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

........................................ A. Soil Survey Interpretations ............................... B. Objectives and Principles ................................ C. Single and Multi-Taxa Soil Maps. ...................................... Systems for Organizing Soil Surfey Interpretations ............................

11. Principles of Technical Classification

111.

IV.

V.

VI.

VII.

A. Food and Agriculture-United Nations System B. Soil Conservation Service USDA-Land Use C. U. S. Forest Service-Land Systems Inventory ........................... D. United Kingdom-Land Use Capability Classification Systems . . . . . . . . . . . . . . . Plant Suitability Evaluation Systems ........................................ A. Woodland Suitability Groups . . .............................. B. Range Sites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ...... C. Soil Groupings for Wildlife . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Systems To Evaluate Engineering Properties.. ................................ A. The American Association of State Highways and Transportation Officials System B. The Unified Soil Classification System ..................... ....... C. Federal Aviation Agency Soil Classification System ....................... The Application of Technical Classification to Soil Surveys ..................... A. Engineering Interpretations . . . . . . . . . . . . . . . . B. Plant-Soil Interpretations ................................ C. Soil Survey Interpretations for Land Use Suita Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References ................................. ...

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287 288

I. Introduction

The objective of soil surveys is to provide reliable information on which to base some sort of land management or land treatment program that is in balance with and in close harmony with the physical nature of an area and still give an accurate geographic expression of the physical characteristics of the area (Bartelli, 1962). Delineations on soil maps are named in accordance with a ‘‘natural’’ system of soil classification. Soil taxonomy (U.S.Department of Agriculture, IFormerly Director of Soil Survey Interpretation Division, Soil Conservation Service, U.S. Department of Agriculture, Washington, D.C. 247 Copyright 0 1978 by Academic Press. Inc. All rights of reproduction in any form i ~ e ~ e d .

ISBN 0-12-0007304

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1975) has been developed to serve in the interpretation of soil surveys. It is a multicategorical system, with taxa representing real, natural bodies of soil. As was pointed out by Mitchell (1973), a natural classification system will seek to emphasize genesis through morphological indications. The taxa in soil taxonomy are defined in terms of soil properties. Differentiae used in soil taxonomy can be observed in the field or can be inferred either from other properties that are observable or measurable, or from the combined data of soil science and other disciplines. Soil properties that are important to plant growth, to engineering behavior, to soil hydraulics, or to the reaction between municipal and industrial wastes and the soil are considered important in soil surveys and are used as differentiae in soil taxonomy; the primary objective, however, is to group soils of similar genesis. Technical classification schemes, on the other hand, are based on practical ad hoc criteria. Mitchell (1973) refers to these schemes as “artificial. They are usually monocategorical. In a sense, soils are looked at as mere assemblages of natural properties. Technical classification systems provide informative guides for grouping soils identified in soil taxonomy into useful assemblages. The technical systems are limited by the procedure inherent in the system that restricts the number of soil properties. These soil properties must be arbitrarily selected. Once selected, all properties must be regarded as of equal importance. The interpretations are varied. Some of the interpretations being made by the Soil Conservation Service and other users of soil surveys are as follows: ”

(1) The selection of adapted crops.

(2) The yields of adapted crops under varying systems of management. (3) The need for special measures of reclamation. (4) Grazing practices and carrying capacities for livestock on range lands. (5) The need, suitability, and practices required for imgation, in addition to crops that can be grown and yields that may be expected. (6) The need for drainage, and methods of providing it. (7) The hazards of erosion, and methods for preventing it. (8) Adaptability and growth rates of specific species in the management of forests, including regeneration, control of undesirable species, and planting, thinning, and harvesting techniques. (9) Environmental impact studies of any land and water development project. (10) The use of soil to treat waste products. ( 1 I ) The location of roads, airfields, and other urban developments. Technical classification groups soil taxonomic units, but care must be taken not to confuse soil taxonomic units with mapping units. Whereas mapping units contain contrasting inclusions, or are complexes of contrasting soils, ratings of taxonomic units cannot be equated directly with mapping units. The best in-

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terpretations are those made in response to the specific needs of the users of the soil maps. Planning of good soil survey interpretations depends first on a clear understanding of these needs. The legend designed and the intensity of soil mapping must be in harmony with the uses anticipated for the soil survey. This chapter summarizes the principles and procedures of the various interpretations being made of soil surveys. II. Principles of Technical Classification

Technical classification is a scheme for grouping together things that are similar. There may be some question as to what is similar; however, some uniformity can be attained if the properties used to define the groups are well understood. Some of the systems are based on many properties, others are based on a few properties. The land use classification system developed by the Soil Conservation Service (Klingebiel and Montgomery, 1961) is based on many properties. It is general, but very useful for a great variety of purposes dealing with suitability of land for cultivation. In contrast, a classification based on a few properties-grouping soils according to corn yields is an example-may be optimal for comparing soils on a short-time basis, but may not be of much general use. The introduction of new varieties or new cultural practices may change the m a y of soils very quickly. Cline (1949) has pointed out that classifications are “orderly abstracts of knowledge, and of concepts derived from knowledge, both of which are legacies from experiences of the past. Much of the legacy is considered to be fact. Part of the legacy is purely empirical relationships; that is, facts are derived from observation or experiment, not theory. Some theory, however, is used to explain the relationships that occur in nature. Care should be taken not to accept the concepts implicit in a system as fact. Such acceptance can freeze the system to knowledge of the past and restrict the introduction or application of new knowledge or new experiences. Any technical classification system is faced with this hazard. ”

A. SOIL SURVEY INTERPRETATIONS

Early attempts at developing a technical classification system for interpreting soil surveys were centered on characterizing the crop-producing capacity of the soil. Rieken (1963) chose the 1928 Johnson County, Kansas, and the 1941 Jackson County, Iowa, soil survey reports as examples. These early soil surveys were much simpler to interpret than the more recent soil surveys in that few separations were made in a soil survey area. As soil surveys became more intensively used, especially in farm planning for improving the conserva-

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tion of soil and in urban developments and engineering developments, soil separations increased to several hundred. More intensive soil surveys also meant closer field-by-field examination and careful location and identification of individual soils to make more-accurate maps. These developments led to morecomplex soil maps with a wide array of users-users who are very explicit in their needs. A technical classification scheme enables the user to recognize only that information that deals with his need. The land capability scheme devised by the Soil Conservation Service (Klingebiel and Montgomery, 1961) is an example of soil mapping units grouped on the basis of being nearly alike in suitability for plant growth and in responses to the same kind of soil management. This does not mean, however, that the grouped soils are precisely alike or that they are equivalent in crop output or in small measurements of management differences. As was pointed out by Rieken (1963), there is some residual unused information in the soils being grouped, which might lead one along a more refined fertility input pathway or a more appropriate selection of means to achieve and maintain good tilth.

B. OBJECTIVES AND PRINCIPLES

The diversity of uses of the soil survey supports the importance of the basic natural soil classification as a point of departure for interpretations. It is possible to prepare a variety of interpretations, and to develop new ones as the need arises, from the same soil survey (Hedge and Klingebiel, 1957; Kellogg, 1961). The seemingly high cost of the soil survey is justified on the basis of its flexibility and its ability to meet future demands as both the science and the art of land use change. Many of the properties that influence the behavior of soils in construction or other applications in engineering and, conversely, most of the properties that influence the growth of plants are related to soils as natural bodies (Orvedal, 1963). This relationship provides the key for translating natural soil bodies into groups of soils that behave alike within specified uses. The technical classification is the means by which one can provide groups of soils that behave alike. Orvedal and Edwards (1941) defined the term “technical grouping” (which can be interpreted as technical classification) as “the placing of soils for immediately practical objectives-objectives that pertain to the use and management of soils. ” Technical classification also provides soil scientists with a procedure for better understanding soil behavior, and for coordinating inputs from other disciplines. Soil survey interpretation involves the synthesis of many disciplines into a simple answer. The “Guide for Interpreting Engineering Uses of Soils” (U.S. Department of Agriculture, 1971) has served this purpose well. As a result, interpretations in published soil surveys, even though they are presented as behavior patterns for individual soils, are well coordinated with all disciplines. An exam-

25 1

SOIL SURVEY INTERPRETATION

ple from this guide is Table I, which presents the parameters for grouping soils for septic tank absorption field evaluations. Soils classified as having slight limitations, which indicate a high degree of suitability, have in common the following soil properties: Moderate or more rapid permeability. Hydraulic conductivity rate of more than 1 in./hr. Percolation rate faster than 45 midin. Depth to water table greater than 72 inches. No flooding. Slope less than 8%. Depth to hard rock greater than 72 inches. No or very few stones. No rockiness. Orvedal and Edwards (1941)also identified an important requisite for any technical classification-a clear understanding of the objective for which the TABLE 1 Soil Limitation Ratings for Septic Tank Absorption Fields'' Degree of soil limitation Item affecting use

Slight

Moderate

Permeability class

Rapid, moderately rapid, and upper end of moderate

Lower end of moderate

Moderately slow and slow

Hydraulic conductivity rate (Uhland core method)

More than I in./hr

1-0.6 in./hr

Less than 0.6 in./hr

Percolation rate (Auger hole methcd)

Faster than 45 midin.

45-60 midin.

Slower than 60 midin.

Depth to water table

More than 72 in.

48-72 in.

Less than 48 in.

Flooding

None

Rare

Occasional or frequent

Slope

0-8%

8- 15%

More than 15%

Depth to hard rock, bedrock, or other impervious materials

More than 72 in.

48-72 in.

Less than 48 in.

Stoniness class

0 and I

2

3, 4. and 5

Rockiness class

0

I

2, 3. 4. and 5

"After SCS Soil Engineering Guide, Washington. D.C.

Severe

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classification was made. This entails an understanding of both the problem and the solution. Very rarely will one artificial classification scheme fit many objectives. For a scheme to be effective, the classification should reflect up-to-date knowledge. Any one definitive soil property will govern the placement of a soil. As an example, if a soil floods, but meets all the other requirements listed in Table I for a slight limitation rating, it fails to obtain a slight limitation rating. Technical classification can be displayed with maps. The boundaries of the interpretation classes will match the soil boundaries on the soil map from which the interpretations were derived. Thus, the boundaries on an interpretive map would be similar in number and position to those on the detailed soil map, even though the technical classification is much more generalized than the natural soil classification. Categorical generalization does not necessarily equate to cartographical generalization (Orvedal and Edwards, 1941). Traditionally, tables and narratives are used to interpret or explain soil maps. The Soil Conservation Service has enjoyed much success in employing a uniform color scheme to display land use capabilities on soil maps in its farm and ranch planning program. Soil maps have also been interpreted graphically to show suitabilities, limitations, or potentials for various uses (Bartelli, 1962, 1966; Wohletz, 1966). Developments in the field of computer-generated maps have opened a new medium for spatial display of soil survey interpretations (Nichols and Bartelli, 1974). Computer-generated interpretive maps are versatile, and, once the basic soil map is stored, different behavior patterns can be generated to fit changing needs from the same data source.

C . SINGLE- AND MULTI-TAXA SOIL MAPS

Interpretations are prepared for soil map units. When the units are based mostly on a single taxon-that is, a single classification unit or units that behave alike dominate the delineation-the delegated natural soil unit carries the interpretation for the soil map unit. However, when the delineation includes more than one natural soil unit that do not behave alike, interpretations become complex. Several procedures may be followed. The simpler approach is to designate the composition of the soil map unit and identify the behavior pattern for each taxon that is listed for the unit. This procedure has some limitations. The user is left with the job of unraveling the effect of the interaction among the unlike soils and devising a treatment for the unit. This procedure aiso creates some confusion with computer-generated interpretative maps that are programmed to evaluate each soil map unit. The U. S. Forest Service introduced the concept of the land system (Wendt er al., 1975) for better manipulation of the interpretations for multi-taxa soil map units. This procedure integrates the interactions between the soil and other members of the environment to produce behavior predictions for such units.

SOIL SURVEY INTERPRETATION

25 3

111. Systems for Organizing Soil Survey Interpretations

A. FOOD AND AGRICULTURE-UNITED NATIONS SYSTEM

The Food and Agriculture Organization of the United Nations (FAO) has issued a “Framework for Land Evaluation” (FAO, 1976) to serve as a guide for grouping soils into meaningful classes of land suitability. The system is offered to provide some standardization among the many systems being used and to allow for easier exchange of information among the cooperating nations. Some of the basic principles of the FA0 system are as follows: (1) Land suitability must be rated for specific uses of land. Each use or group of uses has a specific set of soil requirements. An example of different requirements is the soil depth requirement of shallow- versus deep-rooted plants. (2) Suitability for each use is assessed by comparing required inputs with benefits received. Land rarely possesses productive potential without inputs. (3) FA0 recognizes the need for a multidisciplinary approach. No evaluation is complete without the input of disciplines from related fields of sciences and technologies. (4) The evaluation system must consider the physical, economic, and social patterns of the area. This principle represents an attempt to establish practical groupings or ratings. ( 5 ) Environmental impact must be considered in the rating. The land use is rated on a sustained basis. (6) Evaluations should involve the comparison of more than a single kind of use. This requirement is introduced as a safeguard against overlooking other? more-beneficial uses.

The various criteria (FAO, 1976) are grouped according to land characteristics and land qualities. Land characteristics include those attributes of land that can be measured or estimated. These are the features that are used to design map units, and they normally include soil and associated landscape features. Land qualities are more complex. Land qualities are used to characterize the interaction among the various soil and landscape features as they affect a selected land use. Availability of moisture, resistance to erosion, flooding hazards, and accessibility are some examples. Land quality patterns are very similar to soil behavior patterns. As in soil behavior, there is a large number of land qualities. The list varies with the land use alternatives under consideration. Some of the land qualities related to productivity of crops are crop yields (a result of many other qualities), moisture availability, nutrient availability, root ramification zone, soil toxicity, resistance to soil erosion, and climate. The system for grouping is named land suitability classification. Four categories are recognized-land suitability orders, land suitability classes, land

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suitability subclasses, and land suitability units. Land suitability orders reflect kinds of suitability. The soil is classed as either suitable or not suitable. Criteria for rating a soil are not spelled out. The rating team is given a framework for its evaluation. Land that is rated suitable must be able to sustain the use in question without damage to the land resource. The value of the expected benefits must justify the cost of the inputs. Land suitability classes group soils with similar degrees of suitability. Differences in degrees of suitability are determined by the relationship between benefits and inputs. Normally the inputs and benefits must be expressed in some measurable economic terms. The rating team is instructed to use the classes needed to meet the objectives of the survey area. Parameters to define the limits of each class are left to the discretion of the rating team. Three classes are defined on the basis of behavior. The highly suitable class includes those soils that have no significant limitations to sustained use. The marginally suitable class includes those soils for which the use is very questionable. Limitations are such that sustained application of a selected use will reduce the benefits. The moderately suitable class includes soils that fall in between the highly and marginally suitable classes. Kinds of limitations, such as erosion hazard, nutrient availability, and moisture availability, are used to define land suitability subclasses. Examples of some limitations are listed in Table 11. Only two guidelines are presented for grouping within this category. Namely, subclasses should be kept to the TABLE I1 Some Important Land Qualities in Surinam" Land quality With regard to crop growth Moisture availability Oxygen availability in the root zone Nutrient availability Absence of toxicities

Code

m 0

n t

With regard to management Resistance to erosion Trafficability and accessibility Length of dry periods for harvest and land preparation Freedom of parceling Resistance to compaction With regard to land improvement Ease of leveling or land shaping Ease of vegetative clearance Ease of irrigation and drainage works " F A 0 (1976).

I V

i

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SOIL SURVEY INTERPRETATION

minimum, and the fewest number of limitations as possible should be used in each subclass. Subclasses can be subdivided into land suitability units. Criteria suggested for grouping at the unit level include similarities in production characteristics or in minor aspects of their management requirements. In summary, the F A 0 systems present a framework that will tend to produce some degree of standardization among the various study areas. Quantitative parameters for rating a soil map unit, are not standardized, however. The system does not ensure coordination of ratings of like soils between study areas. Another limitation is that rating guides, which are helpful to field men (guides tend to accumulate past experience), are lacking and must be developed by the rating team. An example is the criteria and rating for moisture availability for oil palm in Surinam (FAO, 1976). For example, no limitation is recognized where moisture shortage is less than 200 mm, a moderate limitation where it ranges between 200 and 400 mm, and a severe limitation if it ranges between 400 and 600 mm. These locally developed parameters tend to develop groupings that are more acceptable at the local level.

B . SOIL CONSERVATION SERVICE USDA-LAND CAPABILITY SYSTEM

USE

The Soil Conservation Service has developed the land use capability system for grouping soils into capability classes, subclasses, and units very effectively in the farm planning program. This grouping has served to introduce the farmer to the complex soil map. The capability classification is made primarily for agricultural purposes. The highest and broadest category in the system places soils in eight capability classes. The risks of soil damage (normally erosion) or limitations in use (the more restrictive use means less cultivation) become progressively greater from Class I to Class VIII. Classes I through IV are considered suitable for the common cultivated crops; Classes VI and VII also can be used with special treatments. Class V, however, does not fit into this orderly pattern because soils too wet for cultivation are placed in this class. Class VIII is reserved for those soils that do not return benefits for inputs of management for crops, grasses, or trees. The second level, the subclasses, are separated on the basis of kinds of limitations or hazards-namely , erosion, wetness, rooting zone limitations, and climate. The smallest class, the capability unit, is a grouping of soils that have about the same responses to management. Criteria for placing soils in capability classes are presented in Agriculture Handbook No. 210 (Klingebiel and Montgomery, 1961). Various soil and landscape features are included, but any feature may limit the safe and productive use of the soil. One unfavorable feature may dominate the rating, or several mi. features, collectively, may become a major problem and thus limit the use die

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soil. The criteria also are modified on a regional basis to fit the similarities of climate. If it is feasible to remove the hazards or limitations, the soil is classified on the basis of other, if any, continuing limitations. Feasible is defined to mean that over broad areas limitations are being removed in the present economic climate. An example is a dry soil in an arid or semiarid area where irrigation projects are being developed. Climate limitation is not applied in this case. Other situations are flooding, wet soils, stony soils, and soils having toxic salts. Both soil moisture and soil temperature regimes affect the capability rating. Soils with udic soil moisture regimes and mesic or warmer soil temperature regimes are placed in Class I. Soil scientists in Texas and Oklahoma use the following soil moisture guidelines: Udic intergrades of ustic regimes = Class 11; typic ustic regimes = Class 111; torric intergrades of ustic regimes = Class IV; ustic intergrades of torric regimes = Class VI;and tonic regimes = Class VII. Soil wetness is considered when it restricts or limits the kind of cultivated crops that can be grown. If drainage outlets are available, the soil is rated on the basis of its reaction to drainage improvements. Soil permeability or hydraulic conductivity in the saturated state is used as a guide. Wetness is not considered a limitation in soils with conductivity rates faster than 0.80 inch per hour after drainage improvements have been installed. Soils with conductivity rates that range from 0.80to 0.05 inch per hour will be rated Class 111, and soils with rates slower than 0.05 will be rated Class IV after drainage. Salt content is a criterion. Classes are usually defined as follows: (1) Class II-crops slightly affected. These usually have soil concentrations of

0.15-0.35% salt, or conductivities of extract of about 4-8 mmho/cm. (2) Class III-crops moderately affected. Soils usually have concentrations close to 0.35% salt, or conductivities of extract of about 8-10 mmho. (3)Class IV and VI-crops seriously affected on cultivated land. These soils have salt concentrationsof 0.35-0.85% salt, or conductivitiesof extract of 10-15 mmho. (4)Class VII-satisfactory growth of useful vegetation virtually impossible. Salt concentrations are usually greater than 0.65%, and conductivities are greater than 15 mmho. Soil slope is a significant landscape feature that dominates the capability rating scheme because it influences both the rate of water maoff and the rate of soil erosion. But slope alone is not an adequate measurement of the erodibility of a landscape unit. Other factors, and the interaction among these factors, give the best approximation of the erosion hazard. The universal soil loss equation (Stewart et al., 1975)serves as an effective tool for comparing one soil site with another. The K factor, which is used in the soil loss equation, reflects the inherent erodibility of a soil (Wischmeier, 1977).

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257

The calculated soil loss for up-and-down cultivation, continuous corn on a 9% slope, and 72.6-foot length is used to rate the capability of a soil landscape. For example, ratings of 0-3 tons per acre per year would place a soil unit into Class I, 3-12 tons into Class 11, 12-30 tons into Class 111, 30-55 tons into Class IV, 55-85 tons into Class VI, and over 85 tons into Class VII. This method is used to evaluate the risk of erosion. Past erosion, also, is significant in the use, management, and response of soil. The severity of the soil damage due to past erosion is reflected in the capability of the soil landscape. Soil depth, which includes the total depth of the soil profile favorable for root development, is also used to rate a soil. The following relations between soil class and soil depth are listed (Klingebiel and Montgomery, 1961): Class I, 36 inches or more; Class 11, 20-36 inches; Class 111, 10-20 inches; and Class IV, less than 10 inches. Where other unfavorable factors occur in combination with depth, the capability decreases. Available water-holding capacity is another soil parameter. Usually, a Class I soil should have sufficient water-storage capacity to promote plant growth throughout the average drought periods in the region without supplementalirrigation. The land use capability system is categorical. It generalizes by grouping soils together on the basis of soil properties and landscape features. The system gains spatial characteristics when it is used to rate a soil map unit. If the map unit includes a complex of unlike soils, the rating is difficult. The system does not group adjacent, unlike soils together.

C. U . S . FOREST SERVICE-LAND

SYSTEMS INVENTORY

The land systems inventory is an ecological inventory developed by the U. S. Forest Service (Wendt et al., 1975). It is a multicategorical system that integrates the relationships between physical (geology and soils) and plant ecology. The objective is to inventory the land capability. The system is complex in that criteria vary, from climate and lithology in the highest category, to soils, land forms, and biospheres in the lowest category. Six categories are recognized in the Boise National Forest inventory (Wendt et al., 1975). The lowest category represents the total integration of ecological components. The system is designed to meet specific planning needs in the national forests. In a sense, the land system hierarchy corresponds to the planning hierarchy. Each level of the system satisfies a need at the corresponding planning level. For example, the land-type phase (lowest category) is used for project development and detailed planning in the Boise National Forest (Wendt et al., 1975). A review of the various unpublished inventories being carried out in the national forests indicates that several different methods are used to identify the

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various land units in the system (personal communication from Devon Nelson, U.S. Forest Service, Milwaukee, Wisconsin). In the genetic approach, distinctive land units are recognized on the basis of ecosystem-formingprocesses. The physical divisions identified by Fenneman (1938) serve as a useful base in the eastern United States. A more refined breakdown is possible by considering other processes, such as alpine glaciation, continental glaciation, and soil-forming processes. Emphasis is placed on landscape-forming features. The second approach groups soil landscapes on the basis of an empirical analysis of a selected group of surface characteristics. Such features as local relief, percentage of area with slopes of less than 8%, generalized soil profiles, distinctive surface materials, and major lineaments such as streams, crests, and valley sides are considered. Quantitative values are assigned to the various factors, with emphasis on topographical features. This approach is described in more detail by Hammond (1964). The advantage of this procedure is that it can be applied with modem remote sensing techniques. This approach may also be combined with the genetic concept for a very effective system. The empirical analysis system leads to standardization of techniques and better coordination of like landscapes among the various workers. In the third approach the mapmaker delineates the standard landscapes, such as mountain ranges, mesas, upland moraine, or hilly lands. In a sense, the character of the land is sought through its appearance as in an aerial view. Interpretation with stereoscopic pairs of aerial photographs is a common procedure. External land forms are used to read the inherent character of the landscape. The objective is to identify and delineate landscapes at the various levels of mapping intensity that are recognized in the field by potential users. Where possible, plant communities are used to identify the map unit, but vegetation lacks the ecological stability of physiography. The more subtle landscapes that lack physiographic expression are difficult to subdivide. Map interpretations are made with the soil taxonomic unit. Representative soil pedons of each map unit are classified within the system of soil taxonomy (Wendt et al., 1975). Each land unit with its component soils and vegetation is interpreted for opportunities, constraints, and hazards appropriate to management needs. The interpretations range from general statements that describe timber productivity, erosion hazards, and most suitable potential use, to a more precise grouping on the basis of land capability to produce timber, forage, and water, and with similar responses to management. The more intensive soil surveys (Larry Burkhart, personal communication, U.S. Forest Service, Sault Ste. Marie, Michigan) list interpretationsfor each map unit that include the following: natural productivity, species suitability, and scenic sensitivity for timber, suitability for roads, season of use, source of topsoil, borrow source, suitability for recreation, suitability for agriculture, and watershed characteristics. These interpretations are based on phases of soil series.

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259

D. UNITED KINGDOM-LAND USE CAPABILITY CLASSIFICATION SYSTEMS

The land use capability classification system has been developed to express the influence of soil, site, and climate on farming in the United Kingdom. Mackney (1974) lists the following aims of the system: ( I ) To simplify soil maps and express their content in terms of land potential, and limitations that restrict use. (2) To provide a basis for farm planning and technical advisory work. (3) To aid in planning land use.

These groupings are based on soil properties that are significant for a stated use. The groupings are mostly qualitative. They also reflect climate, management, and crop performance. As in the USDA system, land is divided into three groups, based on the severity of use: Classes 1 through 4 include land suitable for arable crops and other uses. Classes 5 and 6 are not suitable for arable crops but are useful for grazing and forestry. Class 7 is not suited to arable crops, grazing, or forestry. The system differs, however, from the USDA system in that Class V is not used for wetland. The United Kingdom system retains a theme of progressively greater limitations from Class 1 through 7. The system has three categories. Subclasses are used to identify the particular factor or factors influencing production or needing correction. Five groups of limiting factors are recognized-soil, wetness, climate, gradient, and erosion. Subdivisions of subclasses distinguish the different management and improvement practices required. The United Kingdom system of grouping soils is based on specific information on soil productivity. Wilkinson (1974) describes productivity as the function of soil, topographical, and climatic factors integrated together with technological management. In practical farming Wilkinson (1974) recognizes the distinction between potential and actual productivity. Actual productivity rarely reaches potential productivity, owing to the imposed limitations connected with soil, topography, and climate. Table I11 lists the various limitations that are considered. By measuring potential productivity and actual productivity, and by keeping the management factor at a constant defined level, Wilkinson (1974) strives to assess the total impact of the limitations and to identify and grade the components. The limitations that influence productivity are grouped according to the inherent relationship. Soil limitations include those factors related to the soil pedon; associated landscape features are considered as topographical limitations and rainfall; and temperatures and exposure are grouped into climatic limitations.

260

LINDO J. BARTELLI TABLE 111 Limitations for Land Capability Classification" Limitations Soil limitations Distribution pattern Physical factors Chemical factors Biological factors Topographical limitations Geographic position Slope Flood and erosion hazard Elevation Air drainage Climatic limitations Rainfall Solar radiation Exposure

Elements

Uniformity or variability Texture, drainage, available water capacity. stones, structure, depth Nutrient deficiencies, organic matter, nutrient toxicities Susceptibility to pest, disease, and weed infestation Longitude and latitude Angle and complexity Aspect and exposure

Quantity and intensity Temperatures. duration, frost hazard Elevation, wind speeds, erosion hazard

"After Wilkinson (1974).

Potential productivity is assessed by collecting yield data under strictly controlled management on a number of sites per each bench-mark soil and collecting data from microplots on selected soil series under controlled management. Crop yields are used as a measurement of the integrated influence of the soil's physical resources and the environment. These data are used to classify soil units according to the degree to which the limitations affect their capability. The data are used to define the cutoff points for the capability class. Subclasses within a class are ranked in descending order of their overall potential. Capability units are identified within subclasses on the basis of their physical uniformity, similar cropping possibilities, and comparable productivity. Again, as Wilkinson (1974) points out, the capability units are ranked in descending order according to their overall relative potential. The procedure aims to reduce the subjective element in the classification procedure. This is shown by studies (Wilkinson, 1974) that compared yields of heavy-, medium-, and lighttextured soils. Mean total dry matter yields for heavy soils were slightly lower than those for medium-textured soils, but higher than those for light-textured soils. These yields reflect the negative effect during high rainfall seasons of adverse soil structure in the heavy-textured soils.

SOIL SURVEY INTERPRETATION

IV. Plant Suitability

26 1

Evaluation Systems

Several systems have been developed for evaluating soils for plant suitability. The Soil Conservation Service has developed schemes (Lemmon, 1969; Shiflet, 1973) for selecting suitable sites for plants in rangelands and forestlands. Woodland suitability groups are devised to simplify the use of soil maps in managing wood-producing enterprises. Soils are grouped on the basis of similarity in woodland growth and response to management. A range site is defined by Shiflet (1973) as the product of all the environmental factors responsible for its development-climate, soils, and topography. Soil surveys in the rangelands also are interpreted through a grouping of soil mapping units into range sites. Soils are also grouped on the basis of growing plants for wildlife habitat. The soil survey of Brevard County, Florida (Huckle et al., 1974), serves as an example of woodland suitability, range sites, and wildlife habitats. A. WOODLAND SUITABILITY GROUPS

Soil groupings for forestry are based on a synthesis of those soil properties that influence selected soil-tree behavior patterns. The behavior patterns considered in the Brevard County, Florida, soil survey are productivity, erosion hazard, limitation of equipment, plant competition, mortality of seedlings, hazard of windthrow, and trees to favor or plant. Table IV summarizes the criteria used to define the groups. Productivity is expressed in the site index of the trees growing on that soil. Site index refers to the height in feet of the larger trees at a given age. Site index is used as a soil parameter to define the yield range of each group of soils. For example, each group of soils in Brevard County, Florida (Huckle et al., 1974), has a site index spread of 10 points. The erosion hazard considers the risk of soil loss through erosion, which may occur after harvesting and other management input. Soil erodibility (K values of the soil loss equation) and degree of slope are intergraded into three classes. An example of a guide that can be used to rate soil erodibility is as follows: Rating

Soil K and slope

0-8% with K of 0.4 or more, 0-15% with K of 0.3-0.4, 0-35% with K of less than 0 . 3 Moderate 3-15% with K of 0.4 or more, 15-35% with K of 0.3-0.4, 35% or more with K less than 0 . 3 , Severe 15+% with K of 0.4 or more, 35+% with K of 0.3-0.4 Slight

Limitation of equipment refers to the limits placed on the use of equipment as a result of soil characteristics. Soil wetness, slope, flooding, and soil texture of surface layers were used in grouping the soils in the Spartanburg County, South

TABLE IV Soil Factors Used to Form Woodland Suitability Groups in Brevard County, Florida Soil factors Woodland group

Texture

Wetness

I

Sandy

2

Sandy

3

Sandy

4

Sandy

5

6

Sandy Sandy

7 8

Sandy Sandy

Excessively drained Excessively drained Moderately well drained Moderately well drained Poorly drained Poorly drained (wet most of the time) Poorly drained Moderately well drained Very P ' l Y drained Well drained

9 10

Sandy

Depth (cm)

Flooding

Productivity (site index)

>300

None

Low (sandpine

>300

None

Moderate (slashpine

>I50

None

Low (slashpine = 60)

>I50

None

Moderate (sandpine

> 100

None None

Moderate (slashpine = 70) Moderate (slashpine = 70)

6 mos or more None

Moderate (slashpine = 70) Moderately high (slashpine = 80) High (slashpine = 90)

>I00

> 100 >I00

None Bedrock to 50.00

= <50) =

=

70)

70)

Moderately high (slashpine = 80)

SOIL SURVEY INTERPRETATION

263

Carolina, soil survey (Camp, 1968). Wet soils and soils with steep slopes (more than lo%), soils in which erosion exposes plastic subsoils, and soils with stones and boulders were classed in the severe limitation class. Soils on slopes ranging from 5 to 10% and somewhat poorly drained soils were rated in the moderate limitation class. All other soils were rated slight. Plant competition is used to measure the degree of invasion or growth of undesirable species when openings are made in the forest canopy. Availability of soil water and the natural fertility level of the soil are the parameters. Soils with a good moisture supply and a high base status are rated severe because a wide selection of plants will grow vigorously on these soils. Seedling mortality reflects the influence of the site on the probability of survival of either naturally occurring or planted tree seedlings. Droughty soils, sandy in texture, with low moisture supply capacities, have higher seedling mortality and are separated from the more productive soils. The exposure of the site also influences the rate of seedling mortality, for the rate is higher where the exposure is severe. Windthrow hazards reflect the likelihood of trees being uprooted by wind. Soil depth and soil wetness are the major criteria. Suggested classes include wet soils with rooting depths of less than 10 inches; soils with rooting depths of 10-20 inches, or less than 10 inches if not wet; and soils with more than 20 inches of rooting depth.

B. RANGE SITES Soils that produce about the same kinds and amount of forage are grouped into range sites. The range site is used to predict the climax vegetation-the plants that were growing there when the region was first settled. The potential natural vegetation cluster is another parameter of the soil map unit. Both soil taxonomic characteristics and associated landscape features serve to define the limits of the range site group. The following features were used to group soils in the soil survey of Medina County, Texas (Dittmarer al., 1977): effective rooting depth, soil surface shape, slope gradient, nutrient level, lime content, soil surface texture, permeability, and available water capacity. There is a close correlation between these soil features and potential natural vegetation Table V summarizes the grouping criteria in the soil survey of Medina County, Texas. In addition to the description of the group, the climax plants and principle plant invaders are named. An estimate of the potential annual yield of air-dry herbage is listed for each group. Yields are given for each site when it is in excellent condition. The soil properties are grouped into classes that are defined in the “Soil Survey Manual” (U.S.Department of Agriculture, 1951).

TABLE V Soil Features Used to Group Soils for Range Sites in Medina County, Texas

Range site

Depth

Slope

Shape

Permeability

Texture

Average water capacity

Nutrient Level

Position in Landscape

I

Deep

Level

Concave

Very slow

Clays

High

High

Uplands

2

Deep

Level

Smooth

Moderate

Loam

Medium

Very high lime content

Stream terraces and outwash plains

3

Shallow

Undulating

Convex

Slow to very slow

Silty clays. clays Low

Moderate to high

Uplands

4

Shallow

Gently sloping

Convex

Moderate

Sandy loams

Low

Moderate

UpIands

5

Very shallow to shallow

Steep

Convex

Moderately slow

Clays

Low

High lime content

Uplands

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C. SOIL GROUPINGS FOR WILDLIFE

The distribution of the kinds and numbers of wildlife is greatly influenced by the kinds and distribution of the soil. This effect is caused indirectly by the kinds and amount of vegetation produced by the soil, the amount of water available, and the presence of particles of different sizes in the soil material. The following soil properties were used to rate or group soils for wildlife interpretations in the soil survey of Medina County, Texas (Dittmar et al., 1977): effective rooting depth, texture of soil surface, available water capacity to a depth of a meter, soil wetness, surface stoniness or rockiness, flood hazard, slope, and soil permeability. Each soil is rated according to its suitability for producing various kinds of plants that make up the wildlife habitat. For example, soils rated very poor for domestic grasses and legumes are rated very poor for openland wildlife. Openland wildlife includes birds and mammals that live in meadows, pastures, and open areas where grasses, herbs, and shrubby plants grow. Examples are quail, doves, and cottontail rabbits. Soils also are rated or grouped for range wildlife, wetland wildlife, and woodland wildlife in a similar manner, using these soil features that influence plant growth. V. Systems to Evaluate Engineering Properties

The agricultural or pedological soil survey is a valuable tool for the engineer because of the areal information presented in the soil map and the engineering predictions of the behavior of the surface earthy material over time. The predictions encompass the environmental conditions of the soil unit. The wetting and drying that a soil experiences during the year greatly influence its behavior. Gromko (1974) recognized this process, as he recommends the integration of the various engineering tests-Atterberg limits, colloid content, consolidation tests, and free swell index-with climatic data for complete behavior analysis. There are some limitations to the use of pedological soil surveys. Interpretations are made for soils that are rarely examined deeper than 2 meters. The scale of maps does not normally permit the showing of certain details that may be important to the engineer. In addition, in mixed-up country, as in glaciated areas, inclusions in the map delineations of small areas of unlike soils may occur. In spite of these drawbacks, the soil survey is becoming increasingly important and useful to the engineer. Of the several soil classification systems used by the engineer, three systems-the American Association of State Highway and Transportation Officials (AASHTO) system, the unified soil classification system, and the Federal Aviation Agency system-will be discussed. Two basic soil tests, mechanical analysis and consistency, are used in these systems. Mechanical analysis is the

266

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determination of the percentages of individual grain sizes. This analysis is made with screens to determine the amount of coarse material that passes a No. 200 sieve and with a hydrometer to analyze the material. The consistency tests determine the liquid limit, the plastic limit, and the shrinkage limit (Atterberg limits). The liquid limit is the level of moisture content at which the soil changes from the liquid to the plastic state. The plastic limit is the border between the plastic and semisolid states. The plasticity index, a frequently used value, is the range of moisture content over which a material is in the plastic state. It is the arithmetic difference between the liquid and plastic limits. The shrinkage limit delineates the semisolid from the solid state. Both tests are very effective. Mechanical analysis works well in denoting the behavior characteristics of material coarser than what passes the No. 200 sieve, and the Atterberg limits are useful in characterizing the behavior of the size fraction that passes the No. 200 sieve. The No. 200 sieve, which approximates the 0.08-mm-diameter class, usually separates the plastic from the nonplastic soil material. This is an important separation, but it is not recognized in the pedological soil survey. Other discrepancies among the various systems listed in Fig. 1 are as follows: The clay size recognized in the USDA is 0.002 mm, whereas 0.005 mm approximates the largest diameter for clays in the other system; the AASHTO and unified systems use the 0.4-mm (40-mesh screen) size to separate fine sand from coarse sand, whereas the USDA does not. Also, the separation between fine sand and silt does not match. Some attempt has been made in “Soil Taxonomy” (U.S. Department of Agriculture, 1975) to reconcile these conflicts; however, many of the soil series are defined on the basis of what is listed in Fig. 1 as U.S. Department of Agriculture Soil Classification. The coarse-silty and coarseloamy soil family textures in “Soil Taxonomy” are designed to group the nonplastic soils, and the fine-loamy and fine-silty include the plastic soils. This separation is based on experience and on various analyses which indicated that 18% clay (finer than 0.002 mm) is a logical parameter in many soils. Plasticity is an important soil characteristic which influences the engineering behavior of soils. It is strongly affected by the soil moisture content and the kind and amount of clay. The liquid limit and the plasticity index increase as the percentage of clay rises. However, values are higher for montmorillonitic clays. Lohnes and Demirel (1970) reported on the inadequacy of the traditional engineering classification systems in some tropical soils. Soils such as the Bayamon, Limones, Nipe, and Catalina soils of Puerto Rico have liquid limits exceeding 60 and plasticity indexes that are higher than 23, and show shear strengths of less than 15.0 psi (Lohnes and Demirel, 1970). A coefficient of linear extensibility test (COLE) value of only 0.03 is reported for the Bayamon soil (U.S.Department of Agriculture, 1967). Experience in these kinds of soil is needed to interpret the engineering index tests properly. Soil taxonomy provides a good basis for coordinating such experience.

American Society for Testing and Materials American Association of State Highway Officials Soil Classification

U .S . Department of Agriculture Soil Classification Federal Aviation Agency Soil Classification Unified Soil Classification (Corps of Engineers, Department of the Army. and Bureau of Reclamation)

I Fines (silt or clay)&

Fine sand

Medium sand

Coarse sand

Fine gravel

Coarse gravel

Cobble:

Particle size, mm Colloids included in clay fraction in test reports. *Theliquid limit and plasticity index of “Silt” plot below the “A” line on the plasticity chart, Table VII and the liquid limit and plasticity index for “Clay” plot above the “A” line. “

FIG. I .

Soil-separate size limits of ASTM. AASHTO. USDA, FAA, Corps of Engineers, and USBR (from Asphalt Institute, 1969).

TABLE VI Classification of Highway Subgrade Matecals (with Suggested Subgroups)" Silt-clay materials (more than 35% of total sample passing No. 200)

Granular materials (35% or less of total sample passing No. 200)

General classification:

~~

A- I Group classification: Sieve analysis, % passing: No. 10 No. 40 No. 200 Characteristics of fraction passing No. 40: Liquid limit Plasticity index

A-2

A- I -a

A- I -b

A-2-3

50 max 30 max 15 max

50 max 25 max

51 min

6 max

Group index

"From Asphalt Institute (1969).

0

A-7

A-2-4

A-2-5

A-2-6

A-2-1

A-4

A-5

10 max

35 max

35 max

35 max

35 max

36 min

36 min

NP

40max 41 min 40 max 10 max 10max 1 1 min

41 min 1 1 min

40max 41 min 40 max 41 min 10max 10 max I 1 min 1 1 min

0

0

4 rnax

8 max

12 max

A-6 A-1-5. A-1-6

36min

36 min

16max 20max

SOIL SURVEY 1NTERPRETATlON

269

A. THE AMERICAN ASSOCIATION OF STATE HIGHWAYS AND TRANSPORTATION OFFICIALS SYSTEM

The American Association of State Highway and Transportation Officials (AASHTO) system is designed to group soils together on the basis of their similarity in general load-carrying capacity and road service characteristics. The system is multicategorical, with the highest category recognizing two classes: granular material (35% or less passing the No. 200 screen), and silt-clay material (more than 35% passing the No. 200 screen). Seven basic groups are recognized in the second category. They are designated A-1 through A-7. In general, A-1 includes the best soils for subgrades, with suitability getting poorer with each increase in group number. Particle size (percentage passing No. 10, No. 40, and No. 200), liquid limit, and plasticity index are used as criteria to define the groups. The limits of each class are listed in Table VI. The subgroups are divided into smaller and more specific classes by a group index number. The group indexes range from 0 for the best subgrades to 20 for the poorest and are always shown in parentheses after the group symbol as: A-2-6(3). The group index is used within each subgroup. The index reflects the combined effect of increasing liquid limits and plasticity indexes and decreasing percentages of coarse material (Asphalt Institute, 1969). The system is very quantitative; all classes are defined with measured data. The tests are conducted on samples that have been removed from their natural sites. The tests do give an estimate of the load-carrying capacity conditions, but the final behavior pattern is controlled by the environmental factors, especially the soil moisture content.

B. THE UNIFIED SOIL CLASSIFICATION SYSTEM

The unified soil classification system was proposed by Casagrande (1947) for classifying soils to indicate their suitability as subgrades for roads and airfields. As in the AASHTO system, this system is multicategorical and groups soils on the basis of particle size for those soils with a small amount of fines. If the quantity of fines is great enough to affect the behavior, the criteria are based on plasticity-compressibility characteristics. The classification scheme is based on the following soil properties: (a) percentages of gravel, sand, and fines, using the No. 4 and No. 200 sieves; (6) shape of the grain size distribution curve; (c) plasticity and compressibility characteristics. The soils in the highest category are divided into three classes. These classes are (a) coarse-grained soils, (6) fine-grained soils, (c) highly organic soils. The coarse-grained soils contain 50% or less of material smaller than the No. 200 sieve; the fine-grained soils contain more than half of the materials smaller than No. 200 sieve; and the organic soils are identified visually.

TABLE VII Unified Soil Classification System“

Major divisions

r

Group symbols

rGW

Clean gravels“ 1 G P

Clean l S a n d s c 1sands’

Laboratory classification criteriah

Well-graded gravels, gravel-sand mixtures, little or no fines Poorly graded gravels, gravelsand mixtures, little or no fines

C.

Silty gravels. gravel-sand-silt mixtures

Atterburg limits below “A” line or P.I. less than 4

Clayey gravels, gravel-sand-clay mixtures

Atterburg limits above “A” line with P.I. greater than 7

Well-graded sands, gravelly sands, little or no fines Poorly graded sands, gravelly sands. little or no fines

C,

=

D,O

greater than 4;C, =

(D30)’) between I and 3 DIO x D ,

Not meeting all gradation requirements for GW

d U

Coarse grained soilsb

Typical names

”’

=

D 10

greater than 6; C ,

=

Above “A” line with P.I. between 4 and 7 are borderline cases requiring use of dual symbols

between I and 3 D,o x D , (D30)2

Not meeting all gradation requirements for SW

d Silty sands, sand-silt mixtures U

Clayey sands, sand-clay mixtures

Atterburg limits below “A” line or P.I. less than 4 Atterburg limits above “A” line with P.I. greater than 7

Limits plotting in hatched zone with P.I. between 4 and 7 are borderline cases requiring use of dual symbols.

Inorganic silts and very fine sands, rock flour, silty or clayey tine sands. or clayey silts with slight plasticity Inorganic clays of low to medium plasticity, gravelly clays, sandy clays, silty clays. lean clays Organic silts and organic silty clays of low plasticity Inorganic silts, micaceous or diatomaceous h e sandy or silty soils, elastic zrlts Inorganic clays of high plasticity, fat clays Organic clays of medium to high plasticity. organic silts Highly organic soils

PI

Peat and other highly organic soils

Liauid limit Plasticity Chart

“From Asphalt Institute (1969). *Coarse-grained soils have more than half of the material larger than No. 200 sieve size, whereas more than half of the fine-grained soil passes through No. 200 sieve. ‘In gravels more than half of coarse fraction is larger than No. 4 sieve size, whereas more than half the coarse fraction of sands is smaller than No. 4 sieve. dSilts and clay may be divided into those with a liquid limit (LL) of less than 50; ML, CL, and OL and those with a liquid limit of greater than 50; MH.CH, and OH. ‘Gravels can be further divided into those with little or no fines (clean gravel) and those with appreciable amounts of fines (gravels with fines). ’Clean sand has little or no fines, sands with fines have appreciable amounts of fines. #Division of GM and SM groups into subdivisions ofd and u are for roads and airfields only. Subdivision is based on Atterburg limits; suffix d used when LL is 28 or less and the plasticity index (PI) is 6 or less; the suffix u used when LL is greater than 28. *Determine percentages of sand and gravel from grain-size curve. Depending on percentage of fines (fraction smaller than No. 200 sieve size), coarsegrained soils are classified as follows: Less than 5%. GW, GP. SW, SP; more than 12%. GM. GC,SM, SC; 5-12%. borderline cases requiring dual symbols. Borderline classifications. used for soils possessing characteristics of two groups. are designated by combinations of group symbols, for example, G W G C , well-graded gravel-sand mixture with clay binder.

LINDO J. BARTELLI

272

TABLE VIII Diagnostic Features Used in Various Categories of the Unified Soil Classification System Classes and features

Category

I

I1

Highly organic, visual

No subclass

Coarse-grained (No. 200 sieve) Sands

Fine-grained

(No. 200 sieve)

Gravel (No. 4 sieve)

(No. 4 sieve)

L (liquid limit)

H (liquid limit)

111

No subclass

Three classes, No. 200 sieve

Three classes, No. 200 sieve

Three classes, plasticity

Two classes, plasticity

IV

No subclass

Six classes based on gradation and plasticity

Six classes based on gradation and plasticity

Four classes based on plasticity

Four classes based on plasticity

In the second level, the coarse-grained soils are subdivided into gravels and sands. The No. 4 sieve (approximately 5 mm) is used to make this division. Sands are defined to have more than 50% grains smaller than No. 4 sieve size. Gravels are coarser. Fine-grained soils are subdivided into silts and clays on the basis of their liquid limit. Soils with liquid limits of less than 50 are placed in the L class, and soils with liquid limits higher than 50 are placed in the H class. Particle size distribution is still used in the third category for the coarsegrained soils. However, plasticity is used to define the classes for the finegrained soils. The amount of soil material passing the No. 200 sieve is used as the criterion to define three classes. The plasticity chart defines classes of the fine-grained soils. The “A” line, which is an arbitrarily drawn line on the plasticity chart, separates the more clay-like soils from the silt-like soils. Soil materials with plasticity index and liquid limit values that plot below the line are less clayey and less plastic than those that plot above the line. Further subclasses are recognized in some of the classes at the third category level. A separation of organic and inorganic materials is based on visual analysis in the fine-grained materials. Gradation, or the distribution of particle size, is used for further subclasses in the coarse-grained materials. A quantitative definition of gradation is based on the ratio between the amount of material that passes the No. 60 sieve and the No. 10 sieve. Well-graded soil material has all sizes of particles, with no excess of material in any size range. Table VII, derived from the Asphalt Institute “Soils Manual” (Asphalt Institute, 1969), summarizes the unified soil classification system. An analysis of the diagnostic features (Table VIII) indicates a well-quantified system highlighting those features that can be measured in the laboratory. The system is useful in analyzing the potential

SOIL SURVEY INTERPRETATION

273

behavior of a site. However, the system is most effective when integrated with the pedological soil classification system. This integration allows one to consider the environmental features and their effect on the engineering behavior of the site.

C. FEDERAL AVIATION AGENCY SOIL CLASSIFICATION SYSTEM

The Federal Aviation Agency soil classification system also is based on a mechanical analysis criterion for coarse-textured soils and the liquid limit and plastic limit tests for fine-grained soils. The system has two categories. Granular soils are separated from fine-grained soils on the basis of the amount of combined silt and clay passing the No. 270 sieve. This diameter class matches the diameter used in the pedological soil survey to separate silt and clays from sand. The liquid limit and the plasticity index are used to define the groups in the finegrained class. An important feature of the FAA system is the incorporation of environmental factors, such as climate, topography, and drainage. This enables a more accurate interpretation of the site behavior. Thirteen soil groups are recognized, and subgrade classes are used to reflect frost hazard and drainage. Drainage reflects topography, surface water runoff, internal water movement, and ground water level. The frost hazard is considered severe if the depth of frost penetration for the site exceeds the thickness of surface, base, and sub-base. The reader is referred to the “Soils Manual” of the Asphalt Institute (1969) for a complete description of the system. VI. The Application of Technical Classification to Soil Surveys

Soil surveys are unique in that they can be interpreted for many uses (Bartelli, 1962). They are designed to give geographic expression to units of a natural soil classification system-namely, soil taxonomy. These units are defined on the basis of the inherent qualities of the soil. These same inherent soil characteristics are used to classify soils into meaningful groups for the selected user. Each class of user relies on a separate grouping, but the soil survey remains intact. The various techniques are discussed in this section.

A. ENGINEERING INTERPRETATIONS

The major contribution of soil surveys to engineering uses is the facility to extend soil test data to an area much greater than the sample site or even an area

274

LINDO J. BARTELLI

geographically removed from the sample site. Thornbum and Larson (1959) reported that certain soil test data can be predicted from bench-mark soil tests to soil map units with a reasonable degree of precision. Soil surveys also serve as a good check for coordinating soil test results. Another contribution is that engineering properties can be assigned to both disturbed and undisturbed soil. In addition, engineering properties can be extrapolated from soil characteristics. For example, a soil material with a great amount of 2:l active clays is apt to have high liquid limits and plastic index values.

I . Shrink-Swell Behavior Most soils change volume with a change in water content. This change in volume is influenced by the amount and kind of clay. In the swelling phase, the volume change can lead to the generation of very large pressures, which may be detrimental to any structure or building resting on that site. Two methods are used to measure the shrink-swell potential. In one method, dry soil is packed in a cell, and water is added. The pressure generated by the volume change is measured. This device is called a PVC meter and is used by the Federal Housing Administration (Henry and Dragoo, 1965). In the other method, the linear extensibility is calculated from the bulk density measurements of moist and dry soils (Grossman et a f . , 1968). It is called the coefficient of linear extensibility (COLE). The potential volume change of a soil horizon may be obtained by multiplying the COLE value by the horizon thickness, and horizons may be summed together to get the change for a soil pedon. The Soil Conservation Service (U.S. Department of Agriculture, 1971) defines five classes of soils grouped on the basis of COLE, PVC values, and the unified class of the soil material. The limits are as follows: Very low LOW

Moderate High Very high

COLE values of 0.01 or less, PVC of 1.O or less, and Unified classes are SP, SM, SP-SM, and GP. Some are ML. COLE values of 0.01-0.03, PVC of 1-2, unified classes may be CL, SC, ML, ML-CL. COLE values of 0.03-0.06, PVC of 2-4, and mostly unified CL classes. COLE values of 0.06-0.09, PVC of 4-6, and mostly unified CH classes. COLE values of more than 0.09, PVC of more than 6, and mostly CH classes.

Soils occurring in the humid part of the United States, where intense droughts are not common, may not experience much soil movement, even though they may be classed as having a high potential. Soils in the more droughty sections (especially soils with ustic and xeric moisture regimes) are notorious even when classed as moderate. The natural soil must occur in an environment of wetting and drying to gain the full shrink-swell potential.

SOIL S U R V E Y INTERPRETATION

275

2 . Soil Erodibility The K factor rating assigned to soils is used to group soils with similar water erodibility behavior. The K factor is one of the components of the universal soil loss equation. It is either measured or estimated from soil characteristics of the soil horizon. The K factor represents the erosion rate per unit of erosion index for a specific soil in continuous cultivated condition on a 9% slope 72.6 feet long (Wischmeier and Smith, 1965). Two methods have been used to measure soil erodibility. The first approach which measures soil movement in plots, is costly and time-consuming. The second approach involves the use of a rainfall simulator (Meyer and McCune, 1958). This process is less costly than the first, but it is still time-consuming, with data available for only about 1% of the soils. Several workers have advanced empirical formulas to compute K values from easily measurable basic soil parameters (Wischmeier et al., 1971; Moresco and Gray, 1977; El-Swaify and Dangler, 1977). For the surface horizon the following properties have appreciable predictive value: percentage of silt plus very fine sand, percentage of sand coarser than 0.1 mm, sum of the iron and aluminum extracted by the reducing agent sodium dithionate, and the silicone extracted by dithionate citrate. For tropical soils in Hawaii, El-Swaify and Dangler (1977) reported that the base saturation, particle size, mineralogy reflecting amorphous constitutents, and aggregate stability were strongly correlated. However, these models are limited by the number and distribution of measured plots. One of the difficulties in assigning K values is inherent in the definition. Values are estimated for a 9% slope. This may not be the typical or model slope of the soil series. Errors can be made when adjusting measured erosion from a plot that was not 9%. Soils are also grouped on the basis of allowable soil loss. The index is expressed in tons per acre per year. It is an estimate of the amount of soil loss that may be tolerated while maintaining indefinitely a high level of production by economic means over a reasonable length of time. The ceiling of 5 tons per acre per year is an estimate of the maximum amount of downstream sedimentation that can be tolerated by the drainage system. The second assumption is questionable because sediment yield is related to the soil loss occumng in fields but is not entirely dependent on soil loss as calculated with the universal soil loss equation. Other sources of sediment, such as roadside ditches, steambank erosion, and gullies, are not included in the soil loss equation, nor is the efficiency of the watershed to trap sediment considered. Present guides (Advisory Soils-6, Soil Erodibility, and Soil Loss Tolerance Factors in the Universal Soil Loss Equation, February 6, 1973) in the Soil Conservation Service for grouping soils into soil loss tolerance classes use soil depth and potential of the substrate for renewal with modem farming techniques. Five classes of allowable soil loss rates in tons per acre per year are defined as follows:

276

LJNDO J . BARTELLI Soil loss tolerance Rooting depth (inches)

Renewable substrates

Nonrenewable substrates

0-10 10-20 20-40 40-60 60

+

Soils with similar wind erosion behavior are grouped according to soil surface texture. The groups recognized by the Soil Conservation Service are as follows: Wind erosion group 1 2

3 4 4L 5

6

Predominant soil texture class Very fine sand, fine sand, sand, or coarse sand Loamy very fine sand, loamy fine sand, loamy sand, loamy coarse sand, or well-decomposed organic matter Very fine sandy loam, fine sandy loam, sandy loam, or coarse sandy loam Clay, silty clay, noncalcareous clay loam, or silty clay loam with more than 35% clay content Calcareous loam and silt loam, calcareous clay loam and silty clay loam with less than 35% clay content Noncalcareous loam and silt loam with less than 20% clay content, or sandy clay loam, sandy clay, or poorly decomposed organic matter Noncalcareous loam and silt loam with more than 20% clay content, or noncalcareous clay loam with less than 35% clay content

3 . Potential Frost Action

Potential frost action is the upward or lateral expansion of soil caused by the formation of segregated ice lenses and the subsequent loss of strength on thawing. The segregated ice crystals are formed when soil temperatures drop into the freezing zone and soil water is available for the formation of ice lenses. As ice crystals begin to form, water is strongly attracted to the ice cell, freezing on contact. The resulting ice lens continues to grow until all water that can migrate has migrated to the lens area. The water movement is influenced by the effective soil-void size. Ice lenses form in soils where the voids are fine enough to hold water under tension but coarse enough to transmit water. Coarse materials transmit water rapidly if saturated, but as the water is removed to form a lens the unsaturated hydraulic conductivity decreases sharply and water ceases to flow. Thus, segregated ice lenses do not form. Instead, ice is continuous and the soil particles are embedded within. Clayey soils hold large quantities of water, but

277

SOIL SURVEY INTERPRETATION TABLE IX Soil Properties Used to Group Soils for Potential Frost Action Soil moisture regimes Ustic, aridic intergrades of xeric, and ustic, xeric intergrades of aridic

Aridic, and ustic intergrades of aridic

Aquic, aquic intergrades

Udic, xeric, udic intergrades of ustic

Low

Fragmental

Fragmental, sandy, sandy-skeletal

Moderate

Sandy, sandy- Coarse-loamy, fine- Coarse-loamy, fineskeletal, loamy. loamyloamy, coarseclayey, and skeletal, clayey, silty, fine-silty, skeletal clayey-skeletal, loamy-skeletal, cindery, ashycindery, ashy, skeletal, medialmedial, ashyskeletal. thixioskeletal. thixiotropic-skeletal tropic, medialskeletal, thixiotropic-skeletal

None

High

CoarseCoarse-silty. tinefine-loamy, silty, ashy. coarse-silty, medial, thixiofine-silty. tropic, peat, loamy muck, muckyskeletal, peat cindery, ashy, medial, thixiotropic ashyskeletal, medialskeletal, thixiotropicskeletal, peat. muck, mucky-peat.

None

Frost action classes

Fragmental, sandy, sandy-skeletal, clayey, clayeyskeletal

None

All textures

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LINDO J. BARTELLI

tension is so high and hydraulic conductivity so low that soil water migrates so slowly to the freezing front that thick ice lenses do not form. Silty soils have the pore size and tension to generate the highest potential for ice segregation. The guide used by the Soil Conservation Service to group soils for potential frost action lists soil family texture classes and soil moisture regimes (U.S. Department of Agriculture, 1973). Texture classes are applied to the average of the whole soil to a depth of frost penetration. Table IX summarizes the SCS guide. Jessberger (1973) summarized the frost-susceptibility criteria used by engineers into three groups based on the following characteristics: ( a ) gradation curves; (b) particle size, frost-heave rate; and (c) phase-interface relation. The gradiation curve and particle size are most popular. Some fixed value, such as more than 15% passing the No. 200 sieve, is used to differentiate between soils. Jessberger warns his readers that these definitions do not relate to the bearing capacity of thawed soil-a weakness with tests that are not made in situ.

4 . Corrosion of Iron and Steel Certain soils are much more corrosive than others. This has led to a comprehensive study of the relation between soil characteristics and rate of corrosion (Olson, 1964). An explanation of the processes and a set of guidelines for grouping soils are presented in the SCS guide for interpreting engineering uses of soil (U.S. Department of Agriculture, 1971). Soil properties used to group soils include soil drainage class, soil texture, salt concentration of the soil solution, and total extractable acidity and permeability. The pH is used when it falls below 4 or is 7 and above. Soils with fluctuating water tables exhibit a higher probability of corrosion, as does that part of the soil near the boundary to another soil with a different drainage condition. The zones between soil horizons also are more apt to promote corrosion. The classes used by SCS are defined as follows: LOW

Moderate

High

Well-drained coarse and medium texture, and somewhat poorly drained coarse texture; soils are moderately to rapidly permeable; total acidity is less than 8.0 meq per 100 g of soil, or electrical conductivity of the saturation extract is less than 0.2 mmholcm at 25°C Well-drained moderately fine texture, moderately well-drained medium texture, somewhat poorly drained moderately coarse texture, and very poorly drained with all textures; moderately slow to slow permeability; total acidity ranges from 8.0 to 12 meq per 100 g of soil, or electrical resistivity at field capacity is 2.000-5.000 ohm-cm at 6C"F, or electrical conductivity of the saturation extract is 0.2-0.4 mmho/cm at 25°C Well-drained and moderately well-drained fine texture, moderately well-drained moderately fine texture, somewhat poorly drained medium texture, and moderately fine texture and poorly drained where water table fluctoates; total acidity exceeds 12.0meq per 100 g of soil, or electrical resistivity at moisture equivalent is below 2.OOO ohm-cm at 60"F, or electrical conductivity of the saturation extract is greater than 0.4 mmho/cm at 25°C

SOIL SURVEY INTERPRETATION

279

5 . Corrosion of Cement

Soils are also grouped according to the potential for inducing corrosion of concrete material placed on or in the soil. The classes are defined on the basis of those soil properties that influence corrosivity the most. These soil properties are (a) the amount of sulfates, (b) the soil texture of the zone in contact with the concrete material, and (c) the acidity of the soil material. The classes med by the Soil Conservation Service (U.S. Department of Agriculture, 1971) are as follows: Low

Moderate

High

( I ) soils with coarse and moderately coarse texture, organic soils with pH above 6.5, and soils with medium and fine textures with pH above 6.0, and (2) soils with less than 1.000 ppm of water-soluble sulfate (as SO,) ( I ) soils with coarse and moderately coarse textures, organic soils with pH of 5.5-6.5, and soils with medium and fine textures with pH of 5.0-6.0, and (2) soils with 1.000-7.000 ppm of water-soluble sulfate (as SO,) (1) soils with coarse and moderately coarse texture, organic soils with pH of 5.5 or less, and soils with medium and fine textures with pH of 5.0 or less, and (2) soils that contain more than 7.000 ppm of water-soluble sulfate (as SO,)

6 . Hydrologic Soil Groups

Soils are grouped on the basis of the amount of runoff waters when the soil system is at maximum wetness. These soil groups are used to calculate runoff from watersheds. Such soil properties as infiltration rate, permeability rates, and impervious soil or rock layers that influence the rate that excess water moves through the soils are used to define the groups. Soils are grouped, however, on those soil characteristics that influence the soil-water behavior properties. The soil characteristics and the limits for each group used by the Soil Conservation Service are as follows: Group A Group B Group C Group D

Low runoff. Deep, well to excessively drained sands or gravel. Moderate runoff. Moderately deep to deep, moderately well- to well-drained soils with moderately fine to moderately coarse textures. Moderately high runoff. Soils with layers that impede downward movement of water, or soils with moderately fine or fine texture. High runoff. Clay soils with high swelling potential when saturated, soils with permanent high water table, and soils with impervious soil or rock layer at or near the surface.

7 . Other Groupings of Soils Many other groupings are used to interpret soil surveys. Some of the groupings related to engineering uses of soils are as follows: (a) septic tank absorption fields; (b) sewage lagoons; (c) shallow excavations; (d) dwellings without basements; (e) sanitary landfills; (f) trench-type sanitary landfills; @) area-type sani-

280

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tary landfills; (h) source of cover material for area-type sanitary landfills; (i) local roads and streets; (j)road fill; (k) source of sand and gavel; and ( l ) sources of topsoil (U.S. Department of Agriculture, 1971). Soil criteria considered in these classifications are those features that influence soil behavior. For example, the groupings that segregate soils for use as septic-tank absorption fields rely on those soil properties that affect the movement of water through the soil. Such soil properties as shrink-swell, compaction, and textures are used for grouping soils for road fill, local roads and streets, and behavior patterns for dwellings.

B. PLANT-SOIL INTERPRETATIONS

The plant-soil relationship is an important part of the concept of soil productivity. Production from a tract of land depends on the kind of soil, its climate, what man does to the soil, and his skill in doing it (Aandahl, 1960). The things man does in that part of the management system is based both on past experience and on knowledge of the plant-soil relationship. The plant-soil relationship is based on those soil properties that affect root ramification-namely , those that affect soil moisture supply, and those that affect the supply of plant nutrients. Manipulation of these soil properties is a part of the management inputs. The management system usually reflects the most efficient combination of production goals and production inputs. As Aandahl(l960) points out, the production function is not simple. It involves proper crop selection, proper timing of management inputs and a clear understanding of plant-soil relationships. The measurable soil properties that influence plant-soil relations are effective depth of the root ramification zone, particle size distribution, organic matter content, salt content, cation exchange capacity, base saturation, kind of clay mineral, permeability, saturated and unsaturated conductivity, soil wetness, depth to perched or apparent water table, available water-holding capacity, thickness of surface horizon, and shape and degree of soil slope. I . Crop Selection and Yield

The most useful expression of soil productivity has been in terms of crop yields. Crop yields are usually given for each soil mapping unit in a soil survey report (Alexander and Paschke, 1972). One should not assume, however, that yield figures in a soil survey report are based on research conducted in all soils. The ccst of such an undertaking would be prohibitive. The usual procedure is to study key bench-mark soils in detail. Predictions are extended from studied soils to others on the basis of key soil characteristics. Parameters for grouping soils are derived from these detailed soil studies. Ode11 (1950) reported from such studies in Illinois that thickness of the A, horizon affected corn yield on Mollisols. The

SOIL SURVEY INTERPRETATION

28 1

degree of influence varied with the character of the subsurface horizons. Odell (1950) also reported that the Tama soil with a friable, permeable subsoil was much more productive than the Swygert soil, which has a dense and slowly permeable subsoil. Illinois soils were grouped into five classes for yield predictions (Odell, 1958). These groups were defined as follows: (1) Predominantly dark-colored soils developed from glacial till and outwash. (11) Predominantly dark-colored soils developed from medium to thick loess. (111) Moderately dark- and light-colored soils developed from loess over strongly weathered till. (IV) Moderately light- and light-colored soils developed from thin loess over strongly weathered till. (V) Predominantly light-colored soils developed from thin to moderately thick loess on bedrock or weathered till. Yields for corn, oats, soybeans, wheat, and hay are presented under four levels of management for each major soil group. Soil properties used to develop estimated crop yields on Iowa soils (Schrader et al., 1960) were parent material, organic matter level, subsoil permeability, natural internal aeration, slope, erosion hazard, and subsoil suitability for plant rooting. Key soil characteristics listed for bench-mark soils in the Illinois report (Odell and Oschwald, 1970) were surface color, natural drainage, aeration, profile permeability, available waterholding capacity in root zone, rooting depth, and nutrient supplying power (P and K) of the soil. Soil characteristics for top-yielding bench-mark soils (Tama, Muscatine, and Flanagan soils) are used to identify the top producers. Other, less-favorable soils are scaled down accordingly. For example, the Tama and Muscatine soils are assigned a productivity index for basic management of 100. The Cisne soil, with poor natural drainage, very slow permeability, about 25 cm of available water in the rooting depth, about 100 cm rooting depth, and low P and K supplying power, is assigned a basic value of 60. Other soils are assigned indexes on the basis of the relative favorability of the selected soil characteristics. The productivity indexes and crop yields indicate the adaption of various crops to different soils. Factors that influence plant adaption are the soil characteristics that affect the rooting medium of the plant, such as root ramification zone, nutrient status, toxic amounts of minerals, and water supply. Basically, these are the same soil characteristics that most strongly influence crop yield. A study of the relation between plant communities and soil taxonomic units in a pristine range area of southern Idaho indicates that such soil characteristics as depth to bedrock, nature of the bedrock, content of coarse fragments, depth to and presence of a clay B horizon, slope and exposure that influence the distribution, and

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akailability of soil moisture are important factors in determining the composition of plant communities (Hugie et al., 1964). With mean annual precipitation of about 330 mm in the study area and with a short supply of summer rains, those soil factors that influence soil moisture overshadow other soil characteristics. If rainfall is not limiting, other factors such as nutrient status become more influential. In the report of the soil survey of LaSalle County, Illinois (Alexander and Paschke, 1975), small grains were not recommended for soils that flood annually; cultivated crops are restricted from shallow and steep sloping soils; and limited water-storage characteristics of the sandy soils restrict the use of small grains. Trees and permanent grasses were recommended on the very steep erosive soils. The following soil characteristics were used by Alexander and Paschke (1975) to group the soil mapping units into management groups: soil depth, slope, permeability, available moisture capacity, natural fertility, and acidity of the soil surface. Capability unit groupings in other soil survey reports are based on similar criteria. 2 . Tree Planting Guide In grouping soil mapping units for developing tree planting guides, one aims to match the rooting habits, moisture demands and tolerance, nutrient demands, and TABLE X Partial Forest Tree Planting Guide for Northern Illinois Planting trees for forests Sheltered sites: coves north and east slopes

Exposed sites: ridges south and west slopes

Soils that are welltomoderately well drained in upland position, with moderate permeability

White oak, red oak, black walnut, white pine

Spruce, Douglas fir, red pine, jack pine, Scotch pine

Soils that are moderately well drained in upland position, with moderately slow permeability

Red oak, white pine, cottonwood, Osage orange

Larch, Douglas fir, red pine, jack pine, red cedar, Scotch pine

Soils that are poorly drained, in upland and bottomland position with moderate to moderately slow permeability

Silver maple, cottonwood. ash, sycamore

Soils that are well drained in terrace and outwash position with rapid permeability

White oak, black oak, white pine

Soil group

Red pine, Scotch pine

TABLE XI Partial Tree Planting Guide for Ornamental Planting in Northern Illinois Trees

Soil group

Shade

Street

Lawn

Hedges. screens, and windbreaks

Exposure

Tulip tree, black gum. sweet gum

East red cedar, LomColorado spruce, white birch, Eurobardy poplar, tree pean mountain ash. lilac Amur maple

Sun

White oak, green ash. sycamore

Little leaf linden. mountain maple, sweet gum

Colorado spruce. Quaking aspen, Canada Norway spruce. hemlock, Lombdrdy white birch. poplar. tree lilac flowering dogwood

Partial shade

White ash, sycamore, striped maple

Ginkgo tree

Red bud, Norway spruce, flowering dogwood, mountain ash

Shade

Well to moderately European beech, well drained upland Norway maple. soils with moderare sugar maple. red permeability oak. pin oak

East red cedar. quaking aspen, hedge maple

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LINDO J. BARTELLI

salt tolerance of the plant with soil characteristics. Thus, an apple or pear tree that can tolerate wet rooting conditions is more suitable for a soil with slow permeability and some poor drainage characteristics than a peach or cherry tree that prefers deep, well-aerated soils. The generalized tree planting guide prepared for the soil survey report of Ela Township, Illinois, grouped soils according to soil drainage, permeability, depth to water table, wetness condition, and landscape position and exposure (Newbury et al., 1961). A partial forest tree planting guide is presented in Table X. Guides for ornamental plantings also can be prepared. Table XI is an example of an ornamental tree planting guide. Adapted plants are selected on the basis of their environmental requirements and are matched with key soil characteristics.

C. SOIL SURVEY INTERPRETATIONS FOR LAND USE SUITABILITY ANALYSIS

The basic input for most land use suitability analyses is the natural soil unit delineated on soil maps. The soil is an ideal unit on which to make decisions concerning land resource development. A soil survey can serve as the basis on which an economic and social classification can be superimposed for land development. The various classes of land use can be summarized as follows (Bartelli, 1962; Bauer, 1966): Farming-includes those cultural activities dealing with managing and producing food and fiber crops except wood trees. Residence-includes single and multidwelling units less than three stories high. Woodland-includes land managed for production of wood products. Recreation-includes land used for either natural (undeveloped) or developed facilities such as camping and picnic grounds, playgrounds, and golf courses. The natural phase includes wilderness areas, wetlands, and range and forest preserves. Commercial and light industry-includes, in addition to commercial and industrial parks, large school complexes, highways, and airports. Sanitation treatment-includes such waste treatment measures as distribution fields for septic tanks, waste stabilization ponds, sanitary landfills, and spreading of biodegradable solids and liquids. After the several kinds of land uses have been selected, soil properties are used as parameters to define the various suitability classes. The suitability class intergrades various soil properties into a use-behavior prediction. To evaluate the behavior pattern properly, however, one must learn the effects of certain soil

285

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properties on the land use in question. Also, interactions among the several soil properties may be great enough to change the effect of a single property. Thus, before the placement of a soil map unit is made final, one must compare the empirical rating with in situ experience.

I . Farming, Residence, Commercial and Light Industry, Developed and Natural Vegetation, and Woodland Land Uses In the design of a system for classifying soils for farming use, one gives major consideration to those soil properties that influence plant selection and growth, soil erosion, and equipment usage. In the comprehensive interpretation prepared for the Northeastern Illinois Metropolitan Area Planning Commission (Bartelli, 1962), major consideration was given to drainage problems (soil wetness and permeability), drought problems (soil depth, available water supply, soil texture, and infiltration rates), erosion hazards (slope and soil K value), and potential productivity. In addition to some soil properties used in farming, soil stability, shrink-swell, and bearing strength were used for residence requirements. Where on-site sewage disposal systems were used, suitability for waste disposal was added to the class definitions. Depth to rock, depth to free water table, suitability of the soil and substrata for foundations, and availability of sand and gravel were the parameters for defining classes for industry and commercial land use. Table XI1 is an example of a system based on soil wetness as a parameter for defining TABLE XI1 Criteria for Evaluating Soil Wetness for Different Land Uses Use ratings ~

~~

~______

~__________

Soil wetness

Residences

Recreationdeveloped

Commercial and light industry

Wet-soils with free waters at or near surface of soil for some weeks during season of use. Frequent flooding and ponding.

C Severely limited

C Severely limited

Moderately suited

C Severely limited

Somewhat wet-soils with free water between 25 and 100 cm during season of use.

B Moderately suited

B Moderately suited

A Well suited

B Moderately suited

Drained-soils with no ponding or seepage and free water below 100 cm. Do not flood or are protected from flooding.

A Well suited

A Well suited

A Well suited

Farming

B

.

A Well suited

286

LINDO J. BARTELLI

land use classes. In this system three classes were defined. These recommendations should not be misinterpreted. Soil areas rated C, “severely limited, for a particular use can still be developed for that use; however, these areas may be more difficult or costly to develop because of the problems inherent in the soil.

”

2 . Sanitation Treatment Soils are grouped according to their ability to accept and treat wastes. Some of the important soil behavior patterns that should be considered are (a) the amount of a particular waste that a soil can degrade; (b)the specific bacteria and virus kill power of a soil; (c) the quantity of liquid and the rate at which a liquid can be applied; and (d) the cation and anion fixing or exchange capacity of the soil. Several soil characteristics influence these behavior patterns. The clay mineral has considerable influence. The less-active kaolinitic types have lower exchange capacities and hold less water. Soils with high quantities of montmorillonitictype clays are much better performers. The microbial activity in a soil also influences the soil’s ability to break down and destroy wastes. Soil temperature, pH, soil depth, organic matter content, soil moisture regime, and inorganic

TABLE XI11 Suggested Key for Classifying Soils for Waste (Bicdegradable) Treatment Sites Use classes

Item affecting use Clay content (expandable) Clay content (nonexpandable) Sand content Organic matter (surface mineral horizons) CEC (rneq1100 g soil) Base saturation (sum of bases) Hydraulic conductivity Soil temperature (family class) Soil moisture PH Depth to water table Depth to hard rock, or impervious layer Slope Percolation rate Flooding

Good performers >5%

>IS% <90% >2.0%

>6 <50%

>0.6 in./hr Mesic and warmer Humid >5.5% >I m >I m
>60 midin. Less frequent than occasional

Poor performers

<5% 90% <2.0% <6 >50%

<0.6 in./hr Frigid and colder Arid <5.5% 15% (60 midin. Occasional or frequent

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287

nutrient supply will govern the performance of soils. A suggested key for placing soils into two classes is presented in Table XIII. Recent studies indicate that the proper soil is a very effective and efficient waste treatment medium. The results of a study now in progress of a waste distribution field that has been used by the city of Calumet, Michigan, since about 1880 is very encouraging. No evidence of any movement of heavy minerals or bacteria beyond the surface horizon and no evidence of ground water pollution have been noted. Hill and Frank (1974), in their study of the longevity of septic tank systems in Connecticut soils, relate behavior to specific soil properties. The study of liquid waste movement in relation to different septic systems and precise soil morphology by Bouma (1974) will lead to a more effective use of soil maps for the selection of sites and the design of septic systems. The potential of soil is great for renovating waste material. VII. Conclusion

In any soil classification scheme that relies on a single soil characteristic, the tendency is to overlook the influence of the soil as an entity. For example, one may group soils into broad texture classes; but if the grouping is broad enough to include clayey soils composed of both active 2: 1 lattice clays and less-active 1:1 clays, the engineering behavior pattern, the plant response pattern, and even the soil use pattern is too broad to permit sensible predictions to be made. The “Soil Survey Manual’’ (U.S.Department of Agriculture, 1951) carries this important statement on page 7: ‘The influence on soil behavior of any one soil characteristic, or of a variation in any one, depends upon the others in the combination. The final test of any grouping system is to observe the behavior of the soil unit in situ. Predictions of soil behavior are most precise when they are made available to the soil map user directly for the soil mapping unit without any reference to interpretive groupings. Often this procedure is the simplest, for it bypasses the explanation of another set of classification units that may be complicated or difficult. Interpretive groupings do have a place in the use of soil surveys. Interpretive classification schemes lead to studies of the effect of soil characteristics on selected soil behavior. Interpretive groupings also facilitate the study of relationships between soils, and many interpretive groupings employ the language of the specific soil map user. This chapter has summarized the many technical grouping systems used by the Soil Conservation Service and by other agencies making soil surveys. All systems rely on salient soil properties that are collected during the making of a soil survey. The soil scientist, however, never loses sight of the overall objective of the soil survey-that is, classifying the natural soil, noting its distribution on a map, and observing the soil behavior. ”

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Aandahl, A. R. 1961. Trans. Int. Congr. Soil Sci., 7th, I960 Vol. IV, pp. 365-370. Alexander, J. D., and Paschke, J. E. 1972. Ill., Agric. Exp. Sin., Soil Rep. 91. Asphalt Institute. 1969. “Soils Manual for Design of Asphalt Pavement Structure,” 2nd ed., 3rd printing. Asphalt Inst., Houston, Texas. Bartelli, L. J. 1962. J . Soil Water Conserv. 17, 99-103. Bartelli, L. J. 1966. J. Soil Water Consent. 21, 3-6. Bauer, K. W. 1966. In “Soil Surveys and Land Use Planning” (L. J. Bartelli, ed.), pp. 42-59. Soil Sci. SOC.Am. & Am. SOC.Agron., Madison, Wisconsin. Bouma, J. 1974. Soil Sci. Soc. Am., Proc. 38, 941-946. Camp, W. J. 1968. ‘‘Soil Survey of Spartanburg County, South Carolina.” Soil Conserv. Serv., U.S. Dep. Agric., Washington, D.C. Casagrande, A. 1947. Pror. Am. Soc. Civ. Eng. No. 2351, 901-991 Cline, M. G. 1949. Soil Sci. 67, 81-91. Dittmar, G. W., Dieke, M. L., and Richmond, D. L. 1977. “Soil Survey of Medina County, Texas. ” Soil Conserv. Serv., U.S. Dep. Agric., Washington, D.C. El-Swaify, S. A., and Dangler, E. W . 1977. Proc. Natl. Conf. Soil Erosion, 1976, pp. 105-114. FAO. 1976. “A Framework for Land Evaluation,” Soils Bull. 32. Soil Resour. Dev. & Conserv. Serv., Land Water Dev. Div., FAO, Rome, Italy. Fenneman, N. M. 1938. “Physiography of the Eastem United States.” McGraw-Hill, New York. Gromko, G. J. 1974. Proc. Am. Soc. Civ. Eng. 100, No. GT6, 667-687. Grossman, R. B., Brasher, B. R., Franzmeier, D. P., and Walker, J . L. 1968. Soil Sci. Soc. Am., Proc. 32, 573-577. Hammond, E. H. 1964. Ann. Assoc. Am. Geogr. 54, 11-23. Hedge, A. M., and Klingebiel, A. A. 1957. V . S . , Dep. Agric., Yearb. Agric. pp. 400411. Henry, E. F., and Dragoo, M. C. 1965. “Guide to Use of FHA and PVC Meter, Including Results of Nationwide Soil Tests and Correlation with Climatic Factors,” FHA-595. Fed. Housing Admin., Washington, D.C. Hill, D. E., and Frank, C. R. 1974. Conn., Agric. Exp. Stn., New Haven, Bull. 747. Huckle, H. F., Dollar, H. D., and Pendleton, R. F. 1974. “Soil Survey of Brevard County, Florida.” Soil Conserv. Serv., U.S. Dep. Agric., Washington, D.C. Hugie, V. K., Passey, H. B., and Williams, E. W. 1964. In “Forest Plant Physiology and SoilRange Relationships” (J. E. McClelland et al.. eds.), Spec. Publ. No. 5, pp. 190-204. Am. SOC.Agron, Madison, Wisconsin. Jessberger, H. L. 1973. Highw. Res. Rer. 429, 4 0 4 6 . Kellogg, C. E. 1961. “Soil Interpretation in the Soil Survey.’’ Soil Conserv. Serv., U.S. Dep. Agric., Washington, D.C. Klingebiel, A. A. and Montgomery, P. H. 1961. US..Dep. Agric., Handb. Agric. 210. Lemmon, P. E. 1969. In “Southern Forest Soils” (P. Y. Bums, ed.), pp. 31-33. Louisiana State Univ. Press, Baton Rouge. Lohnes, R. A., and Demirel, R. 1970. Iowa State Vniv., Eng. Res. Inst.. Prog. Rep. No. 2 . Mackney, D. 1974. In “Land Capability Classification,” Tech. Bull. No. 30, pp. 4-1 1. Meyer, L. D., and McCune, D. L. 1958. Agric. Eng. 39, 644-648. Mitchell, C. W. 1973. J. Soil Sci. 24, 41 1-420. Moresco, F. R., and Gray, F. 1977. Proc. Natl. Conf. Soil Erosion. 1900,pp. 127-134. Newbuny, R. L., Bushue, L. J., Kubalek, E. E., Link, V. G., and Paschke, J . E. 1961. “Ela Township Soils.” Soil Conserv. Serv., Champaign, Illinois. Nichols, J. D., and Bartelli, L. J. 1974. J. Soil Water Conserv. 29, 232-235. Odell, R. T. 1950. Agron. J. 42, 282-291.

SOIL SURVEY INTERPRETATION

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Odeil, R. T. 1958. Soil Sci. SOC. Am., Proc. 22, 157-160. Odell, R. T.. and Oschwald, W. R. 1970. Ill., Univ., Coop Exi. Sew., Circ. 1016. Olson, G . W. 1964. N.Y., Agric. Exp. Sin., Iihaca, Mem. 387. Orvedal, A. C. 1963: Soil Sci. 67, 62-67. Orvedal, A. C., and Edwards, M. J. 1941. soil i c i . SOC. Am., Proc. 6, 386-391. Riecken, F. F. 1963 Soil Sci. 96, No. 1, 49-61. Schrader, W.D., Schaller, F. W., Pesek, J. T., Slusher, D. F., and Rieckers, F. F. 1960. Iowa, Agric. Home Econ. Exp. Sin., Spec. Rep. 25. Shiflet. T. N. 1973. “Range Sites and Soils in the United States,’’ pp. 26-33. Australia Rangelands Panel. Stewart, B. A., Woolhiser, D. A., Wischmeier, W. H., Cam, J. H., and Frere. 1975. “Control of Water Pollution from Cropland,” Vol. I. U.S. Dep. Agric. and U.S.Environ. Prot. Agency, US Govt. Printing Office, Washington, D.C. Thornburn, T. H.,and Larson, W. R. 1959. Proc. Am. SOC.Civ. Eng., J . Div. Mech. Found. 85, 1-13. U.S. Department of Agriculture. 1951. “Soil Survey Manual,” U.S. Dep. Agric. Handb. No. 18. U.S. Govt. Printing Offce, Washington, D.C. U.S. Department of Agriculture. 1967. “Soil Survey Investigations,” Rep. No. 12. Soil Conserv. Sew., U.S. Dep. Agric., Washington, D.C. U.S. Department of Agriculture. 1971. “Guide for Interpreting Engineering Uses of Soils,” Stock No. 0107-0332. U.S. Govt. Printing Office, Washington, D.C. U.S. Department of Agriculture 1973. Guide for Interpreting Engineering uses of Soils,” Notice 2, pp. 47-50. USDA, Soil Conserv. Serv., ,Washington, D.C. U.S. Department of Agriculture 1975. ”Soil Taxonomy: A Basic System of Soil Classification for Making and Interpreting Soil Surveys,” Agric. Handb. No. 436. U.S. Govt. Printing Office, Washington, D.C. Wendt, G. E., Thompson, R. A., Larson, K. N . 1975. “Land Systems Inventory, Boise National Forest, Idaho, A Basic Inventory for Planning and Management.” U.S. Dep. Agric., For. Serv., Ogden, Utah. Wilkinson, B. 1974. In “Land Capability Classification,” Tech. Bu1l:No. 30, pp. 23-34. Wischmeier, W. H. 1977. Proc. Narl. Conf. Soil Erosion. 1976 pp. 371-378. Wischmeier, W. H., and Smith, D. D. 1965. US..Dep. Agric.. Agric. Handb. 282. Wischmeier, W. H., Johnson, C. B., and Cross, B. V. 1971. J . Soil Waier Conserv. 26, 179-193.

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SUBJECT INDEX A

Crandallite, I62 Cucumber mosaic virus, 234 Cutworm, black, 234

Agriores, 234 Akaganeite, 17 Alfalfa, 67, 70, 72, 75-76, 89, 190, 202 Allophane, 20, 24 Ammonia nitrate, 182 Anion adsorption, soil, 1-50 Anrhonomous grandis. 141, 15 1 Arachis hypogaea, I25 Arsenate, 31, 34-35

D Dactylis glomerata. 107 2.4-Dichlorophenoxy acetic acid, 15 Diosgenin, 207-209

E B

Eggplant catapillar, 234 Empoasca, 141, 151 Eucalyptus calaphylla. 109

Barbasco, 208 Barley, 72, 86, 199 Bean, 201 Beetle, Colorado, 234 Boehmite, 19 Boll weevil, 141, 151 Bollworm, cotton, 151 Bombus morrisomi. 149 sonorus. 149 Borate, adsorption, 15, 23, 38-39 Bouteloua gracifis, 108 Buckwheat, 198, 199 Budworm, tobacco, 151 Bumblebee, 149

F Fenihydrite, 20 Fertilizer, phosphate rock, 159-206 Fleahopper, cotton, 151 Fluoride adsorption, 39-40 Fluorite, 168-173 Fluorapatite, 161, 162-167, 171 Francolite, 162, 165, 169, 175 Freezing injury, 51-98 process, crop, 55-60 Fusarium wilt. 142

C G

Cactus, 118 Calcite, 23, 27 Calcium, 123, 194 Cereal, winter, 67, 70, 71, 83 Chloride adsorption, 40 Chloroplast, cold hardiness, 86-87 Clover, 199, 201 ladino, 186 red, 72 subterranean, 190-191 Cold hardiness, 5 1-98 Corn, 107, 190, 192, 196, 198, 200-203 see also maize Cotton, 105, 108, 118 hybrid, problems and potential, 129-157 root density, 109-1 10, 120-121

Genetics, cotton fiber, 144-147 disease resistance, 142 hybrid seed production, 147-150 insect resistance, 140-142 Gibberellic acid, 234 Gibbsite, 14, 17-19, 28, 31 Glycine m a , 101, 124 Goethite, anion adsorption, 9-16. 25, 28, 31 Gossypium anomalum, 147 arboreum. 147 barbadense, 132- 153 harknesii, 130, 147, 152 hirsurum, 105, 108, 118, 132-153 Gossypol, 134, 141 Grama, blue, 108 29 1

292

SUBJECT INDEX

H Halloysite, 23 Helianthus annuus, 101, 125 Heliothis, 140, 141, 151 Hematite, 11, 16-17 Heterosis, 131- 140, 142- 146 Honeybee, 149

I

Moisture, hardiness role, 70-7 1 Molybdate, adsorption, 15, 35 Montmorillonite, 23 Mustard, 199 Mycorrhizal association, 199

N Nematode, root-knot, 142, 234 Nitrate adsorption, 40

Imogolite, 21 0

J Jassid, 141, 151

Oat, 72, 198 Opuntiu. 118 Orchard grass, 107

K P

Kaolinite, 21-23, 31

Langmuir adsorption model, 2-5, 23, 29-31 Leafhopper, cotton, 151 Leafworm, 151 Lepidocrocite, 17 Leptinotursu decemlineuta, 234 Lespedeza, 72 Lettuce, 199 Ligand exchange, 8, 12, 15, 21, 31-33 Light, hardiness role, 68-70 Liming, 194 Lolium perenne, 107 Lycopersicon esculentum, I23 Lygus, 134 linearis. 141

Pussulidium maxillosum , 234 Peanut, 125 Phenology, heterosis effect, 134-138 Phleum prutense, 107 Phosphate adsorption, 5-6, 15-23, 25-34 rock, direct application, 159-206 Photoperiod, hardiness role, 69 Phyllotretu, 234 Picea sitchensis. 11 I Plant-soil interpretation, 280-284 Poropora, 209-2 15 agronomy of, 229-238 Potato, 219 virus Y, 234 Prosopis juliflora, 109, 118 Pseudutomoscelis seriutus, 141, 151 Pubescence, 150- 152

M Maize, 118, 184, 195 see also corn Manure, 183 Medicugo fulcata, 70 sutivu, 70 Melilotus, 70 Mellissodes, 150 Meloidogyne haplu. 234 Melolontha. 234 Mesquite, 109, 118 Millet, 198 Millisite, 162

R Radish, 199 Range soil grouping, 263-264 Rape, 199 Rice, 196, 200 Root, water-supplying capability, 99- I28 Rye, 86. 199 Ryegrass, 75, :07, 199 S Sceloides cordulis, 234 Selenite, 31. 36

SUBJECT INDEX Silicate, 32 Silicic acid, 39 Sisal, 208 Soil, anion adsorption, 1-50 phosphate reactions, 166-183 survey interpretation, 247-289 SoLanum aviculare, 209-215, 217, 226, 229, 230-238 cyananthum, 219 dulcamara, 217. 220 khasianum, 215-216, 238 luciniatum, 209-215, 217, 223, 226, 229, 230-238 solasodine-bearing species, 210-212 xanrhocarpum, 223 Solasodine production, 207-244 Soybean, 101. 105, 110, 124 rooting volume, 116-1 18 Spodoptera littorulis. 15 1 Spruce, Sitka, 1 I 1 Strengite, 162 Sulfate adsorption, 15, 17, 19, 22. 36-38 Sulfur, 182 Sunflower. 101. 125 Sweet clover, 70

293

Trichophyton verrucoccum, 238 Triticum aestivum, 107, 124 durum, 124

Urea, 182

Variscite, 162 Vermiculite, 23 Vernalization, 75 Verricillium wilt, 142 Viability assay, 91-92

W Water, root role in plants, 99-128 Wavellite, 162 Wheat, 107, 123, 199. 201 winter, 69, 72, 75, 77-80, 84 Whitefly, banded-wing, 141 Winter hardiness, 5 1-98 Woodland soil grouping, 261-263, 282-284 Worm, wire, 234

T Temperature, hardiness role, 67-68, 72, 76 Thiobucillus. 182 Timothy, 107. 199 Tomatidine, 208, 223 Tomato, 123 Transpiration, model equation, 100- 101 Triulurodes abutilonae. 141

A

B

c a

0 9 E

O

F I 6 2 H 3 1 4

J 5

Y Yam. 208 Z

Zeu mays. 107, 108, 114, I18

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