Advances in Ecological Research, Volume 6

Advances in

ECOLOGICAL RESEARCH VOLUME 6

This Page Intentionally Left Blank

Advances in

ECOLOGICAL RESEARCH Edited by

J. B. CRAGG Environmental Sciences Centre (Kananaskis), University of Calgary, Calgary, Alberta, Canada

VOLUME 6

1969

ACADEMIC PRESS London and New York

ACADEMIC PRESS INC. (LONDON) LTD. BERKELEYSQUAREHOUSE BERKELEY SQUARE LONDON,W l X 6BA U.S. Edition published by ACADEMIC PRESS INC. 111 FIFTHAVENUE,NEW YORE 10003, NEW YORK

Copyright @ 1969 by Academic Press Inc. (London) Ltd.

All Rights Reserved NO PART OF THIS BOOK MAY BE REPRODUCED I N ANY FORM BY PHOTOSTAT, MICROFILM OR ANY OTHER

MEANS,

WITHOUT WRITTEN PERMISSION FROM THE PUBLISHERS

Library of Congress Catalog Card Number: 62-21479 SBN: 12-013906-5

Printed in Great Britain by T. & A. Constable Ltd., Edinburgh

Contributors to Volume 6 M. F. BUELL,Department of Botany, Rutgers University, New Brunswick, N.J., U . S . A . C. R. JESSEN,Department of Ecology and Behavioral Biology, University of Minnesota, Minneapolis, Minnesota, U.S.A. A. N. LANOFORD, Department of Biological Sciences, Bishop's University, Lennom'lle, Quebec, Canada. K. H. MANN, Fisheries Board of Canada, Marine Ecology Laboratory, Bedford Institute, Dartmouth, N.S., Canada. D. B. SINIFF,Department of Ecology and Behavioral Biology, University of Minnesota, Minneapolis, Minnesota, U.S.A. A. DE Vos, Forestry and Forest Industries Pivision, F.A.O., Rome, Italy.

This Page Intentionally Left Blank

Preface Ecological organization is the resultant of many processes occurring at very different levels of complexity. The outward signs of organization are the patterns of animals and plants which are described by such words a,community or association. The theme of this volume is the understanding of some basic ecological patterns. The paper by Dr Siniff and Dr Jessen is concerned with a particular type of pattern at the organism level, the concept of “home-range”. Their investigations combine two modern techniques, telemetry and computer simulation, and their study constitutes an attempt to give precision to an important component of more extensive ecological pat terns. The three other contributions are concerned with the form and organization of patterns at the community level. Dr Langford and Dr Buell discuss the nature of the plant association. There is perhaps no more controversial subject in phytosociology and the controversy continues as a glance at Vol. 34 The Botanical Review will show. Dr Langford and Dr Buell describe the background out of which modern views on the nature of the plant community have emerged. Above all, they demonstrate the need for precise experimental studies. The papers by Dr Mann and Dr de Vos share common ground. The trophic web is the pattern through which an ecosystem operates. Dr Mann reviews the dynamics of such patterns in aquatic ecosystems, dealing in detail with the difficulties experienced when at’tempting to obtain reliable measures of energy flow between trophic levels, and of the exchange and circulation of materials. Dr de Vos is concerned, in the main, with the utilization by man of the wild herbivore component of terrestrial ecosystems. His review reveals the tentative and sometimes “guesstimate” nature of much of our information on the production of such systems. Both papers have special relevance in view of current investigations within the International Biological Programme.

J . B. CRAW April, 1969

vii

This Page Intentionally Left Blank

Contents CONTRIBUTORS TO VOLUME 6

PREFACE

-

V

_

-

-

_

vii

The Dynamics of Aquatic Ecosystems

K. H. MANN I. Introduction 11. Progress in the Understanding and Measurement of Production A. Primary Production B. Secondary Production 111. Studies of Whole Ecosystems A. Studies of Energy Flow B. Studies of the Circulation of Materials IV. Studies of Single Species or Groups of Species A. Energetics B. Turnover of Materials V. Studies of Decomposition Process VI. The Search for General Principles A. Various Approaches B. The Use of Microcosms C. Theoretical Models VII. Discussion Acknowledgements Nomenclature Addendum References -

-

1 4 4 16 30 30 37 39 39 53 58 60 60 61 62 65 70 70 71 71

Integration, Identity and Stability in the Plant Association

ARTHURN. LANGFORD and MURRAYF. BUELL I. Introduction - 11. The Biotic Community and the Theory of the Climax A. The Organismic Concept of the Association B. Other Clementsian Concepts and their Modification 111. The Individualistic Concept of the Association, the Continuum and Ordination A, The Linear Continuum as a Quantitative Substantiation of Clements’ Concepts of Succession B. A Criticism of the Linear Continuum C. Recent Reassessments of the Controversy IV. Neutral Approaches to Community and Association Study V. A Modern View of the Association - A. Tansley’s Broadening of the Climax Concept -

ix

84 92 92 93 95 95 96 98 101 104 104

X

CONTENTS

B. The Influence of Dominants C . The Integrated Association D. Homeostasis in the Plant Association E. Ecotones VI. The Question of Critical Levels along Gradual Environmental Gradients A. Introduction B. Mycorrhiza C. Edaphic and Climatic Factors D. Ecotypes E. The Universality of Divisiveness F. Geographical Aspects of the Association Concept, with Special Reference to Stability VII. The Special cases of Auto-intoxication, Synergism and Allelopathy A. Early Work and the Period of Concentration upon Single Factor Explanations of Biological Events B. The Emergence of an Understanding of the Complexity of Biochemical Interactions among the Higher Plants VIII. Concluding Statement References -

105 107 107 111 112 112 113 114 115 117 118 122 122 124 128 131

Ecological Conditions Affecting the Production of Wild Herbivorous Mammals on Grasslands A. DE Vos I. Introduction 11. Basic Ecological Considerations 111. Definitions IV. Descriptions of Grasslands and Savannas A. The North American Grassland Biome B. The African Grassland Biome V. The Ecology of Drought Cycles VI. The Ecology of Fire A. Environmental Alteration - B. Effects on the Vegetation C. Effects on Animals D. Changes in Productivity of the Vegetation VII. Animal Influences on the Grassland Environment A. The Effects of Wild Ungulates on Grasslands B. The Role of Rodents and Lagomorphs in Altering the Grassland Ecosystem C. The Role of Rodent Mounds and Termitaria VIII. Biomass and Energy Production of Herbivorous Mammals A. Basic Considerations B. Available Evidence on Productivity C. A Comparison between Africa and North America in Terms of Biomass Production D. The Effects of Degradation of the Environment on the Productivity of Wild Herbivorous Mammals IX. Management Considerations -

-

-

137 138 140 141 143 144 146 147 147 148 149 149 160 151 155 160 163 163 166 169 170 171

xi

CONTENTS

A. Game Ranching and Utilization B. Range Management for Wild and Domestic Herbivores X. Recommendations and Research Summary and Conclusions References -

-

-

171 174 177 177 179

-

-

A Simulation Model of Animal Movement Patterns D. B. SINIFFand C. R.JESSON I. Introduction11. Basis for a Simulation Model A. Animal Movements B. Home Range 111. The Simulation Model A. Empirical Requirements for a Successful Model €3. Theoretical or Desirable Distributions which Appear Useful C. The Evolution of our Model D. Our Current Model E. Comparison of Telemetry Data and Siinitluted Data IV. Discussion and Future Developments Acknowledgements References - -

-

185 187 187 197 199 199 200 203 210 210 213 217 218

AuTaoR INDEX-

-

221

SUBJECTINDEX-

-

227

-

This Page Intentionally Left Blank

The Dynamics of Aquatic Ecosystems K . H. MA"

Fisheries Research Board of Canada, Marine Ecology Laboratory, Bedford Institute, Dartmouth, N .S., Canada I. Introduction . 11. Progress in the Understanding and Measurement of Production A. Primary Production . B. Secondary Production . 111. Studies of Whole Ecosystems . . A. Studies of Energy Flow B. Studies of the Circulation of Materials . . IV. Studies of Single Species or Groups of Species A. Energetics B. Turnover of Materials . V. Studies of Decomposition Processes . VI. The Search for General Principles . A. Various Approaches . B. The Use of Microcosms. C. Theoretical Models . VII. Discussion . Acknowledgements . Nomenclature . Addendum References .

.

.

.

.

.

1

. .

4 4

.

16 30 30 37 39 39 63 68

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

.

60 60 61

62 66 70 70 71 71

I. I N T R O D U C T I O N It is more than a quarter of a century since Lindeman (1942) proposed the trophic-dynamic model of ecosystems. I n the intervening years the concept has been refined by the contributions of Slobodkin (1962), Macfadyen (1964) and others, and there have been several attempts to verify the model by evaluating the pathways of energy flow in various natural systems (Odum, 1957; Teal, 1957; Teal, 1962; Mann, 1964). The hope has arisen that a body of knowledge would be accumulated which would enable us to have sufficient insight into the workings of ecosystems to be able to manipulate them with confidence and predict the consequencea of our actions. B

1

2

K. H. MANN

On the whole, progress in this direction has been slow. Those systems selected for intensive study have been less complex than the average: for instance constant -temperature springs, or salt marshes, where the fauna is limited by the wide range of conditions encountered. The average ecosystem is so incredibly complex that ecologists interested in dynamics have tended to concentrate their attention on single species or isolated food chains. The aim of this review is to identify the problems

\

detritus feeders

producers

Sun’s energy

Nutrients

FIG.1. Diagram illustrating the trophic structure of an ecosystem and the flow of energy (thick arrows), materials (thin arrows) or both (broken arrows). From K. H. Mann (1967). Reproduced with permission from “The Teaching of Ecology”, p. 105. Blackwell Oxford.

of studying whole ecosystems, to see whether the detailed studies of components of such systems have increased our understanding of the working of the whole, and to examine the adequ9cy of the models that have been put forward. The development of our understanding of the dynamics of ecosystems has consisted chiefly in a progressive clarification of the concepts of production and of the factors controlling food uptake, assimilation and metabolism. Consider the simplified model in Fig. 1. The organisms are divided into groups according to their method of nutrition, and the primary producers are shown as fixing the energy of sunlight along with

AQUATIC ECOSYSTEMS

3

inorganic nutrients, thus synthesizing high-energy organic compounds. A proportion of this energy is released by the plants’ own respiration and some energy and materials pass to the herbivorous animals with their food. Unused plant material dies and decays, transferring energy and materials to the decomposers. The process is repeated at successive trophic levels until we reach the top carnivores, which by definition have no predators, so that all their materials pass to the decomposers in excretion or after death and the energy which does not pass to the decomposers in this way is all respired. Materials passed to the decomposers are ultimately released into the medium, soil or water, and made availbble to the plants. Thus the materials circulate while the energy flows through the system on a one-way basis: it enters in photosynthesis and is finally dissipated as heat to the environment. The model as it stands represents a closed system, but one of the diEculties of applying it to actual situations is that these are never closed, and it is necessary to allow for import and export at each level of the system. One of the main criticisms of simple models, as exemplified by Fig. 1, is that it is not always possible to classify the nutritional habits of the organisms. An important part of the process is the transfer of energy and materials from one group of organisms to another. By growth and reproduction the first group causes an increase in its biomass and in the course of feeding the second group removes some of this increase. If there are two populations, the predator and the prey or the grazers and the grazed, in some sort of steady state relationships with one another, it is all too easy for the observer to notice the small changes in number and biomass which occur in the two populations and fail to notice the large amount of material passing between them. The development of understanding of the dynamics of ecosystems has consisted chiefly in a progressive clarification of firstly the processes of production and eecondly food capture, ingestion, assimilation and metabolism. To make comparisons of results within the whole spectrum of production and trophic ecology it is necessary to have a common set of terms. A list, based on those of Ricker (1968)extended where appropriate is given in the appendix. The basic relationships are: For autotrophic organisms:

P, (net) = P, (gross)- R, - up where: P, = primary production R, = respiration of primary producers U p = excretion of primary producers.

4

K . H. MANN

For heterotrophic organisms:

Ps

=

C-F-Ua-Ra

where: P8 = production by specified heterotrophs (secondary production) C = food consumption F = faeces egested Us = excretion by the specified heterotrophs R8 = respiration of the specified heterotrophs. The equation may be evaluated in terms of energy (usually calories) or in terms of materials such as carbon or nitrogen.

11. PROGRESS IN

THE

U N D E R S T A N D IANNG D MEASUREMENT PRODUCTION

OF

A.

PRIMARY PRODUCTION

The interest of plant physiologists in the process of photosynthesis has meant that the distinction between biomass and plant production has been obvious for a long time. On the other hand, the fundamental concepts pertaining to production by animals, particularly invertebrates, have been clarified comparatively recently and techniques for measuring secondary production have lagged far behind techniques for measuring primary production. The literature on primary production is copious and in this section methods will be emphasized which are of particular interest to an ecologist concerned with whole ecosystems.

1. Production by planktonic algae I n many aquatic ecosystems the chief primary producers are the planktonic algae. There are two main groups of techniques for measuring their production: those involving incubation of samples of water with contained algae in transparent containers and those involving monitoring changes in nutrients or oxygen in natural bodies of water. The incubation methods are particularly fully documented (e.g. Ivlev, 1945; Ryther, 1956b; Strickland, 1960, 1965; Steemann Nielsen, 1963; Goldman, 1966; Raymont, 1966; Margalef, 1967) and there are two main variants. I n one, introduced over 40 years ago (Gaarder and Gran, 1927), changes in dissolved oxygen are followed in water samples in bottles incubated in the light and in the dark. I n the light bottles oxygen changes are brought about by photosynthesis and respiration, while in the dark bottles only respiration should be operating, i.e. light bottles give a measure of P, (gross)- R, - R8

AQUATIC ECOSYSTEMS

5

while dark bottles give a measure of and P, (gross)is obtained by combining the two. In practice the rate of respiration may not be the same in the light as in the dark, and the rate of photosynthesis may be influenced in a variety of ways resulting from the confinement of the algae in the containers. For example, the algae may settle out in the bottles and shade one another. Thus, mechanical rotation of bottles exposed in the River Thames led to a 38 % increase in the estimate of production (Kowalczewski, personal communication). I t is not possible to distinguish between R , and Rsso no direct measurement of net production can be made. Yet net production is the better estimate of what is available to other trophic levels. The second incubation method involves the introduction of 14C into the containers. The radio-activity of the filtered residue a t the end of incubation is considered to be proportional to the amount of carbon assimilated. This method has largely supplanted the oxygen method, particularly in marine ecology, largely because of its convenience and greater sensitivity. Interpretation of the results is complicated by lack of precise knowledge of how much assimilated 14C is released in respiration or excretion, how much is recycled within the cell and how much of the radio-activity of the residue is attributable to sources other than algae. In general, and with appropriate corrections, it is thought to give an estimate of net production. Steemann Nielsen (1963) suggested that a notional figure for algal respiration should be added to give an estimate of gross production. Recently an incubation technique for measuring the uptake of 15Nhas been developed (Dugdale and Goering, 1967). It involves conversion of the fixed nitrogen to gaseous phase and measurement in a mass spectrometer. It probably has not yet reached the stage of being suitable for routine use. In any incubation experiment there is an element of uncertainty as to whether the samples incubated are representative of the area from which they were taken; yet the experiments are too lengthy to replicate freely. One possible approach is to seek a relationship between rate of production, chlorophyll concentration and light intensity. Since chlorophyll and light can be measured much more rapidly than photosynthesis, it should be possible to estimate production at a large number of stations. Ryther (1956a) and Ryther and Yentsch (1957) evolved a relationship which included the terms chlorophyll concentration, surface light intensity, extinction coefficient and a factor of 3.7. They claimed that the latter figure was a mean of ratios of carbon assimilated to chlorophyll concentration ranging from 2.1 to 5.7. Strickland ( 1960) showed that this ratio extends at least from 1 to 10 and that the figure

6

K. € MA" I .

3.7 has little meaning as a basis for generalization. However, in a particular time and place, with a fairly homogeneous population of primary producers, there seems no reason why a good relationship between light and chlorophyll should not be used as a basis for extrapolation of production data. Kowalczewski (unpublished) working on plankton production in the River Thames expressed light intensity and extinction coefficient as depth of compensation point, d, and obtained the relationship

P, (net) = 0.497 Ch x (d - 0.77) x 0.2698 where P, (net) = net primary production in mg 0,/m3/day Ch = g chlorophyll/m3. Another variant on the incubation techniques which holds perhaps the greatest potential value to the ecosystem ecologist is that used in conjunction with a Coulter particle counter. It was introduced as a field method by Cushing and Nicholson (1966) and has since been used by Sheldon and Parsons (1967) and Parsons et al. (1969a). The principle is that a water sample is taken and the size-frequency distribution of the particles in suspension is determined with the counter. From these data the volume of material in each size class may be calculated. Incubation experiments with light and dark bottles are then conducted and the Coulter counter is used to determine changes in particle number and volume. One difficulty is that water samples often contain considerable amounts of suspended detritus, but Cushing and Nicholson evolved a mathematical technique for correcting for this. A succession of determinations of particle volume are made, and used to calculate an apparent growth constant k. Into the calculations are introduced a number of estimates of the volume of detritus, D which is subtracted from the total volume of material present on each occasion. At one of these values of D the growth constant does not change with time. This is taken to be the correct value of D and is used to calculate the true phytoplankton volumes at different times (Fig. 2). An attractive feature of the method is that it enables one to distinguish various size fractions of the population, such as nanoplankton and microplankton, which may be producing at different rates. Provided that grazers have been eliminated from the samples, the data provided are good estimates of net production, in terms of cell volume. A conversion to calories would yield valuable data about the production available to the next trophic level. The main reservations are those that apply to all incubation experiments, namely the effects of confining the producers in an artificial environment, particularly since these experiments normally take longer than 14C experiments.

AQUATIC ECOSYSTEMS

7

Fro. 2. Data obtained with a Coulter Counter on water from Departure Bay, British Columbia, incubated at 10°C. (a) Variation in k (the apparent growth constant) with time, at different values of D (the estimated volume of detritus). (b) Slope of lines in (a) plotted against D. Broken lines indicate point of zero slope. From R. W. Sheldon and T. R. Parsons (1967) Reproduced with on the Use of the Coulter Counter”, p. 44. Coultkr Electronic Sales

from “A Practical Manual E”,.,mission East Toronto, Canada.

Turning now to methods of measuring primary production which do not involve incubation, we find that these consist of measuring changes of concentration of oxygen or nutrients in the water mass, and relating these to the amount of production that has taken place. As early as 1922 Atkins published an estimate of vlgal production in the English Channel, based on measurements of the decrease in CO, content of the water. He found that between July and September there was a decrease of 1.2 mg/l of carbon, equivalent to a fixation of 100 g C in the water column beneath 1 m2 or synthesis of 250 g dextrose per ma. He then remarked, “Were photosynthesis to remain uniform and respiration in abeyance it is obvious that there would be a vast accumulation of carbohydrate in the sea. As it is, the amount present is an equilibrium between the production due to photosynthesis and the destruction by plant and animal respiration.” Cooper (1933) followed with estimates of production in the English Channel based on changes in concentration of CO,, O,, phosphate and nitrate at 10 stations. At that time i t seemed that nutrients were fairly uniformly distributed over the area of study at the time of winter maximum and that the decreases at different places were reflections of the amount of assimilation that had taken place. He realized that his estimates were minimal, since any recycling or influx of nutrient-rich water would tend to minimize the decrease in nutrients. His figures ranged from 1000 metric tons/km2 (wet wt) based on 0, to 1600 tons based on CO,. Atkins’ earlier results,

8

K. H. MA"

expressed in the same way, were 1400 metric tons/km2, suggesting that the correct order of magnitude had been reached. However, in a study of the chemical oceanography of the English Channel in the period 1947-50 it was found that the distribution of nutrients was far from uniform at the time of the winter maximum and that the pattern of circulation varied considerably from year to year. Cooper (1958) therefore concluded that it was not practicable to use the apparent consumption of nutrients as an index of primary production in the English Channel. Strickland (1960) concluded that the method was likely to yield very inaccurate results unless there was detailed knowledge of vertical and lateral transport of nutrients and of the magnitude of regenerative processes. Riley (1956), working in Long Island Sound, calculated production and utilization of organic matter from the observed changes in distribution of both phosphate and oxygen. He assumed that lateral transport and diffusion could be ignored and corrected for vertical eddy diffusivity. Utilization of phosphate in the upper 2.5 m proved to be fairly uniform throughout the year, and net uptake of phosphorus extended to 17.5 m during the spring bloom. The maximum amount of regeneration occurred at the bottom in summer, but in autumn and early winter regeneration exceeded uptake in all but the upper 2.5 m. By complex manipulation of data on net oxygen changes in the water column, light and dark bottle experiments, algal respiration as related to the concentration of chlorophyll in the water and zooplankton respiration as calculated from the volume of zooplankton in net samples, Riley was able to calculate estimates of gross and net production and the respiration of the various components of the ecosystem for 10 separate periods in 1952-54. He concluded that the mean annual gross production was 470 g C/m2 and net primary production 205 g C/m2. On the basis of the oxygen budget 69% of production appeared to be used by pelagic organisms and 31 % by benthos. On the basis of phosphate analysis the figures were 61 yoand 39 yo respectively. The phosphorus cycle has also been used as the basis for estimates of primary production in the Gulf of Maine (Redfield et al., 1937; Ketchum and Corwin, 1965). The second set of observations were limited to a 10-day time interval but were made on a water mass the movement of which was tracked with a parachute drogue. Good agreement was obtained between estimates of primary production from P removed, organic P produced, 0, produced and increase in chlorophyll a. They ranged from 2.08 to 2.21 g C/mZ/day. Steele (1958) made further progress with the depletion of nutrient method by choosing an area of study where lateral transport was thought to be unimportant, and by evolving a method for correcting

AQUATIC ECOSYSTEMS

9

for vertical transport. He worked on the Fladen Ground of the North Sea and studied changes in the phosphate concentration at intervals in the photic zone, and a t the bottom (140 m). During the season of production he found that phosphate decreased in the upper 30-40 m and increased in the deeper water. He assumed that only production occurred in the upper layer and only regeneration in the lower. He corrected for vertical water mixing and calculated the change in phosphate concentration attributable to biological activity. Using a conventional ratio between carbon and phosphorus he estimated production on the Fladen Ground as 55-81 g C/m,/yr, these figures being close to the earlier estimates for the English Channel and to Teal’s estimate for Vineyard Sound. He made a limited number of 1*C determinations and obtained good agreement between the two methods. Teal and Kanwischer (1966) pointed out that the measurement of pC0, is more sensitive to biological activity in sea water than is the measurement of oxygen. By combining CO, budgets with estimates of primary production by the method of Ryther and Yentsch (1957), they drew up a budget for production processes in Vineyard Sound, near Woods Hole. Changes in pC0, were monitored by pumping sea water to an equilibration chamber from which gas was circulated to an infra-red dCO, gas analyser. The ratio of change of pC0, to total CO,, dpC0,’ was determined a t various salinities in the laboratory. Appropriate corrections were made for exchange with the atmosphere a t various wind velocities and for changes in p C 0 , due to temperature changes. No attempt was made to calculate the effects of lateral or vertical mixing, and measurements made near the surface were assumed to represent the whole of the mixed layer. The results are shown in Fig. 3. The change in total CO, reflects net production, compounded of photosynthesis less community respiration, P , - R, - R,,and this was found to be positive in winter and negative in summer. Calculated photosynthesis was highest in summer, with a smaller peak in winter. Respiration, R, + Rd, calculated by subtracting net production from calculated photosynthesis ranged from a few percent of photosynthesis during winter to 2.3 times photosynthesis in early autumn. Calculated photosynthesis over an 11-month period of observation totalled 70 g C/m2 while respiration totalled 7 7 g C/m2, suggesting that the ecosystem approximated to a steady state condition, with the annual gross production being balanced by the respiration of the plants and animals. A good example of the combined use of “open water” and incubation techniques for determining primary production is that of Gilmartin (1964). Working in Indian Arm, a fjord in British Columbia, he studied the physical oceanography intensively for three years until he could

10

K . H. MANN Chlorophyll A (n

E \

c3

5

N

E

Calculated photosynthesis

\

c

0

20

a

I

N 1961

DIJ F

M A 1962

MIJ J

A

s O N D ~ JF M 1963 1964

O N D J F M A M J J A S O N D J F M 1961 1962 1963 1964 FIG.3. Changes in chlorophyll A and p C 0 , in the waters of Vineyard Sound and the net

production and total photosynthesis calculated from them. From J. M. Teal and J. Kanwischer (1966). Reproduced with permission from J . mar. Re#. 24, Fig. 3.

determine the pattern of circulation and water replacement. During the third year (1958-59) he was able to calculate the monthly rate of oxygen transport by freshwater runoff and inflowing and outflowing salt water. After correction for surface diffusion he was able to calculate the net changes in oxygen due to biological activity. These when converted to carbon equivalent, suggested a net production (gross)- R, - &) of 381 g C/m2/yr. In periods when the deep basin was cut off from the mixed layer and from advective processes, he calculated the rates of (f'b

11

AQUATIC ECOSYSTEMS

oxygen depletion, and extrapolated these to obtain an estimated mean of 290 g C/m2/yr. Arguing that the same rate of respiration probably applied to the upper layer, he suggested that gross production was of the order of 381 + 290 = 671 g C/m2/yr. Independently he made estimates of primary production and respira-

.

0

*9 0 \

N

E

\

‘

“

.

‘

‘

.

‘

.

L

80. .

* 60 -

I

*

.

Net oxygen productlon

40’

20-

o’,

/ L

N

J

M

M

J

S

1958 /59

FIG. 4. Annual cycles of oxygen utilization, oxygen production and grow primary production in a British Columbia fjord. From Y.Oilmartin (1964). Reproduced with permisaion from J . Fish &S. Bd. Can. 21, Fig. 12.

tion throughout the water column by incubation techniques and arrived at estimates of 609 and 455 g C/m2/yr for gross and net production, suggesting that gross production does indeed lie in the range of 600-676 g C/m2/yr. The difference between net production in the euphotic zone and respiration in the deep water indicates a surplus production available for export. Comparison of the annual curves for gross production, net oxygen production and oxygen utilization (Fig. 4) suggests

12

K. H. MA"

that material produced during spring and early summer tends to be used within the fjord, while that produced in autumn tends to be carried out, impelled by the flow of fresh water from the land. Although the examples used in the preceding section are all drawn from marine ecology, parallel developments have taken place in limnology. The light and dark bottle method has continued to yield valuable results, particularly in the more productive freshwater situations (e.g. Hepher, 1962; Talling, 1965) and the 14C method has been widely used (Goldman, 1963). Changes in the 0, or CO, content of the water have been used to calculate production in lakes (Jackson and McFadden, 1954; Talling, 1957) but this method has proved particularly valuable for measuring the productivity of rivers. Most of the primary productivity of rivers is attributable to attached benthic plants, which by their mode of life are prevented from being swept away by the current. The techniques used in their study are rather distinct and form the subject of the next section. 2. Production by benthic plants

I n the littoral zone of fresh and salt water habitats an important contribution to primary production is made by macrophytes. I n temperate climates they often show a marked annual rhythm of growth, and annual production can be determined by concentrating measurements in the growing season. Indeed, as a first approximation it can be assumed that the maximum biomass achieved by many aquatic macrophytes is close to their annual net production (Westlake, 1966). Borutzky (1950) claimed that the net production of Phragmites communis exceeded the autumn standing crop by only 2.2 %, although Penfound (1956) found that the terminal standing crop of Typha latifolia in Oklahoma was considerably less than the total productivity during the growing season. Emergent freshwater macrophytes often have more biomass underground than above it, but the underground material is not renewed annually and the cycle of translocation, storage and utilization must be studied in detail before accurate estimates of total production can be made. However, when due allowance has been made, Westlake (1963) concluded that reedswamps are the most productive systems in temperate zones. The common submerged macrophytes of rivers have a much smaller root system and Owens and Edwards (1962) studied production by measuring the biomass of representative subsamples cut above ground at intervals throughout the growing season. I n this way they obtained estimates of the rate of net production over periods of a few weeks. The method is also valuable as a way of identifying the time of maximum biomass. I n situations where losses to grazers or decomposers are significant the maximum biomass will be consider-

AQUATIC ECOSYSTEMS

13

ably less than the annual production and a better approximation will be obtained by integrating rates of production measured at short intervals throughout the growing season (e.g. Smalley, 1959). Reliable estimates of rates of production of seaweeds are particularly hard to obtain by this method. There is a wealth of data on standing crops in different areas collected by those interested in cropping forms of economic importance (Boney, 1965) and data are available on the rate of growth of the fronds, but animals like echinoids, amphipods and gastropods are known to browse heavily on the seaweeds so that there is a large amount of production which is removed by herbivores before it can be measured. Data quoted by Blinks (1955) and Westlake (1963) indicate that the standing crop of seaweeds is about 100 times as great as the standing crop of planktonic algae per unit area of the sea, and that the annual production is about 10 times as great, of the order of 1000-2000 g C/m2/year. Of course, these figures apply only to a narrow zone adjacent to the land, and seaweed production is small compared with plankton production in the major oceans. In many shallow aquatic habitats attached microscopic algae make a significant contribution to production. A commonly used technique for estimating their production has been the exposure of glass slides or other suitable surfaces in the habitat and a study of the rate of colonization by periphyton organisms (e.g. Maciolek and Kennedy, 1964). At best this must be regarded as an index of relative production, for the rate of colonization of the slides must be a function of the motility of the organisms and is known to depend on the precise nature of the substrate used (Sladeckova, 1966). Moreover, periphyton algae are part of a complex community, named by Ruttner (1964) the aufwuchs community, having its own consumers such as protozoans, bryozoans and nematodes, and the natural populations of algae are in dynamic equilibrium with these, while the new populations on the slides will not have established such equilibrium. An alternative method of determining production of periphyton is to enclose the algae in bottles and use modifications of the oxygen or the 14Ctechniques. Assman (1953) used the oxygen method for measuring the production of algae on reed stems in situ. Using modifications of this method both Straskraba (1963) and Pieczynska and Szczepanska (1966) found that production by periphyton exceeded production by plankton in the littoral zone of lakes. Wetzel ( 1964) placed transparent chambers over macrophytes or periphyton in situ and introduced lac.After incubation the plant material was removed and its radio-activity determined in the gaseous state after combustion. I n a shallow lake in California he found that the average rate of production of the periphyton per unit area was about three times that of the phytoplankton and nearly ten times that of the

14

K. H. MANN

macrophytes. I n the lake as a whole periphyton production accounted for 42 % of the production. Pomeroy (1959) studied the algal production on the surface of an intertidal salt marsh, using bell jars pressed down over the mud surface and determinations of dissolved oxygen. All of these chamber methods are open to the criticism that they cut off the natural water movements which may stimulate production by breaking down the concentration gradients at the plant surface. As was mentioned earlier, monitoring changes in the oxygen content of water has proved a most useful method of studying production in rivers. We saw that for studying production by algae in open water the chief difficulty in using the oxygen budget method was that of obtaining details of vertical and lateral transport. I n running water these difficulties are surmountable since in most rivers there is complete turbulent mixing and the horizontal movement is all in one direction. The principle is that the diurnal rhythm of photosynthesis, associated with more or less constant respiration, gives rise to diurnal cycles of dissolved oxygen, which by analysis can be made to yield information on rates of production and respiration. The method has been used by Winberg (1940, 1955), Odum (1957), Hoskin (1959), Edwards and Owens (1962) and Owens and Edwards (1963). The oxygen concentration of the water is monitored at two stations, preferably in a stretch of river receiving no tributaries or run-off water. The change in oxygen concentration is brought about by photosynthesis, community respiration and exchange at the water surface. During the hours of darkness photosynthesis is eliminated, and diffusion may be calculated from the saturation deficit of the water and an appropriate exchange coefficient,so respiration can be measured. Assuming that respiration is the same by day as by night, it is then possible to calculate photosynthesis. Figure 5 illustrates data obtained by Edwards and Owens (1962). If separate estimates of the rates of respiration of the producers, the consumers and the decomposers (particularly those in the bottom deposits) can be made, a fairly complete picture of community metabolism can be built up. Odum (1956) showed that many rivers are heterotrophic, their communities consuming more than they produce, the difference being made up by imports from upstream. Odum and Odum (1955) used the same method to obtain a rough estimate of production of a coral reef community, where there was a, continuous flow of water driven by a prevailing wind. Odum and Hoskin (1958) extended the technique to a study of production in marine bays and estuaries, while Park et al. (1958) made parallel calculations on the basis of changes in CO,. Clearly, the measurements of primary production in aquatic habitats depend for the most part on monitoring the changes in oxygen, carbon dioxide or nutrient salts in either small samples enclosed in bottles, or

15

AQUATIC ECOSYSTEMS

7

2000

.

2300

.

.

.

0200

.

.

.

0500

.

.

.

.

.

.

0800 1100 Time

.

.

.

1200

.

.

.

1700

.

.

2ooo

. . .

I

2300

FIG.6. (a)An example of the diurnel variation in oxygen content of river water observed at two stations on the River Ivel by Edwards and Owens (1962). (b) Photosynthesis, diffusion and community respiration calculated from the data in (a) above. Reproduced with permission from J . Ecd. 60, 214.

L

16

I(. H. MANN

in large bodies of water. Since photosynthesis is accompanied by respiration it is necessary to measure the latter separately. The factors leading to difficulty in the interpretation of results are first, the problem of distinguishing between the respiration of the producers and that of the rest of the community, and second, doubts about the extent to which oxygen, carbon dioxide or nutrients are regenerated and recycled during the period of observation. It will be shown below that the latter is a particularly intractable problem. B. S E C O N D A R Y P R O D U C T I O N 1. The concept Animal production in terms of yield to man is an old and readily grasped concept. For instance, Ivlev (1945) wrote, “Numerous fishcultural investigations and t,he latest handbooks of pond-fish culture all indicate that fish culturalists understand the productivity of a given body of water to be the average annual production of fish taken from it, expressed in weight units”. I n the situation in which fish are put in at the beginning of a year and harvested at the end of it, it is obvious that the weight of fish removed less the weight originally put in is the production for the year, provided that there are no mortalities and no reproduction during the year. If the fish are removed at frequent intervals, for instance weekly, the sum of the weight of fish removed, less the weight of the initial stock, is the annual net production. From this it is but a short step to imagining the situation in which fish are removed more or less continuously, as by a population of predators, where it is clear that the production is the total weight of fish removed by the predators during the year plus any increase in weight of the stock. Carrying the idea still further, one can see that if a fish dies of disease during the year and is consumed by bacteria, this is a form of production to the decomposers.We have thus recognized three categories of production: production to man (often called yield) production removed by predators, and production removed by decomposers. Each of these is associated with mortality, the first often being called fishing mortality and the other two natural mortality. But there is also the situation in which the weight of the fish stock increases, for instance by reproduction, and is not removed in the period under consideration. This is not necessarily associated with any particular kind of mortality. The weight of the stock may be increased by growth of its individual members or by reproduction. A definition of production which covers all these situations is: production is the increase in biomass which occurs in a given period of time, whether or not all of it survives to the end of that period.

AQUATIC ECOSYSTEMS

17

At this point we should note that there are many ways of measuring the increase of biomass which takes place. For instance, it may be recorded as wet weight, dry weight, content of carbon or nitrogen, or energy content. If one is comparing, say, the production of two fish stocks one of which is putting on mostly protein while the other is putting on mostly fat, the result of the comparison will appear very different according to the units used. We shall return to this problem later (p. 53). The concepts pertaining to secondary production are not difficult when they are related to animals such as fish which can be recognized as individuals and readily handled for measurement. When, however, we extend the concepts to populations of invertebrates which can only with difficulty be recognized as individuals and which have complex life histories often involving metamorphosis or long periods of more or less continuous reproduction, considerably more difficulty is involved. This led early workers concerned with the productivity of a wide range of organisms to resort to the concept of turnover rates. Juday (1940), a pioneer in this field, estimated the production of the plankton and the benthos of Lake Mendota by this method. He argued that under favourable conditions the bacteria may divide several times a day and the algae may double or quadruple their numbers daily. On the other hand the rotifers and crustacea may require one to several weeks to go through a complete life-cycle, but these make up only about 6% of the total quantity of plankton. He, therefore, estimated that the average turnover in the organic matter in the mean standing crop of plankton takes place on average about every two weeks throughout the year, and obtained his figure for plankton production by multiplying the mean standing crop by 26. By a similar argument he concluded that the benthic fauna turned over once per year. I n one of the most comprehensive studies of production a t all trophic levels made to date, Odum’s (1957) study of Silver Springs, Florida, the best that could be done for secondary production was to estimate the turnover rates. These estimates were, however, based on studies of the rate of growth of organisms during periods of the order of 30 days. A similar method was used by Teal (1957) to determine the production of a population of oligochaetes. An early study of the production of marine benthic animals by Boysen Jensen (1919) is important in establishing a firm foundation for more rigorous estimates, yet it seems to have been overlooked in previous discussions of thesubject (Ivlev, 1945; Clarke, 1946; Macfadyen, 1948). His ideas may be illustrated by reference to his data on Solen. I n 1912 he observed that the population density of a particular age class was 226/m2 the average weight of a specimen being 0.15 g. Next

18

K. H. MANN

year their numbers were reduced to 41, of mean weight 0.32 g. The population had therefore produced for the consumption of other trophic levels (predators or decomposers) 185 animals ranging in weight from 0.15 to 0.32 g. Taking the average weight as the mean of the two extremes he estimated production a t 185 x 0.235 = 43.5 g. The general

(a)

I I

I I

I

-

-

WI

w2

Mean weight

, _WII vv2 -w3 - w4 I

I

I

-

w5

-

Wn

Mean weight

FIQ.6. (a)Numbers plotted against mean weight on two occasions. Production is given by N , - N , x#(iitl+Ee). (b) Hypothetical curve relating number to mean weight on five occasions. For details see text.

case is illustrated in Fig. 6a. Production of an age class in the time interval t, to t, is given by:

where N , and N , are the numbers per unit area at times t, and t , and w,and w,are the mean weights of the age class at times t, and t,. In the diagram P is represented by the area AN,N,B. In Fig. 6b is represented the hypothetical situation in which a population is counted on five occasions and the data plotted in the same way as in Fig. 6a. By extension of the argument just used, the production of the population is represented by the area bounded by AN,N,E. If data were available to plot numbers against mean weight throughout the life

AQUATIC ECOSYSTEMS

19

history of the age class, production would be given by the area under the curve NoGnwhich is

g

y

N

This logical extension of Boysen Jensen’s approach was never made, but 30 years later Allen (1951) achieved the same result by a slightly different method. He argued, in effect, that the production of an age class in a fish stock in a short period of time A t is the product of the average number present, N , and the average weight increment wa-wl. Thus in Fig. 7 the production between two observations at M and N is

M

-WI w2

Mean weight FIU.7. Curve relating numbers to mean weight in a cohort of fish. For details see text.

represented by the area Mwlw2N and by summation of many such measurements one arrives at the total production for the year class throughout its life as

The curve relating numbers and mean weight of an age class throughout its life history may be called an Allen Curve. It is arrived at either by considering the number lost from a population in specified intervals of time and multiplying this by the average weight of those lost, or by considering the number surviving at a particular time and multiplying

20

K . H. MANN

this by their average weight increment in a specified interval of time. The first is an estimate of the production removed by predators (and possibly decomposers) the second is the production of the survivors. Over the whole of the life span these two are identical, but in a short period of time they are not. We shall see that most of the methods currently in use for measuring animal production are variants on one or other of these approaches. The graphical method lends itself to the interpretation of empirical data, for it does not incorporate any assumptions about the shape of the curve relating numbers in the age class to their mean weight. Ricker (1946) showed that it is possible to calculate production of an age class algebraically if one makes the assumption that growth and mortality are similarly distributed seasonally. If the instantaneous rate of growth of a stock is g and the instantaneous rate of mortality is z, the rate of change of biomass B of the stock is given by:

dB - = (g-Z)B. at Integrating

B = BOe(g-zV where B, = weight of stock at time to and the average biomass present during the year is given by:

Then the year’s production, P,is given by the average biomass multiplied by the instantaneous growth rate on a yearly basis:

gBo(eg-”- 1) p=g-z

One difficulty in the application of this method is that growth rates rarely remain constant for long. Ricker and Foerster (1948) made separate calculations for a succession of half-month periods. A modification of this method was used by Mann (1965) using the assumption that the whole of a year’s growth takes place at a constant relative rate during a six-month growing season and that the year’s mortality all occurs during the same period (p. 52).

2. Techniques of measurement (a) Techniquesfor zooplankton. I n the oceanic environment secondary production is almost synonymous with zooplankton production (fish

21

AQUATIC ECOSYSTEMS

being referred to as tertiary or terminal producers). Methods of sampling zooplankton populations and considerations of standing crop data formed a prominent part of a review in this series by Raymont (1966) and will not be treated here. Yablonskaya (1962) reviewed estimates of production of marine planktonic copepods by Russian workers from 1940 onwards. Her own data were on Diaptomus salinus, which is monocyclic. Breeding takes place in April-May, after which the parents die. By July most of the new generation have reached copepodite I V and in October 90% become adults and hibernate until the following TABLEI

Summary of data for calculation of production of Diaptomus salinus rearranged from Yablonskaya (1962)

Developmental stages, May Survivors, August New brood, August Survivors, October New brood, October Survivors, May Total production to predators Biomass of survivors Production for year

Number per m3

Meanwt. (mg)

6777 2691 692 2226 152 1188

0.0045 0.0204 0.0135 0.0454 0.0036 0.0764

Production to predators (mg/mY

83-354

-

52.528

-

78.540 214.422 90.754 305.176

spring. Data on numbers and mean biomass were collected in May, August and October. Production was calculated by the method described above (p. 20) as “production removed by predators”, i.e. the decrease in numbers between observations was multiplied by the average biomass of the organisms that disappeared. The pertinent data are set out in Table I. The method does not reach the degree of precision required for a rigorous Allen Curve type of estimate because the data on numbers and mean weights are for mixed age classes, but a reasonable approximation is achieved. The data obtained by this method and reviewed by Yablonskaya give estimates of annual production ranging from 130 to 433 mg/m3 (presumably as wet weight). An interesting generalization is that the estimates of annual production all with one exception fall between 2.1 and 3.1 times the spring biomass. This raises the possibility of obtaining rough estimates of production in comparable situations from biomass data alone. The situation in which a planktonic organism passes through several generations per year causes considerable difficulty in interpretation of

K. IT. MA”

22

the data. However, an attempt to overcome the difficulties was made by Greze and Baldina (1964). For instance, they sampled a population of Acartia clausi in the Black Sea near Sevastopol about twice a month on average. The organisms were sorted into eggs, nauplii, copepodites, ~

70

I

-

/

~~

4

/

/

0

0

0

4

0

0

0

0 /

//

d

I

0

50

100

I

I

I

150

200

250

I

I

350

xx)

I

400

Age (days) FIO.8. Growth curves for Acurtia c b m . at a range of temperatures appropriate t o (a)summer, (b) autumn, (c) spring, (d) winter. The broken lines include egg production. From Cfreze and BaIdina (1964).

females and males and from consideration of the seasonal fluctuations they decided that there were seven generations in the year. They used L. A. Chayanova’s data on development times at 20°C and corrected for other temperatures according to Winberg’s (1956) adaptation of TABLEI1 Poplation structure of Acartia clausi in the B h k Sea (E?ront Greze and Baldina, 1964) Numbers per _-

Nauplii Copepodites Adults

mS

Summer

Fall

Winter

Spring

730 406 173

141 36 20

57 1 130 26

916 316 128

23

AQUATIC ECOSYSTEMS

Krogh's curve. Using published data on the weight of each stage of Acartia clausi, they constructed growth curves appropriate to each development time (Fig. 8) and converted these to daily growth rates appropriate to each season. The populations structure at each season

FIG. 9. Lower curve, daily increments in weight of Acarth c l a d of different sizes from curve a in Fig. 8. Upper curve, cumulative curve of numbers in the summer population plotted against weight, from the data in Table 11, column 1. After Greze and Baldina (1964).

was then tabulated and plotted as in Table I1 and Fig. 9. The number in each size class was then multiplied by the daily growth increment appropriate to that size class to give a daily production rate (Table 111). TABLEI11 Calculation of production in Bummer season by Acartia clausi from data presented in Table I I and Fig. 9

(mg x 10-3)

Number per mS

Individual daily growth (mg x 10-3)

Daily production (mg x 10-3)

0-2-5 2.5-10 10-20 20-30 30-50 50-70

850 250 87 35 47 40

0.09 0.45 1.20 1.68 1.20 0-47

76.5 108.0 104.4 58.8 56-4 18.8

Size group

422.9

24

K. H. MA"

The seasonal production was obtained by summing the daily rates for each size class for the appropriate number of days, and the annual production was the sum of the seasonal totals. I n this way they calculated that the annual production of A . clausi was 66.8 mg/m3, this being about 13 times the mean annual biomass

(5

= 13).

The authors were also able to calculate production of Acartia clausi from the data for the English Channel published by Digby (1950), assuming that the Russian data on biomass of the various stages and development times were applicable. They showed that average biomass was greater off Plymouth, but the lower temperatures reduced the number of generations to five or six. Reproduction occurred only between April and October, with the result that although annual production off Plymouth was about 50% higher, the ratio

P

-

B

was lower

(Table IV). TABLEIV

Comparison of production data for Acartia clausi in t?Ae Black Sea and the EnqlislL Channel. (From Greze and Baldina, 1964)

Length of production season (days) Average temperature during season ("C) Average biomass (mg/m3) Annual production (mg/ms) P Total - coefficient

B

Black Sea

English Channel

365 14.9 5.1 66-8

260 13.0 12-0 104.8

13.0

8.7

These calculations, which are some of the most ambitious estimates of plankton production so far produced, rest on a number of assumptions which would need further work to justify them, namely, that development time, and hence growth rate is primarily dependent on temperature rather than, for instance, food abundance, that the dependence on temperature follows Krogh's curve, and that observations on development times made by one author at a particular time and place can validly be transposed to another. Further, the calculations imply a meaningful average population structure a t a time when the population is likely to be turning over rapidly and a meaningful average temperature when the organisms may be migrat,ing through a thermocline. Calculations involving the same principles have been made by Pechen and Shushkina (1964). The calculations of production of Calanus plurnchrus by Parsons

AQUATIC ECOSYSTEMS

26

et al. (1969a, b) are more soundly based, for the growth data were determined in situ from the times of maximum numbers of each stage and combined with abundance data to give estimates of production. I t amounted to 2-8 g C/m2, about 10% of the primary production of the area. From the observed growth rates, the change in zooplankton biomass was predicted and found to be in good agreement with actual standing stocks. From this they inferred that predation on the stocks of copepods was negligible. One of the problems in determining the production rate of a plankton population may be stated as follows. Suppose the population size and age structure appears to be similar on two successive sampling dates. Is the population static or is it in a state of flux, with a significant mortality rate balanced by recruitment? I n the first case production is low, in the second, high. A method of distinguishing between the two is that of Edmondson (1960),who showed how to determine the birth and death rates of a population from preserved quantitative samples. Eggs and females were counted and the ratio eggs : females was determined. The higher this ratio, the higher the rate of egg production. To obtain an estimate of the absolute birth rate it is necessary to know the duration of development of the eggs. These were determined in the laboratory and the birth rate calculated from

where B = rate of egg laying as eggs laid per female per day E = number of eggs per female in the samples D = the duration of the embryonic stage in days. The corresponding instantaneous birth rate b' was calculated from B by the formula b' = In ( B + 1). If one assumes that reproduction goes on continuously and that the characteristics of a population remain constant for the period between observations, population growth is described by: N, = Noe'"t where No = the initial population size N , = the population size at time t r' = the instantaneous coefficient of population increase. r' can be calculated from population counts on two successive occasions:

,

r =

lnN,-lnN, t

26

K . H. MA”

and from this mortality rate d‘ can be calculated as:

& = b’-r’. The product of mortality rate and biomass data gives production. Hall (1964) applied this method to a natural population of Daphnia and found that mortality and hence production was low except in summer, when there was a population loss of 28% per day. This he attributed to predation. It followed that an amount equal to the total biomass of the population was being produced for predator consumption about every four days. The population exhibited the common pattern of variation in abundance, with peaks in spring and autumn, and Hall interpreted this as indicating that predation was the main factor reducing numbers between the spring and autumn maxima and that without it the population might have remained at a high density throughout the summer. The method just described has been used to calculate the production of other populations of freshwater plankton by Amren (1964) and Hillbricht-Ilkowska et al. (1966). Yet another method of calculating production from losses to predators is that used by Heinle (1966). It was not practicable to work with egg numbers and development times, so quantitative estimates were made of numbers of nauplii, copepodids and adults. From these, mortality rates were estimated, the time scale being determined from laboratory observations of the time required to develop from one stage to the next. The finite death rate multiplied by biomass data gave estimates of production. This was at an average rate of 2.77 mg/m3/h (dry weight) between mid-July and mid-September, which amounts to some 220 kg/ha in the summer period, and is about 5 % of the planktonic primary production in the same area. Heinle made prominent use of the concept of turnover time, defined as the reciprocal of the finite death rate. Thus a population which has an instantaneous death rate of 0.69 has a finite death rate of 0.5 and a turnover time of two days. At biomass B the production is 0.5 B per day. I n both Hall’s and Heinle’s studies the turnover time was shorter than the development time, so the calculations of the ratio of production to standing crop from considerations of length of life history (Juday, 1940) were not well founded. Stross et al. (1961) calculated the turnover time of two Daphnia populations and calculated production in this way. (b) Techniquesfor benthos. The pioneer work of Boysen Jensen (1919) in determining the rate of production of marine benthos has been discussed (p. 17). Sanders (1956), after remarking that no one since Boysen Jensen had studied a marine benthic community from the same point of view, went on to calculate the production to predators by an elegant refinement of the same basic method. He used his field

AQUATIC ECOSYSTEMS

27

data to produce two curves: (i)a growth curve relating log weight to age and (ii) a mortality curve relating the number of survivors to time. From these curves he read the population mortality and the mean weight of an individual at monthly intervals and multiplied the two

P

- ratio for two species of polychaete B and two molluscs, all having a life history extending over more than one year, were between 1.94 and 2.28. The ratio for the short-lived Ampelisca was about 5. From a consideration of the mean biomass and length of life of other species, Sanders made estimates of their produc-

together to give production. The

P

tion using the same - ratios. The Sanders method was used by Richards B and Riley (1967) to calculate the productivity of benthic epifauna. In freshwater studies there are rather more examples of the estimation of production by benthic organisms. Borutzky (1939a, b) made intensive studies of changes in the biomass of a limited number of species in Lake Beloie. From the reduction in numbers at each stage of the life history he calculated the production removed by predators and decomposers. I n the case of Chironomus plumosus there was a net reduction in the biomass present from one year to the next and this was taken into account in assessing the true production. Nees and Dugdale (1959), concerning themselves with the production of aquatic midge larvae, gave an exposition of the Allen Curve method of computation and showed that when cohort size is plotted against mean larval weight on a log scale the data of Anderson and Hooper (1956) mostly fall on the same straight line. This presumably means that growth and mortality varied in a parallel manner throughout life. Waters (1966) calculated the production rate of a mayfly larva in a stream from data on population density and instantaneous growth rate at monthly intervals. He obtained an estimate of production of 12.6 g/m2 wet

P

weight per year, with a - ratio of 9.7. A calculation of biomass change B taking into account emergence of the insects and drifting in and out of the study area gave a substantially lower figure probably because no allowance was made for predation or decomposition. Negus (1966) was able to determine the growth rate of the freshwater mussels Anodonta and Unio from the winter rings on their shells. By combining growth rates with population density data she obtained estimates of production. It amounted to 205 kg/ha of wet weight of soft tissue, for three species combined. The ratio

P

- was 0.17. Stanczykowska (1966) recorded bioB mass and production of Dreissena polymorpha in 31 lakes. She arranged

28

K. R. MA"

three groups according to their population density, with biomasses

P

averaging 6,200, and 480 g/m2respectively.The ratio - was 0.485,0.466

B

and 0.359 in the three groups. I n all the examples cited so far there was no great difficulty in separating the age classes for study of their individual rates of production. In situations where there is a long period of more or less continuous breeding the calculation of production is considerably more difficult. Cooper (1965) studied the freshwater amphipod Hyalella azteca in which the females are capable of producing broods of young at every moult following the onset of reproduction. Growth rates, duration of instars, mortality and the intrinsic rate of natural increase were determined in the laboratory at a variety of temperatures. He calculated production in two ways. After observing the abundance of a particular instar in the field he used laboratory data to predict the abundance of the next instar at the next date of sampling. The difference between predicted and observed abundances was an estimate of field mortality. He was then able to calculate production by combining mortality with biomass data. The process was repeated for a range of instars on a number of occasions throughout the year. His second method was to determine growth rates from the size-frequency distributions in the natural populations and combine these with abundance data to give estimates of the rate of production of the survivors. (c) Techniques forfish. For reasons given at the beginning of section B (p. 16) the difficulties of determining production by fish populations are less than for most other classes of aquatic animals. However, only in a comparatively small number of situations have the necessary population parameters been collected so that an accurate estimate of population production can be made. The study by Allen (1951) of the brown trout population of a New Zealand stream is a good example. Gerking (1954, 1962) studied populations of bluegills in lakes in Indiana, and Hayne and Ball (1956) measured production by the same species in an experimental situation. Horton (1961) estimated the production of trout in a stream in south-west England and Mann (1965) gave figures for a variety of species, mainly Cyprinidae, in the River Thames in southern England. A more complete list is given in the review of production in fish populations by Chapman (1967). I n the marine environment production measurements in terms of area are more difficult to obtain because the fish stocks frequently undertake extensive migrations and the area occupied by the populations at any one time are seldom known with precision. On the other hand there is an enormous literature on growth, mortality and stock size which can readily be interpreted in terms of production per head

29

AQUATIC ECOSYSTEMS

of the population. Many of the commercial statistics are restricted to fish above a certain size, so that even the calculations of the type just mentioned are restricted to a fraction of the total population. For the fish stocks of the North Sea, Steele (1965) quoted the commercial yield and added to this an estimate of natural mortality. The latter varied from one third of yield in the case of demersal fisheries to twice the yield in “Bank” stock of herring in the northern North Sea. Steele tentatively assumed that for the North Sea as a whole the natural mortality is 4s

2 007

\

36 10

0

0.06

005

-

0

c

c

x

E 24

004

Q)

L

5

.-c 003 .-

n

0

z

~

O

002

12

n

001 0

0 2 4 6

10

15

20

30

40

50

0

Weight ( g 1 FIG.10. Lower curve, daily weight increments of the round goby plotted in relation to body weight. Upper curve, cumulative curve of numbers in the population plotted against mean weight.

about the same as the yield, and arrived at an estimate of total production of 0-6 g C/m2 year. Greze (1965), using the techniques of calculating production which have been quoted in relation to zooplankton (p. 23), plotted the daily weight increment and the cumulative curve for numbers against body size for a population of the round goby Neogobius melanostomus from the Sea of Azov (Fig. 10). Production was calculated from the product of the number in each size class and their daily growth increment. This brought out very clearly that the greatest part of production is contributed by the small fish not normally harvested by man. Table V shows that about 75% of production is attributable to fish under 10 g in a

K. R. MANN

30

TABLEV Production of Neogobius melanostomus population in the Sea of Azov. (From Greze, 1965) Weight group (g)

Number in the group 13 800 12 800 15 400 2 700 2 100 950 250 70 20 10

0-1 1-2 2-4 4-6 6-10 10-15 15-20 2&30 30-40 40-50

Daily increment

Daily production of the group (g)

0.006 0.017 0.026 0-041 0.051 0.057 0.059 0.064 0.059 0.023

82.8 217.8 400.4 110.7 107.1 5 41 14.7 4.5 1.2 0.2

species which attains 40-50 g. Similar calculations for a variety of species suggest that as a general rule the yield to man constitutes not more than 25% of the total production of the population.

111. STUDIESO F WHOLEECOSYSTEMS A.

S T U D I E S O F E N E R G Y FLOW

One of the f i s t attempts to draw up an energy budget for a whole biological system was that of Juday (1940). He synthesized the results of about 25 years’ study of Lake Mendota, in Wisconsin, and produced both physical and biological energy budgets for the lake. He referred to photosynthesis as “the primary accumulation of energy” and heterotrophic organisms as “a secondary stage in the storage of the energy accumulated by aquatic plants”. As mentioned earlier, he used data on the mean standing crops of organisms and converted these to estimates of production by consideration of their life histories and probable turnover times. From analyses of organisms in terms of carbohydrate, fat and protein he converted the production data to calories (Table VI). He argued further that the energy metabolized by an organism does not appear as production, so he made estimates of the ratio of production to metabolism and entered items for metabolism in his energy budget. I n discussion he considered the efficiency with which energy of sunlight was converted to plant tissue and the amount of plant tissue required to produce a unit of animal tissue. Although the details of the calculations are open to many sorts of criticism, Juday’s work heralded an era of thinking about the energetics of ecosystems.

31

AQUATIC ECOSYSTEMS

TABLEVI Annual production of various groups of organism in Lake Mendota and estimates of the energy of metabolism. (From Juday, 1940) Groups of organisms Phytoplankton Benthic plants Zooplankton Benthic animals Fish

Production dry organic matter kg/ha/year 50 512 390

production cal/cma/year

Energy of metabolism cal/cma/year

299 22 22

100 7 100

3

15

The next major advance was made when Lindeman (1942) acknowledging his debt to G. E. Hutchinson, proposed his trophic-dynamic model of ecosystems. He proposed that organisms should be formally grouped according to their mode of obtaining energy: primary producers, herbivores, predators on herbivores, and so on and each group he called a trophic level. He designated their energy content by the symbols A,, Az, ... A,. Next he pointed out that the energy content of a trophic level is in a state of flux, receiving energy from the previous trophic level and losing it by passing it to the next trophic level or by dissipating it as in metabolism or decomposition. Therefore:

where A, = the rate of flow of energy from the previous trophic level An-, and A,, = the rate of energy flow to the next trophic level and the rate of energy dissipated from A,. He then went on to consider the item A,. under the headings of respiration, predation and decomposition. Predation on a particular trophic level was calculated from the estimated energy requirement of the trophic level above. Decomposition was based on estimates of the amount of material which, according to the analyses of Birge and Juday (1922), were likely to be indigestible and therefore passed out with the faeces of a predator. The values for respiration of typical organisms in each trophic level were based on the rather scanty literature of the time. Lindeman then took various estimates of production, included those of Juday cited above, and made corrections for the various losses from the trophic levels. His calculations of revised energy budgets for various lakes were wrong in detail (see Slobodkin, 1962)

32

K. H. MANN

but the debt which we owe to him for his tropho-dynamic hypothesis is incalculable. In marine ecology, attempts to describe the dynamics of whole ecosystems were made by Clarke (1946) and Harvey (1950). Clarke brought together the work of Redfield (1941), Riley (1941) and others to outline the energetics of phytoplankton, zooplankton and fish on George’s Bank, and to draw attention to the role of the benthos. His phytoplankton data were based on Riley’s light and dark bottle studies; he made a minimal estimate of zooplankton production from observed changes in the standing crop, and estimates of fish production were obtained from the commercial landings. Harvey (1950) considered a much wider range of data, drawing on observations from the English Channel over a long period, supplemented by data from the North Sea. The annual production of phytoplankton was calculated from changes in concentration of phosphate and other nutrients. The sizes of the fish stocks were estimated from data on commercial landings, and published information on growth rates and food requirements were used to build up a picture of feeding and growth. The composition of the zooplankton and of the benthos were carefully documented, and estimates of their growth production were compared with the estimated food requirements of the fish. An interesting conclusion was that 100 g of plant material consumed by bivalves which were eaten by demersal fish is likely to yield about 1 g of fish flesh, while the same amount of material passing through zooplankton to pelagic fish might yield 6 7 g. The next major attack on the dynamics of a large ecosystem was that of Odum (1957) who produced an energy flow sheet for a running water community at Silver Springs, Florida. The community under study was characterized by nearly constant conditions of temperature, water chemistry and community composition. The dominant primary producers were large plants of eelgrass, Sagittaria, to which were attached dense encrustations of diatoms, blue-green and filamentous green algae. Their production was estimated by following the diurnal variations in oxygen content of the water, as discussed above (p. 14). The observations were repeated on nine occasions throughout the year including both cloudy and sunny days. It was found that about 30% of the production was by the Sagittaria and 70% by the attached algae. Carbon dioxide changes were also monitored and used to calculate photosynthetic quotients and community respiration. The growth rates of the main consumer organisms were determined from specimens kept in cages in the water for periods of about one month. These were combined with estimates of population density to give production figures but the author admitted that a really satisfactory series of measurements of herbivore and carnivore production

AQUATIC ECOSYSTEMS

33

had not been obtained. Similar very brief experiments were carried out to determine the metabolic rates of the dominant species of animals. Teal’s (1957) study of community metabolism in a temperate cold spring was more restricted in its scope and correspondingly more precise. The area studied was about 2 m across and the water was only 10-20 cm deep. Primary production and respiration of micro-organisms were measured by a modification of the light and dark bottle method, using cylinders pushed into the bottom mud and protruding above the surface of the water. Although over 40 species of animals were found to be present, only one-third of these were sufficiently abundant to make a significant contribution to the energy balance. Production was calculated from mortality data and net annual changes in the standing crop, except in the case of the planarians which put nearly 50% of their energy into manufacturing mucus. Respiration was measured by placing organisms in 20-ml syringes immersed in the spring and following changes in the oxygen concentration of the water. The amount of allochthonous material entering the spring in the form of leaves, fruit and branches, and the amount leaving in the outflowing stream were monitored. Teal found that about one-quarter of the energy of the ecosystem waa provided by photosynthesis of aquatic plants, the remainder coming from outside. Of this energy, 71 % was transformed to heat (respired), 28% was deposited in the community and 1 % emerged aa adult insects. This was probably the most accurate analysis of the functioning of an ecosystem to date. The insights which it gave into the sources of energy for the system and the importance of various classes of organisms in the utilization of that energy made it obvious that further studies along these lines would be fruitful. The studies by Odum and Teal were carried out in springs where relatively constant temperature conditions prevailed. To obtain similar information about a habitat subjected to the normal temperature fluctuations of a temperate climate would involve much more elaborate studies of seasonal changes in the metabolic rates of organisms and of the population dynamics of the component species. Clearly this would require the efforts of a team of workers over a period of years. The work on the Sapelo Island salt marsh ecosystem of Georgia has been such a study. Contributions by Burkholder and Bornside (1957), Teal (1958, 1959), Odum and Smalley (1959), Pomeroy (1959), Smalley (1959, 1960), Teal and Kanwischer (1961), Kuenzler (1961a, b), and Wieser and Kanwischer (1961) have been synthesized by Teal (1962). The chief primary producers were Spartinu and the algae on the mud surface. Their average net annual production measured by the methods described in section I I A (p. 13) amounted to 6685 and 1620 kcal/ma respectively. The grasshopper and leaf hoppers removed only 4.6% C

34

K . H. MANN

of their potential food supply. Spartina detritus and algae were consumed by crabs, annelids, nematodes and molluscs, but much of their food had been partially consumed by bacteria before they obtained access to it. Bacterial respiration alone was thought to account for about 47% of net production. Another 45% was exported from the marsh in the daily movements of tidal water. The consumption of energy by carnivores amounted to less than 1% of the energy of net primary production (Fig. 11). Teal remarked that a study in such detail was only possible because the fluctuating conditions of a tidal salt marsh limited the number of species of primary and secondary producers thus making a relatively simple system. A complex aquatic system now being studied quantitatively at all trophic levels is the River Thames at Reading, England. This river has the annual fluctuation of temperature typical of its latitude, and although polluted has a rich and varied fauna. At present only the work on the fish and mussel populations has been published (Williams, 1963, 1965, 1967; Mann, 1964, 1965; Negus, 1966) but the preliminary unpublished results from other groups and trophic levels (kindly made available by the people concerned) give considerable insight into the workings of the system. The fish populations, dominated by bleak (Alburnus alburnus) and roach (Rutilus rutilus) had a biomass estimated at 659 kg/ha, one of the highest figures recorded for a natural habitat. Production was estimated at 426 kg/ha, equivalent to about 43 kcal/m2. This dense, slowly growing population appeared to be at the limit of its resources. Many of the fish resorbed their germ cells before spawning time and roach and bleak were found to obtain over one-third of their energy from low-grade food, organic debris (Table VII). TABLEV I I Percentages of assimilated energy of roach and bleak populations in the River Thames derived f r o m each source. (From Britton (unpublished))

Detritus Algae Macrophytes Zooplankton Benthos excluding molluscs Molluscs Insects from surface (manyemerged from benthos) Allochthonous sources (e.g.fishermen’s bait)

Rutilua rutilus

Alburnus alburnus

Combined populations

60.1 9-5 2.5 5.7 10.0 11.6

26.6 3.7 3.9 4.3 1.7

0

35.7 5.3 3.5 4.6 4.0 3.1

0

43.6

31.7

0.5

16.2

11.9

FIQ. 11. Energy flow diagram for a Georgia salt marsh. From J. M. Teal, 1962. Reproduced with permission from Ecology 43, 622.

36

I(. H. MANN

The populations of river mussels (Unio spp. and Anodonta spp.) averaged 2.9 metric tons/ha (fresh wt), equivalent to about 76 kcal/m2. These, together with other filter feeding organisms, sponges, bryozoans, etc., accounted for over 90 yo of benthic invertebrate production (MacDonald, unpublished). Their source of energy was the suspended organic matter in the water. This averaged about 7 g/m3 dry organic weight over the year, of which 2 g/m3 was phytoplankton. The remaining material was unidentified, but must have been derived from the production of benthic plants, the leaves of overhanging trees, or imported matter including sewage solids. The magnitude of primary production by various components in the ecosystem (Table VIII) TABLEVIII Primary production in the River Thamea in kcal/m2/year Producer Phytoplankton

Method

Estimate

light and dark bottles (rotated) change in biomass

4388

Macrophytes, Acorua and N U P ~ T Willow trees (Salix spp.) Biomass of leaf fall

20

104

Source Kowalczewski and Lack (unpublished) Lack (unpublished) Mathews and Kowalczewski (in press)

indicates that macrophyte production is small compared with phytoplankton production. There is as yet no estimate of production by benthic algae. If the pattern of production holds in sections upstream of that studied, it is likely that the 7 gm/m3 suspended organic matter derives no more than 50% from plant production and the remainder from sewage solids. From Britton’s data (Table V I I ) it appears that the most important single channel of energy flow leading to fish production is the organic detritus complex, which consists of decaying plant material, sewage solids, and decomposer organisms. Next most important are the insects captured by bleak at the surface of the water. About 50% of these completed their growth as aquatic larvae in the benthos. The amount of energy derived from molluscs, sponges, bryozoa and tubificid worms seems extremely small, but this component could have been underestimated, since it is digested extremely rapidly. The pattern which emerges is of a river densely populated with fish and molluscs, very productive, but depending for perhaps half of its energy flow on allochthonous materials such as sewage solids, and on the detritus rather than the grazing food chain (Odum, 1962).

AQUATIC ECOSYSTEMS

B.

37

S T U D I E S O F T H E CIRCULATION O F MATERIALS

The flow of energy and the cycling of material are parallel and equally important processes in the functioning of ecosystems, but studies on the circulation of materials have not led to any comprehensive accounts of the type reviewed in the last section. Primary production is commonly assessed as carbon assimilated, and zooplankton production has been expressed in terms of carbon for comparison with the primary production (e.g. Parsons et al., 1969b), but it seems never to have been practicable to extend the method to a whole ecosystem. Curl (1962) collected carbon data for the phytoplankton, herbivores and carnivores of a marine plankton community, and by incorporating a rather large number of assumptions was able to arrive at a ratio of primary to herbivore production, but he found it impossible to extend his calculations to the carnivores. Gerking (1962) argued that since protein synthesis is the most characteristic feature of animal growth it is appropriate to study production in terms of nitrogen. He completed an admirable series of ecological and physiological studies of the nitrogen turnover of a fish population which he related to the nitrogen content of the zooplankton and benthos, but he was not able to complete the picture by relating it to primary production. I n fact, only recently have techniques been developed for using 16N-labelledcompounds to assess the primary production of plankton, taking full account of the variety of sources from which the algae obtain their nitrogen (Dugdale and hering, 1967). In making estimates of primary production fromdata on the depletion of nutrients, an important unknown factor has always been the extent of regeneration and recycling. The use of labelled nutrients such as 8aPhas made it clear that rapid recycling occurs and observed change in total dissolved nutrients represent a slow shift in a system which is in a constant state of rapid turnover. Early workers in freshwater habitats (Hutchinson and Bowen, 1947, 1950; Coffin et aZ.,1949; Hayes and Coffin, 1951) found evidence of very rapid uptake of radiophosphorus by micro-organisms, and a slower movement through the food web. In fact, when the total phosphorus in a lake was increased by -only 0-25%, 80% of the added material was removed in 3-4 days. It looked like selective removal of the isotope. As an alternative they proposed that all the phosphorus in the water was being turned over every few days by exchange with the organisms in contact with the water (Hayes and Coffin, 1951). Experimental evidence has since been accumulated in support of this view. Rigler (1956) separating the plankton from the bacteria by filtration showed that the bacteria turned over their phosphorus content in minutes, while the plankton took

38

K. H. MANN

hours. Hayes and Phillips (1958) showed that antibiotics inhibited the conversion of phosphorus from the inorganic to the organic form, and in sea water Pomeroy (1963) showed that the exchange of 32Pbetween sea water and material in suspension is inhibited by the addition of methylene blue or cyanide. In this case antibiotics had little effect, and it seemed likely that phytoplankton were the main agents of exchange. Time of 32P activity Inter- quartile interval of Activity density--Time curves Calculated EZBZ Estimated ESSS Secondary Consumers

cottus Salmo Atherix Nigronia

Predators

Hexagenia Entosphenus Pteronarcys

Detritus Feeders

Omnivores

Brachycentrus Gammarus

Periphyton Scrapers

E. cornuta E. needhami

FILTER FEEDERS

Hydropsyche Simulium

Primarv

Consumers

ma m mm

Ezmzzza

Periphyton Macrophytes

Producers

- 1

I

EzJEmna

lzzm

Water I

10

I

100

I

I

10.000 Time (min. after release of spike) I.000

IWCCQ

FIG.12. Time of s*P activity of components of ,a stream ecosystem. The time intervals shown are the central 50% of the time various components had detectable activity. Estimated quantities were obtained by extrapolation of d i s h e d activity curves. From R. C. Ball and F. F. Hooper (1963). Reproduced with permission from “Radioecology”, p. 226. Reinhold. New York.

I n an estuarine environment (Pomeroy et al., 1965) it appeared that the effect of the tidal current was to confine the biologically active elements to the sediments, where they exchanged with the interstitial water, and only slowly with the water above. When a dose of 32P was injected into a stream in three successive years, the fate of the injected material varied from year to year (Ball and Hooper, 1963). On one occasion 70% of the tracer had been

AQUATIC ECOSYSTEMS

39

incorporated into solids by the time it had travelled 200 yards (approx. 180 m), and the uptake by macrophytes, omnivores, detritus feeders and fish was particularly high. I n the other years the phosphorus remained in solution much longer and was taken up chiefly by periphyton, mud browsers and filter feeders. Thus, the whole pattern of nutrient cycling was determined by the extent of phosphorus fixation (possibly by bacteria) during the first few minutes of the experiment. The time scale of events is illustrated in Fig. 12. An illustration of the great length of time required for a population to become completely equilibrated with a radio-isotope in its environment was provided by Ophel(l963). He found that in a lake contaminated with DOSr,the perch reached equilibrium with the most readily exchangeable portion of their tissues in about 42 days, but there was a reservoir of non-exchangeable material which was radioactive only in those fish which underwent development and growth in the water.

IV. STUDIESO F S I N G L ES P E C I E SO R GROUPSO F S P E C I E S A.

ENERGETICS

In view of the difficulties inherent in studying whole ecosystems, it is not surprising that attention has been concentrated on parts of such systems. Ivlev (1939a, b, c, d) pioneered this field by his studies on energy transformations by fish and aquatic invertebrates. I n the terminology of Ricker (1968), the energy budget of an animal or of a population may be written as C = P+R+F+U where C = potential energy of food consumed P = potential energy of production (by growth and reproduction) R = energy of heat loss and work, a function of respiration F = faeces; the potential energy of food consumed but not assimilated U = excretion; the potential energy of material lost in urine or through the body surface. The terms on the right-hand side have been grouped in various ways. Slobodkin (1962) referring to populations, used

C=R+Y where Y = yield of potential energy in the form of dead animals and excretory products. Unfortunately, his use of this term is liable to be confused with the

K. H. MANN

40

same term used in fishery biology to denote that proportion of production used by man (Ricker, 1968). I n practice it is often impossible to measure separately faeces and urine and many authors have measured C, P and R, and effectively balanced the equation by assuming that C - (P+ R) represents the unassimilated portion of the food. This is not quite correct, for urine and other excretions are derived from material which has fist been assimilated. The techniques for studying the energetics of plankton, benthos and fish tend to be different and will be considered separately. 1. Plankton The rate of respiration of zooplankton has been measured on many occasions and has usually been found to be related to body weight W by the expression

R

=

or log R = a + y l o g W .

0lW7

Thus Richman (1958) found that the oxygen consumption of Daphnia at 2OoC fitted the line (Fig. 13)

R

kin -8 C E

8 kia

= 0.0014

W0.88l.

0.50 ' 0.30 .

0.20

'0

s

Q,

c

0.10 ;

v)

8

c a3 rn

2

0.05

,

0 Y-

O

003

v)

?2 c

-= 092 2 0

.-

5 001

I

0001

I

I

0002

I

I

I

0005

I

I l l

0010

Size of Dupphnia (mg

I

I

1

0020

- dry

1

1

1

1

0050

weight 1

FIQ. 13. Oxygen consumption of Daphnia at 2OOC. 0,Warburg method; 0 , bottle method. From 9. Richman (1968). Reproduced with permission from E d . Monogr. 28, 279.

AQUATIC ECOSYSTEMS

41

In general, the slope of the line, y, tends to remain reasonably constant, while changing conditions affect the intercept a. Published values of y vary from 0.662 to 1.141 (Conover, 1968) but the mean is close to 0.80. Pavlovs (1967) predicted the rate of respiration of Cladocera in the Black Sea from the expression R = 0.2 W0.8 a t 20°C with corrections for other temperatures according to the curve of Krogh (1916), but this appears to be unwarranted when it is known that plankton respiration is affected by level of feeding and by seasonal variations in the material 7 -

0

- 340

0

I

0

I

0010

I

I

I

Size of Duphniu (mg

- dry

1

0030

0020

'

weight

FIG. 14. The filtering rate of Daphnia &.four different food concentrations. 0 , 25; 0,60; 0, 76; A , 100 thousand cells Chlamydomonm per ml. Solid line is ml filtered per Daphnia per day. Broken line is ml filtered per mg dry weight of Daphnia per day. From 8. Richman (1968). Reproduced with permission from Ewl. Monwr. 28, p. 284, Fig. 1.

undergoing oxidations (Conover and Corner, 1968). I n many cases zooplankton migrate regularly through a range of temperatures and no one temperature can be used as a basis for prediction. Food intake has often been determined by measuring the rate of fltration of organisms in suspension. Thus Richman (1958) found that the volume of water filtered by Daphnia was virtually independent of the concentration of Chlamydomonm over the range 25 to 100 thousand cells per ml (Fig. 14). Similarly Klekowski and Shushkina (1966) reared Mmrocyclops albidus on Paramecium, and Sushchenya (1963) reared Artemia salina on yeast cells. In the case of Daphnia, increase in food consumption was offset by increases in the amount egested, during the period of most rapid

42

K. H. MANN

growth (Fig. 15), although as the animals approached maturity they attained rather larger body sizes in the higher food concentrations. Copepods, on the other hand, are liable to utilize periods of high food abundance to accumulate fat reserves on which they can later draw. Petipa (1965, 1966) observed the physical dimensions of the fat bodies of Calanus heligolandicus after feeding in the euphotic zone, and after descent to the deep waters. She assumed that the decrease in size of

__

...... -... ".50

#C... I .

0

4

8

12

16

20

24

28

L."

_.__._ -.--.--.--.

32

36

40

Time (days)

FIQ. 15. Growth curves of Daphnia fed at four concentrations of Chlamydomonaa (numbers indicate concentration in thousands/ml). From 5. Richman (1958). Reproduced with permission from Ecol. Monogr. 28, p. 281, Fig. 4.

the fat droplets during descent was entirely due to consumption in respiration and concluded that the metabolic rate of a migrating animal was 35 times the routine level. This assumption seems quite unwarranted. If true, it is difficult to see how any advantage of the type demonstrated by McLaren (1963) could accrue to a migrating animal, for the metabolic cost would be prohibitive. The value of studies of energy budgets of plankton, in the context of whole ecosystems, is to provide an indication of the efficiency with which energy in the food is converted to zooplankton production. Production, P, may be compared with total food consumed, C, or with

P

that fraction assimilated, A . - (or K , of Ivlev, 1939b) is the parameter C of greatest ecological significance, and Slobodkin (1959) used the term

43

AQUATIC ECOSYSTEMS

TABLEIX Energy budget of pre-adult Daphnia after the first six days of growth at four concentrations of Chlumydomonaa. (From Richnzan, 1958)

R

Food conc. (cells/ml/day)

C Energy consumed (cal.)

P Energy of growth (cal.)

Energy of respiration (cal.)

25 000 50 000 75 000 100 000

0.469 0.582 1.388 1.910

0.062 0.053 0.066 0.074

0.050 0.039 0.050 0.052

ecological efficiency to denote

P -

C

P Energy of egestion (cal. by dfl.) 0.357 0-490 1.272 1.784

P -

-

(%I

(%)

13.22 9-11 4.76 3.87

55.26 57.61 57.61 58.64

P A

C

for a population. However, laboratory

P

work on zooplankton has almost always shown that - is more variable C

P

and difficult to predict than - (K, of Ivlev). For pre-adult Daphnia A

P

grown in different food concentrations, Richman found that - was A

P

nearly constant a t 55-59%, while - varied from 13 to 4% (Table IX). C

P

I n adult Daphnia - was in the range 52% t o yoyo, when production of A young was taken into account, although the efficiency of growth production was only 4%. Klekowski and Shushkina (1966) similarly found that P for pre-adult Macrocyclops - was near to 50% for three different A feeding levels. At a fourth, higher feeding level there was much more variability, with an inexplicable rise in efficiency between the 6th and 14th days of development (Fig. 16). Slobodkin (1959, 1962) carried the study of the energetics of Daphnia from the level of the individual organism to that of the population. He kept 50 ml cultures of Daphnia in the laboratory at five levels of feeding and simulated predation by removing a fixed proportion of the number of newborn every 4th day. I n some experiments the smallest animals were selectively removed, in others, the largest. For “young removal” populations the size of the residual population could be predicted from: P_F - 1-- F Po 2-F‘ where Po = size of population with no removal PF = size of population with a removal rate F .

K. H. MANN

44

_.'......... ..

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

........ ,

+

_.

r'.

,.-.a

16 18 20 22 24 26 0 2

4

6 8

4

6 8 10 12 14 16 18 20 22 24 26

10 12 14 16 18 20 22 24

3

+

,$

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

40X) .

0

'

'

8

0 2 4 6

'

c

'

'

m

..&,

I

,

,

,

8 10 12 14 16 18 20 22 24 26 0 2

Age (days)

FIG 16. The energy parameters of Macrocyclop8 albidua at four food concentrations: a, 0.1; b, 1.0; c, 5-0; d , 10.0 mg/l of Paramecium. 4, food consumption; - - - - - P , production; R, respiration; A , assimilation; ........................ P P KI=c; + + + + + + K , = x .

.......

-

Deviations from this equation in "adult removal" populations were attributed to the failure of the populations to use all the food supplied, and were used as a basis for estimating the amount of food consumed. Figure 17 shows that ecological efficiency increased with increasing intensity of predation, to an upper limit of about 13 % in adult removal populations, but no more than 4% in young removal populations. This is because the former procedure left behind the fast-growing, efficient individuals while the latter left behind the slow-growing or moribund individuals. On the basis of this and similar experiments with a carnivore, Hydra, feeding on Artemia, Slobodkin postulated that i n nature

45

3

F FIQ.17. Maximum estimates of ecological efficiency

as a function of F ,

the rate of removal. Upper line, removal of adults; lower, removal'of young. Fmm L. Slobodkin (1962). Reproduced with permission from Ada. Ecol. Res. 1.

ecological eeciency is in the range 5% to 15% or 20% for a wide range of organisms. It is now common to use a notional 10% at each trophic level when making rough estimates of energy conversions in food chains.

2. Benth8 The pioneer work was carried out by Ivlev (1939a). He studied the oligochaete worm Tubifex tubifex feeding on mud. He mixed platinum tracer with the mud and estimated the amount of food consumed from the amount of platinum in the faeces. Food and growth were expressed in calories and compared with respiration. I n the equation

C = P+R+F+U

46

K. H. MANN

the first three terms were determined experimentally and P+ U was P determined by difference. - was 62%. A A study of an algal browser was made by Trama (1957). The algae were grown on glass plates, labelled with 32Pand fed to an ephemeropteran nymph. Food assimilation was estimated from the radio-activity of the nymphs. He concluded that only 53% of the ingested calories were assimilated, that

P

P

averaged 14.5% and - 28%. Berezina (1957) C A worked on a carnivore, Aeshna grandis, and Fischer (personal communication) on Lestes sponsa. The latter study involved rearing the animals in the laboratory on a diet of Daphnia and Tubifex from one day after hatching until the onset of metamorphosis 36 days later. It is noticeable how much higher are the efficiencies of the carnivores,

P

- declining

-

slowly from 35% to 25%, and

P

- from 90% to 70%. SimiC A larly, Sushchenya and Claro (1966) studying the energy balance of the crab Menippe mercenaria, found that under laboratory conditions the P P average value of - was 71 %, and - was 6S%, since the assimilation A C efficiency on the fish diet was 96%. It is important to note that optimum growth efficiencies are attained only when organisms are feeding on foods to which they are best adapted, or for which they exhibit a preference. Thus, Carefoot (1967) studied the feeding and growth of Aplysia punctata on eight species of marine algae. He measured all terms of the balanced energy equation, including the metabolism of resting animals. Following Winberg (1956) (see also p. 50 following) he assumed that the metabolic rate in nature was about twice the resting level. On this basis, the preferred seaweeds, Plocamium and Cryptopleura were associated with the best growth rates and with energy equations which balanced within 1 yo and 3 yorespectively. When fed on other species, the equation showed a marked imbalance, which he attributed to the animals having their metabolic rate depressed by the shortage of preferred food. One of the few energy budgets for a population of benthic animals was produced by Kuenzler (1961a, b) for the ribbed mussel Modiolus demissus living in a Georgia salt marsh. Growth and gamete production were measured, and then calculated on a population basis. Metabolic rates were determined from oxygen consumption both in air and in water, and at various temperatures and body sizes. The total oxygen consumption by the population was calculated from the frequency distribution of the size classes, monthly mean temperatures and dura-

AQUATIC ECOSYSTEMS

47

P

tion of the marsh flooding. He concluded that - for the population was A about 25%. Sushchenya (1967) studied populations of the amphipod Orchestia bottae limited to piles of decaying seaweed. Through the life P P history of the animal - varied from 60% to 30%, and - from 30% A C to 8%.

3. Fish The economic importance of fish has meant that there have been numerous studies of their feeding, bioenergetics and growth. The literature to 1966 has been summarized in the contributions of Warren and Davis, Beamish and Dickie, and Mann to the symposium volume edited by Gerking (1967). Warren and Davis give a critical review of the balanced energy equation and its evaluation and reported on laboratory experiments to determine the magnitude of the various terms. Beamish and Dickie concentrated on the terms A = R + P and discussed (i) the factors affecting R as determined by measurements of the oxygen consumption of fish and (ii) the results of food-growth experiments in which R was determined as A - P . They showed that the two methods give comparable results, and went on to discuss

P

-. Mann contributed to the symA posium a review of methods that have been used to determine the food requirements of fish populations in nature. No attempt is here made to review the whole field, but a few points are selected for particular attention. The first is the generalization which Paloheimo and Dickie (1966b) derived for the value of K,. They found that the logarithm of K , was linearly related to the food assimilated by an equation of the form: properties of the parameter K,, i.e.

P

log K , = log- = - a - b . A A

or P = A e x p ( - a - b . A )

where a and b are parameters fitted to the linear form of the equation. This implies that the growth efficiency decreases by a constant fraction, b, with each unit increase in the rations. The relationship appears to be independent of body weight so long as environmental conditions and feeding rates are such as to maintain fish of various sizes within the normal limits of low routine and active metabolism. It is surprising that if a large fish and a small one are given the same ration, such that it is near the minimum ration for the large fish and the maximum for

48

K. H. MANN

the small fish, they will utilize it with the same efficiency, but the prospect of a valid general principle in this field is most welcome. Combining the previous equation with the relationship R = A - P, we have R = A (1-exp { - a - b . A } ) . Paloheimo and Dickie re-analysed the results of feeding salmonid fish on different diets, (1) hatchery mash, (2) G ammam and (3) live minnows, the important difference being the particle size. They were able to show that the three types of food led to very different growth efficiencies ( K lines) (Fig. 18) suggesting that when the particle size

f

3

e

1.0

Diet

I

(3

10

I

Log body weight

-W

001

I00

10

20

Rations - A

( relative units)

2c

-

4

1

(d) 3

I

10

f

2

B

e

(3

C

10

Rations

-A

20

I

0

0

10

30 40 Rations - A

20

50

FIG. 18. A hypothetical example, baaed on the feeding and growth of brook trout (Salvelinus fontinalia) to show the effect of feeding on different diets on ‘(a)respiration in relation to body size (b)growth efficiency (c) respiration in relation to food assimilated and (d) growth production in relation to utilizable food obtained on each diet. From F. W. H. Beamish and L.M. Dickie (1987). Reproduced with permiasion from “The B i o l o ~ d Bad6 of Freshwater Fish Production”. Blackwell, Oxford.

AQUATIC ECOSYSTEMS

49

was small a greater proportion of the energy of the ration was expended in getting food, and proportionately less was available for growth production. This is confirmed by Fig. 18c which shows the relationship between R and A , under constant environmental conditions. Figure 18d shows the relationship between production and food assimilated, in the three diets, and indicates the importance of particle size in determining the pattern of fish production. Their analyses suggested that variations in temperature affected the rate of food assimilation but not the efficiency of its use. On the other hand, variations in salinity and in the amount of nitrogenous waste in the water appeared to have profound effects on both energy turnover and its efficiency of utilization for growth. For those interested primarily in natural ecosystems, the critical question is: can the results of laboratory studies on metabolism and growth be extrapolated to field conditions? The subject WM considered in great detail by Winberg (1956). He pointed out, in effect, that in the balanced energy equation

C = P+R+P+U it is possible to measure the growth and gonad production of a natural population in the field, and it is reasonable to extrapolate laboratory data on faecal production and excretion from the laboratory to the field, so that if only one could predict the rate of respiration in the field the equation could be solved. There is so much more work on the metabolism of fish than on other kinds of aquatic animals that the point can be discussed in considerable detail. As has been mentioned in relation to several other groups of poikilotherms, the relationship between oxygen consumption and body weight generally follows the equation:

R

=

aWY

or logR = log a + y l o g W . Winberg (1956) fitted the data from a very large number of sources to this equation and suggested that a value of y = 0-8for the slope of the line is a reasonable approximation for most kinds of fish. The value of the intercept, a,is influenced markedly by temperature and activity, but characteristic values can be assigned to particular groups of fish performing routine metabolism at a particular temperature. Thus, for instance, Winberg suggested that the respiration of all cyprinid fish with the exception of goldfish, carp and tench at 20°C approximated to: R = 0.336 W0**

50

K . R. MANN

where R is oxygen consumed in ml per hour and W is in g. He further maintained that respiration a t other temperatures could be predicted from the curve of Krogh (1916). This hypothesis was checked for a variety of fish species from the River Thames by Mann (1965) and found to be substantially true. Winberg further suggested, from indirect evidence, that the metabolic rate of fish in nature is a t about twice the routine level. Paloheimo and Dickie (1966a), approaching the question by an analysis of data on food and growth, showed that R calculated from R = A - P , showed the same kind of relationship to body weight as that found by respiration studies, viz. R = 0 1 W y . They found that fish were remarkably conservative in the level of the weight exponent y , most values being close to 0.8, and that a responded to temperature, feeding level and combinations of the two, ranging from the routine metabolism level for fish held on a maintenance diet (designed to produce zero weight change) to an active metabolism level for fish fed ad libitum. They found that the long-term effect of temperature on 01 was comparable with that predicted by the Krogh correction, at ad libitum feeding, but was significantly lower when food was limited. They concluded that a homeostatic mechanism operates, working to maintain a particular type of dynamic balance in the fish’s body. Energy expenditure, R,results in activity which in turn acts upon food supply to produce more energy-giving food, and the fish adjusts its metabolic level until it is in some dynamic equilibrium with its environment. I n order to predict the rate of energy transformations by fish in nature it is of critical importance to know at what level the dynamic equilibrium is achieved. There are two pieces of evidence which suggest that Winberg’s hypothesis, of twice the routine level of a resting fish, is about right. Ivlev (1960, 1961) observed a population of young bleak (Alburnus alburnus) which was accidentally introduced into a hatchery pond. They were feeding almost exclusively on Cyclops. During an 18-day period of intensive observation they fed from a population having a mean density of 808 cal/m3 and grew a t a rate of 5.025 callday. Ivlev had previously established that the actual food consumption c‘ is related to the maximum food consumption C‘ by the equation

c‘ = C’(l-10-PP) is a coefficient. The value of j3 was where p = food density and obtained by determining experimentally the maximum food consumption and the actual food consumption at various food densities. The rate of respiration was determined a t various swimming speeds; the speed of swimming was related to food concentration and it was

51

AQUATIC ECOSYSTEMS

estimated that when feeding in the pond the fish were respiring at 3.15 times the basal rate. If the fish spends a hours per day feeding, the energy of the food consumed, C, is: C = ac’ = aC‘ (1 - 1O-pp) Assuming that 80% of the food is assimilated: O.8C = P + R = + a (R(active) -R(basal)) + 24 R(basal). Solving both equations simultaneously, a = 9.6 hours/day. In feeding for 9.6 hours per day they consumed 38.3 cal per fish, of which 7.7 cal were egested, 25.58 were respired and 5.025 were accumulated in growth. The rate of respiration, averaged over the day, is a little under twice the standard rate, which supports Winberg’s point of view. Edwards (1968) estimated the respiratory rate of young plaice (Pleuronectes plutessu) from the rate of elimination of 65Zn from the body. He showed that in the laboratory the rates of elimination of the isotope were reasonably constant in the period 7-17 days after administration, and he was able to establish a correlation between the rate of elimination at different temperatures and the rate of respiration (Fig. 19). He then placed fish in a large netting cage in the sea and 30

.

P

25 25 -

0

._ E 0

52

15

--

a c

N

u, (D

10 .

5 -

0 0

0.1

0,2

03

I

I

I

04

05

06

Respirotory rote

I

0.7

8

( c c /g / h

FIG.19. Correlation between ESZneliminated in the period 7-17 days after intake, and the respiratory rate. From R. R. C. Edwards (1968). Reproduced with permission from Nalure, Lond. 216, pp. 1335-1337.

52

K. H. MANN

determined the respiratory rate from the rate of isotope elimination. It was 2.03 times a “standard rate” (defined as the rate of respiration of fish fed until 24 hours before measurement and at rest during the period of measurement). This lends further support to Winberg’s formula, although it might have been better if the correlations between elimination of ssZn and respiration had been produced by changes in activity and diet rather than temperature. Estimates of the total energy requirements of populations of several species of fish in the River Thames were made by Mann (1964,1966). In the first paper the balanced energy equation C = P+ R+P+ U was solved for each size group of fish in the following way. P, growth production, was obtained by multiplying the observed annual growth increment of each age class by the average number of fish per unit area and assigning a calorific value of 1 g fish flesh (fresh weight) = 1 kcal. F + U was assumed to be 20% of the energy of the food ingested. R was calculated, following Winberg, as 2 x 0.336 WOa at 2OoC with appropriate corrections for the average temperature of the river in each month of the year and using the value of W appropriate to the average weight of fish in each age class during the year. I n the second paper, Mann (1965) refined this method by taking into account the decline in numbers and increase in weight of the fish during the course of the year. It was necessary to make the simplifying assumption that the whole of the year’s growth and mortality occurred at a constant relative rate during the months April to September. Then the number of fish at time t = Noe-zt = N ( t ) and the weight of a fish at time t = Woegt= W ( t ) where z is the instantaneous mortality rate and g is the instantaneous growth rate. The energy of respiration on a monthly basis was given by:

Id

d+l/lZ

R

=

N(t)A[W(t)]O*8 x2

where A is a constant determined by the temperature, and the energy of production was given by:

P

jd

d+1/12

=

N(t)dW(t).

+

Assuming that the energy of F U is 20 % C, the total energy requirement for each month of the growing season was given by:

C = 1-25 (R+P).

53

AQUATIC ECOSYSTEMS

The calculations for the winter months were made on the assumption of constant values of N and W , as in the 1965 paper. Appropriate corrections, amounting to more than 5% on the population energy budget, were made to account for germ cell production. When the energy budgets for each year group had been completed it was possible to compare the ecological efficiency (population K , efficiency) of the various age classes (Table X). The decline in efficiency with TABLEX for each year class of roach and bleak in

Poplation ecological esciency

the River T h a m . Figures are percentages. (From Mann, 1966) Year clam

I

I1

I11

N

V

VI

VII

VIII

IX

Overall

advancing age is clearly demonstrated, and shows that the overall population efficiency was at the low end of the range predicted by Slobodkin.

B. T U R N O V E R

O F MATERIALS

Two kinds of investigation are to be dealt with under this heading. In the first, the balance between food intake, respiration and production has been determined by measuring the biomass of food and growth and expressing them as either dry organic weight or carbon. The rate of respiration, measured as oxygen consumed, has been expressed as the dry weight or carbon content of material consumed in respiration. These studies do not differ in their fundamental approach from many of the energy budgets discussed earlier, for the raw data could just have well been converted to calories. I n fact, Odum (1962) took some organic matter data of Riley (1956) and Harvey (1950) and converted them to an energy flow chart. The second group of investigations are those concerned specifically with phosphorus or nitrogen budgets of animals. An example is the work of Gerking (1962) in which he measured the nitrogen uptake, nitrogen excreted and nitrogen accumulated in production by bluegill sunfish. Such studies focus attention on the turnover of materials in an organism and may reveal phenomena which

54

K. R . MANN

accompany energy metabolic processes but differ in timing and in magnitude In constructing such a budget, the equation is

C = P+F+U, with no reference to R, since the material released in metabolism is measured in the excretion.

1. Zooplankton For detailed reviews on the nutrition, metabolism and production of zooplankton, see Raymont (1966), Conover (1968) and Corner and Cowey (1968). Conover (1964) determined the assimilation efficiency of Calanus by analysing the organic matter content of the food and the faeces, on the assumption that only the organic component of the food was significantly affected by digestion. He found a high assimilation efficiency and no falling off in efficiency when food was very plentiful. Marshall and Orr (1955, 1956) had much the same experience, but Beklemishev (1957, 1962) and Cushing and Vucetic (1963) found that when food was plentiful copepods ingested large quantities and assimilated very little. This is yet another difficulty in the way of predicting food conversion efficiencies for marine zooplankton. l4C has been used to study the turnover of carbon compounds by zooplankton. The organisms are allowed to feed on the labelled material, transferred to a culture of non-active food, given time to clear their guts, and then have their activity counted as a measure of the amount of carbon assimilated. Interpretation of the results depends on the validity of rather a large number of assumptions (Conover, 1964). There must be complete and rapid mixing of the isotope and the carrier, and there must be no excretion of radio-carbon before the measurements are made. Since the organism consists of a number of carbon pools with different turnover times, this is difficult to control. Sorokin (1966) used the technique to demonstrate for several species that the rate of food uptake increased with increasing food level to an optimum, beyond which there was little change. Lasker (1966) operated a 3-level food chain by feeding Euphausia on nauplii which had been fed on radio-active algae. Marshall and Orr (1961) and Rigler (1961) have studied the turnover of radio-phosphorus by zooplankton. The former found that it took about one week for the 32Pto come in to equilibrium throughout the body of Calanus finmarchicus and that an amount equal to the whole of the phosphorus in the body was excreted in about 20 days. They concluded that the excretion of zooplankton is an important factor in the regeneration of phosphorus above the thermocline in the sea.

AQUATIC ECOSYSTEMS

55

Pomeroy et al. (1963) reached similar conclusions. I n freshwater habitats Rigler (1956) found that the bacteria appeared to be playing a much more important role than the zooplankton in the turnover of inorganic phosphorus. Another approach to the turnover of materials in zooplankton is that of Corner et al. (1967), who produced a nitrogen budget for the developmental stages and the reproducing adults of Calanus Jinmarchiczcs when feeding on the diatom Skeletonema costatum. The rate of nitrogen excretion per unit body weight decreased with increasing body size and the percentage assimilation averaged 61.7 with no clear relationship to food concentration. During growth from egg to adult,

P

- = 34%, and for a female producing 250 eggs in an adult life of 35 days,

C

P

was 14%. The overall ratio for both phases of the life history was C about 24%. Clearly, the amount of nitrogen ingested but not retained by zooplankton is very considerable, and Harris (1959) estimated that in Long Island Sound the excretion of nitrogen by zooplankton was responsible for about half the total regeneration.

-

2. Benthos One of the f i s t studies of the turnover of material in a benthic population was that of Kuenzler (196lb) on the mussel Modiolus demissus in a Georgia intertidal salt marsh. The rate of filtering was determined from the rate of decrease in radioactivity of a suspension of 32P-labelleddiatoms. The quantity of 32Passimilated and the activity of the faeces were also determined. The rate of phosphorus elimination was measured chemically in the laboratory at three temperatures; the rate of uptake of phosphorus from solution was determined using 32P. Although the filtering rate experiments showed higher rates a t higher temperatures and lower rates per gram body weight in larger animals, the data were combined to give an average filtering rate of 6.8 I/g/h. When an attempt was made to balance the phosphorus of food consumed against phosphorus retained in the body, egested or excreted, only 54% of the consumed material could be accounted for. It was assumed that the balance had been lost with pseudofaeces. The data were combined with population data to give the population budget illustrated in Fig. 20. The food requirements were calculated by summing the observed rates of loss in egestion, excretion, reproduction and mortality. The observed filtering rate was combined with data on time available for filtration and concentration of particulate matter in

56

I(. R. MANN

the natural water to yield the estimate of rate of removal of particulate phosphorus. As in the laboratory experiments, the difference between rate of removal and rate of consumption was attributed to pseudofaeces. From these figures Kuenzler calculated that the rate of assimilation of phosphorus was 320 pg/m2/day; with 37 mg/m2 contained in the population this gave a turnover time of 115 days. An amount equivalent to all the particulate phosphorus in the water was removed by the mussels every 2.6 days, so this was the maximum turnover time for the water (other populations of filter feeders in the system would tend to Water Porticulote Phosphate Dissolved organic

14.000 19,000

6 600 39,000

Porticulote Phosphate

5410 70

Modiolus Population

Mortality

21

Gametes

It

Dissolved organic 23

25,000 Pseudofaeces 4700 37,200

Phosphate

I\Faeces

260

460

I I ,

/

MUD’

FIG.20. Diagram of phosphorus flow through the mussel population, in pg P/m*/day. Biomass in pg P/ma. The values in food and pseudofaeces are those necessary to balance the other, measured rates. From E. J. Kuenzler (106lb). Reproduced with permission from Limnol. Oceonqn. 6, p. 410.

reduce this figure even more). Much of this filtered material was deposited on the mud surface as faeces and pseudofaeces and no doubt was regenerated fairly rapidly by micro-organisms and deposit feeders.

P

When measured in terms of phosphate the ratio - was very low, of the C

P

order of 4%; - was about 10%. When the activities of the mussels in

A

promoting the circulation of phosphorus in the system were compared with their contribution to energy flow (Kuenzler, 1961a), it appeared that their activities as biogeochemical agents were the more important. A similar conclusion was reached by Johannes (1964) in respect of the phosphorus budget of the marine amphipod Lembos intermediw,

57

AQUATIC ECOSYSTEMS

for of the phosphorus ingested only about 16% was assimilated, the remainder being egested, much in soluble form. Hence the amphipod, which feeds on diatoms, was most active in transforming the diatom phosphate into a form in which it could be further acted upon by bacteria or taken up by other diatoms. The phosphorus content of the whole animal, including its gut, was turned over every 6-6 hr.

3. Fish The study of turnover of nitrogen by fish populations was pioneered in Ivlev’s laboratory (Meien et al., 1937). Fish were removed from their 12 I

-6 P -P .-2

10

0 0

1952 Experiment 1953 Experiment

8 -

u 6c

0

4 -

c 0 0-

e

c 2-

z

00

-2 0

I

I

5

10

1

I

I

20 25 Nitrogen consumed ( m g l d a v ) 15

I

30

35

FIO.21. Relation between nitrogen consumed and nitrogen retained for a fish of 26 g in two 30-day experiments with bluegill sunfish feeding on meal-worms. From 9. D. Qerking (1962). Reproduced with permission from EwZ. Monogr. 32,Figs 7 and 8.

environment and their rates of nitrogen production in faeces and urine were determined. Growth production was measured and the equation C = P+P+ U completed by summing the right-hand terms. When extended to all classes of a population, the food requirements of the population were predicted. The method rests on the assumption that nitrogen production after catching is the same as that in nature, for which there is very little evidence, and which seems an unlikely hypothesis. Yet the method has been used up to recent times (Shul’man, 1962). Gerking (1962) summarized a long series of experiments on the ratio between food and growth in terms of nitrogen. One such relationship is shown in Fig. 21. Prom this he deduced that a fish of comparable

58

K . H. MA”

weight in Wyland Lake which retained 1.7 mg of N per day consumed 11.5 mg per day. I n a parallel series of experiments he determined the efficiency of protein utilization for growth, in relation to weight (Fig. 22). The point for the Wyland Lake fish was inserted in Fig. 22 and it was assumed that the efficiency varied with size in a manner parallel to that in laboratory experiments. This lower line was then used to predict the food requirements of a fish population of varying sizes. On the whole, it appears that the study of nutrient turnover by 40

\

Laboratory experiments

N .

Log y = 369

-0 0 0 5 2 4 x

‘..

Wyland lake Log y = 19.3 - 0 0 0 5 2 4 ~

5t 0

5

10

15

20 25 30 Dry weight ( g )

35

40

45

50

55

FIG.22. Protein utilization for growth related to the size of bluegills. Upper curve derived from feeding experiments. Lower curve drawn parallel to upper through a point representing the observed growth in a natural population. From 9. D. Gerking (1962). Reproduced with permission from Ecol. Monogr. 32, 47.

animals has yielded less quantitative information about the workings of ecosystems than have the studies of energetics, mainly because the techniques involved are more time consuming. However, when both methods are applied to the same population, as in the case of Modiolus demissus, it appears that in some instances the turnover of nutrients may be ecologically more significant than the transformation of energy.

V. S T U D I E SO F D E C O M P O S I TI P ON ROCESSES I n the diagram in Fig. 1, there is a block labelled “decomposers” which receives dead organisms or parts thereof, faeces and excreted

AQUATIC ECOSYSTEMS

59

material, from all trophic levels. Its function is to regenerate materials which can be taken up by the primary producers, and the organisms primarily responsible are bacteria and fungi. However, we have already seen that substantial amounts of nitrogen and phosphorus pass directly from herbivores and carnivores to the algae, thus by-passing the decomposers. I n situations where decomposers are concentrated, such as bottom deposits, there is a whole ecosystem of micro-organismswith all its trophic levels which has so far been very little studied. In terrestrial habitats particulate and soluble organic matter, upon which the decomposers act, tends to be concentrated in the soil, but in aquatic habitats large amounts are also dispersed throughout the water. Thus, Juday (1940) estimated that in Lake Mendota the organic matter in solution was nearly twice the amount present in the plankton, benthos and fish combined. I n the oceans the deep water has concentrations of dissolved organic carbon which according to various authors and according to location are in the range 0.5-3.0 mg/l (Jsrgensen, 1966; Menzel, 1967), and particulate organic matter of the order of 10 to 500 pgll. Surface concentrations may be an order of magnitude greater. The dynamics of dissolved and particulate organic matter is under active investigation, but there is as yet very little agreement on general trends. Soluble organic material is produced by phytoplankton and zooplankton excretion (Fogg, 1963; Hellebust, 1967; Webb and Johannes, 1967) and it seems probable that there is some truth in the idea of Putter (1909) that organic matter in solution can be used by aquatic animals (Collier et al., 1953; Stephens, 1967; Chapman and Taylor, 1968). It is certainly taken up by bacteria which are used as food by filter feeders. Moreover, Sutcliffe et al. (1963) showed that dissolved organic matter can be converted to particulate form at suitable interfaces, such as the surfaces of bubbles, and Baylor and Sutcliffe (1963) showed that Artemia will feed on particles formed in this way. Thus, the sun’s energy which creates wave action may be used to recycle organic matter, converting i t from a low energy form to a high energy form which animals can use as food. If this process is common and widespread, animals may be receiving an appreciable amount of energy from the sun through the mechanical activity of waves rather than by the chemical activity of photosynthesis. Organic matter originating from the land often contributes the greater part of the energy of a freshwater ecosystem (Teal, 1957, River Thames, see p. 36). There are descriptions of the organisms responsible for the mineralization of this material (Kuznetsov, 1959) but almost nothing is known quantitatively about such systems. Regarding the role of micro-organisms in marine ecosystems, Wood (1965) wrote “our facts are so discrete and disconnected that they do

60

K. H. MANN

not form a story and the most important truths of our disciplines are still unknown^'.

VI. THE SEARCH F O R G E N E R A LPRINCIPLES A.

VARIOUS APPROACHES

In the material reviewed so far, there is little sign of emerging general principles. One of the difficulties is that the collection of sufficient data on biomass and production rate in a complex ecosystem is such a daunting task. Sutcliffe (1965) showed a correlation between

""I

Acartia clausi

23O

0.05-

I

0.02

I

I

I

I

I

I

\

0.05-

Centropages croyeri

P B

o'20.1 -

0.5 -

I

I

t

I

I

I

I

Colonipedo aquae-dulcis

0.5

0.05

0.0002

0.00050.001 0.002

0.005

0.01 0.02

Average weight (mg)

FIG.23. Regressions of the ratio PIB on mean weight of an organism in a population for three speoies of zooplankton in the Azov Sea. P = mean daily production, B = monthly mean biomaea. From Zaika and Malovitskaya (1067).

61

AQUATIC ECOSYSTEMS

RNA concentrations and growth rates in various marine invertebrates, so it seemed likely that it might be possible to calculate growth rates and hence production from RNA measurements, but Pease (1968) found a good correlation only during the exponential phase of growth. There have been some attempts to make general statements about

P

the ratio -. Zaika and Malovitskaya (1967) used the average weight of

B

an organism in a plankton population as an index of its age structure, and found that when temperatures were comparable the younger

P

populations had higher - ratios, with linear relationships on a log-log

B

plot (Fig. 23). When various temperatures were compared both Acartia

P

and Calanipeda showed a linear relationship between log - and log

P

B

temperature. The effect of population density on the - ratio appeared

B

to be small. There is a certain amount of evidence, at least in fish populations, that the production which results from the consumption of a given

Initial number per metre‘

FIQ.24. Production (April-Sept.) versus stocking density for 0 group trout. From T. Backiel and E. D. Le Cren (1967). Reproduced with permission from “The Biological Basis of Fresh water Fish Production”, p. 281. Blackwell, Oxford.

K. H. MANN

62

amount of food is relatively constant, in spite of variations in the density of the population exploiting the resource or the number of links in the food chain. Thus Backiel and Le Cren (1967) showed that when young trout were stocked in streams at densit'ies ranging from 2-2 to 279 per m2, production per unit area was relatively constant at all densities over 12 per m2 (Fig. 24). Martin (1966) reported that trout in Algonquin Park lakes may be piscivorous or planktonivorous yet their yields are comparable regardless of the length of the food chain. Ryder (1965) correlated yield from 23 lakes with total dissolved solids and depth, rather than with the species present or length of food chain. Consideration of the relationship between growth efficiency and food abundance, food particle size and food dispersal, along the lines suggested by the work of Ivlev (1961), Paloheimo and Dickie (1961 a, b) and Parsons et al. (1969 a and b) may well lead to some understanding of the basis of such a stabilizing mechanism. B.

T H E U S E O F MICROCOSMS

One way of testing general hypotheses about ecosystems is to set up microcosms which may be experimentally controlled. Odum and Hoskin (1957) showed that community metabolism was maximal during succession rather than at the climax of periphyton development in a laboratory stream, and the controlled introduction of herbivores and carnivores into laboratory streams has provided details of the inter-related factors leading to optimal fish production (McIntire and Phinney, 1965; Davis and Warren, 1965). Warren et al. (1964) demonstrated the cumulative effect of adding a nutrient (sucrose) to an artificial stream, for there was a great increase in bacteria, insect larvae and trout production. Doubling the food supply to the trout led to a seven-fold increase in production, since in the unenriched state most of the available food was used in fish metabolism. Such non-linearity in relations between trophic levels is common and is an essential part of any theoretical model.

c. T H E O R E T I C A L M O D E L S An early application of the principles of balanced energy equations to plankton populations, and their verification in nature, is seen in the work of Riley (see review, 1963). For phytoplankton production his general equation was:

dP - = P(P,-R-G) at

63

AQUATIC ECOSYSTEMS

where P = phytoplankton population per unit area P, = a photosynthetic coefficient calculated from light, its extinction coefficient, nutrients and vertical turbulence R = phytoplankton respiration, temperature corrected G = a grazing coefficient proportional to the density of herbivores. The success of this model in predicting events in various waters is shown in Fig. 25. 40 - ( a ) Georges Bank N

E 30

coastal water

-

c

0

e

20-

0

I

- 0 N D J F M A M J J A

-:-

1940

( c ) Husan

4

1939 a3

- 4oo -

1935

-:-

1936

L

In -

g

300

-

.c

0

8 200 c u) 0

a

c

loo-

J

F

M

A

M

J

J

1932

A

S

O

N

D

J

__

F

M

A

M

J J A 1933

S

O

N

D

FIQ. 25. Comparison of observed seasonal cycles of phytoplankton (solid lines) with theoretical cycles (dotted lines) computed according to the equations of Riley (1963). From G. A. Riley (1903). Reproduced with permission from “The Sea”, Vol. 2. p. 179. Wiley, New York.

Similarly, the equation for zooplankton herbivores, H was written:

dH - zz H ( A - R - C - D ) at where A = a grazing coefficient proportional to P,up to a maximum of 8% of the animal’s weight per day R = respiratory coefficient C = predation by carnivores, taken as proportional to numbers of Sagitta D = natural death.

64

K. H. MA”

Using empirical values of C and D, good approximations of changes in zooplankton populations were achieved (Fig. 26). Riley (1963) further developed a model to take account of two more trophic levels, forage fishes and “potential tuna”. While Riley’s models were concerned with energy processes, Cushing (1959) proposed a model based on algal and herbivore population numbers and their rates of

6 9 0 c

0.00

(a)

Assimilation rate

0.06

3;

5 0.04 n 0

:: 0.02

c 0

;;“o c 0

0

-0.02

20 -

(b)

N

E

\

0 0

0

10 -

Jan

Feb

Mar

Apr

May

Jun

Jul

Aug

Sep

Oct

Nov

Dec

FIG.26. Seasonal cycle of zooplankton on George’s Bank. (a)The zooplankton growth rate, determined by plotting the postulated seasonal cycle of the coefficient of assimilation, and subtracting successively the coefficients of respiration, predation and natural death: (b) theoretical curve for variations in standing crop, obtained by approximate integration of the rate curve in (a),compared with field observations. From a. A. Riley (1963). Reproduced with permission from “The Sea”, Vol. 2. p. 179. Wiley, New York.

reproduction and mortality. This is comparable with the classical approach to fish population dynamics and is of necessity a less flexible model, for it is only indirectly concerned with the nutrition and metabolism of the organisms in the population. Nevertheless, Cushing obtained a reasonable agreement with the changes in numbers of algae and herbivores in the North Sea during a spring bloom. Dugdale (1967), on the other hand, considered in detail the relationship between limiting nutrients, algal populations and their grazers.

65

AQUATIC ECOSYSTEMS

He cited evidence for the view that the Michaelis-Menton expression in enzyme kinetics is valid for this situation, and showed that a consequence of the model is a feedback such that the fractional rate of loss of nutrients from the population (e.g. grazing, sinking) determines the concentration of limiting nutrient and the size and production rate of the population. Nutrient regeneration was not taken into account. The Michaelis-Menton equation was also used by Smith (in the press) as a basis for a model. Instead of the usual relationship between enzyme and substrate.

Q + E 2+EQ- Y + P + E where Q,E, EQ and P represent the concentrations of the substrate, the enzyme, the enzyme-substrate complex and the end-product respectively, he wrote

F+A

~

X

+B-

Y

-+ 2A

where F , A and B are the density of the food, the feeding portion of the population, and the anabolizing portion of the population. Thus the feeding animal was likened to an enzyme, and the end product of the system is more enzyme. This concept was followed through in great detail: appropriate values were inserted for rate of feeding, efficiency of assimilation, rates of loss by predation, and so on at each trophic level, thus modelling whole ecosystems. By this technique it was possible to calculate the consequences of changing some parameter of the system, such as the number of trophic levels, or the total density of organism plus free resources. Smith found that some of the consequences occurred independently of whether rate constants appropriate to elephants or aphids were used. If the basic premises of the model are sound it seems that ecosystems do indeed have properties which are independent of their species composition, but the model has yet to be tested against natural ecosystems.

VII. DISCUSSION At this point it is appropriate to take stock of the progress that has been made in understanding the dynamics of aquatic ecosystems. Only in relatively simple systems has it been possible to chart the pattern of energy flow at all trophic levels; the obstacle to further progress is the sheer complexity of most ecosystems, which has forced ecologists to concern themselves with the details of particular processes. Through the years the tropho-dynamic model of Lindeman (1942) has served well. Most organisms can be placed in one trophic level or another on '

D

66

K. H. MANN

the basis of their main feeding habits, although close investigation often reveals that a carnivore will take a certain amount of plant food, and so on. I n some cases the diet is so mixed that it is impossible to allocate an animal to one trophic level. Cummins et al. (1966) resorted to the procedure of dividing the biomass of each species among several levels, in the proportion in which it took its food from various sources. This leads to a very difficult situation in trying to evaluate energy flow through a trophic level made up in this composite manner. This problem has also been discussed by Darnel1 (1968). A knowledge of the magnitude of primary production is essential to an understanding of any ecosystem. We have seen that this aspect has been studied more intensively and with better success than secondary production, but even here there is an element of uncertainty. Some have followed the changes in concentration of oxygen, carbon dioxide or nutrients in whole bodies of water and obtained reasonable agreement between two or three of these methods, but in most cases, especially in marine environments, there remains a degree of uncertainty about the amount of material entering and leaving the study area. Moreover, radio-isotope studies have shown that a slow, long-term shift in nutrient concentration may be accompanied by rapid cycling processes in which nutrients are used in primary production and returned to the water with turnover times much shorter than the intervals between samples. The alternative is to take small samples from the study area and incubate them either in the environment or in an incubator which simulates environmental conditions. This technique, especially when used with 14C is both sensitive and convenient, but still there remain the questions of whether the samples are representative of the water mass, whether enclosure in bottles modifies the production process, and what is the influence of the heterotrophic organisms in the sample. I n cases where results from incubation techniques have been compared with those from studies of water masses (e.g. Gilmartin, 1964) the two estimates of primary production have usually differed by less than 20%. This gives some indication of the magnitude of the elements of uncertainty listed above. I n fact the methods in use for measuring primary production are as good as, or better, than those available for the measurement of secondary production. In the ideal study of an ecosystem one would be able to solve the balanced energy equation

C = P+R+F+U

for each element in each trophic level, and for each trophic level as a

AQUA!CIC ECOSYSTEMS

67

whole. I n very few instances has this ideal come near to realization, but a great deal of effort has been put into obtaining solutions for individuals of a species and for whole populations. Of all the aquatic animals, most attention has been paid to fish. Techniques are available for determining population density, age structure and growth rates, and good progress has been made in understanding the principles governing their feeding and metabolism. An excellent summary of the position was given by Winberg (1956) and his ideas were endorsed and developed further by Paloheimo and Dickie (1965, 1966a, b). It is now possible to offer tentative solutions of the balanced energy equation for some natural populations of fish (Mann, 1965). Zooplankton has also received a good deal of attention, but the measurement of production is hampered by the difficulty of keeping track of several overlapping generations. There are two basic methods of calculating production: (i) from the product of the number of organisms present and their rates of growth, measured repeatedly and integrated over the period of study, or (ii) from the product of the number of organisms lost from the population and their mean biomass, assessed at intervals through the period of study. Over the lifetime of a cohort these two methods give the same answer, and both have been used in calculating the production of plankton populations. Provided that an adequate sampling method is available, it is possible to obtain data on population density, natality and mortality. Growth data are obtained either by following the history of an age group in a population, or by simulating environmental conditions and following growth in the laboratory. Neither of these is easy, and production estimates often rely on borrowed growth data, on the assumption that it is valid to transpose them from one environment to another. The relation between weight and respiration in zooplankton often takes the same form as in fish, i.e. R = aWy, with the value of y being close to 0.8. The value of (II can be related to temperature, but it is also influenced by food concentration and seasonal variations in the material undergoing oxidation. When the food concentration is high, some zooplankton organisms pass large quantities through the gut undigested, while others increase their food assimilation and build up reserves. While it is possible to write an energy budget for a few species that have been studied in the laboratory, much more information is needed before the energy requirements of natural populations of plankton can be predicted. Benthic invertebrates are notoriously difficult to sample quantitatively, so there are very few studies of the energetics of natural populations. Yet in shallow habitats it is likely that they play at least as important a role in the transformation of energy as the plankton.

68

K. H. MA"

The point made by Carefoot (1967), that Aplysia showed the best growth efficiency when feeding on its preferred species of algae, is an indication of the subtlety of the relationships between an animal and its food that have to be taken into account. Since the measurement of secondary production is such a lengthy process, attempts have been made to find regularities in the ratio

P - so that production could be inferred from biomass measurements. B' This is a promising line for further study. Thus Zaika and Malovitskaya

P

(1967) found that log - was linearly related to the log mean weight of B an individual in the population (Fig. 23) and Mathias (personal communication) found that published data from a wide range of habitats P showed regularities in the annual - ratio, provided that organisms were

B

first sorted into those with a life span of more than one year and those with a life span of one year or less. The former lay close to the line log P = - 1.683+ 1.131 log B and the latter fitted l o g P = +0*411+1*237logB when P and B were expressed in kcal/m2. Studies of single species have often involved consideration of the

P

P

growth efficiencies - and -, also known as Kl and K,. I n most instances C A

P

P

the value of - has been found to be more constant than - in relation A C to both the age of the animal and the amount of food available. For

P

fish, Paloheimo and Dickie (1966b) showed that log - is linearly A related to A , the food assimilated, decreasing by a constant fraction with each unit increase in the rations. They showed that the value of

P

- at any given level of feeding is markedly influenced by the food A particle size and its distribution, and by variations in salinity and other chemical aspects of the environment. For those wishing to know the magnitude of the energy flow in to P and out of a trophic level, - is the more important parameter, and a C value for a population is more important than a value for a single

69

AQUATIC ECOSYSTEMS

individual. Slobodkin’s (1959) study of the energetics of a laboratory population of Daphnia, and his later work with Hydra showed that

P

- for a population (which he called ecological efficiency), depended on C

the intensity of predation and on the average age of the organisms being removed and lay in the range 6 1 3 % . Silliman (1968) performed

P

similar experiments with fish populations and obtained - values as C high as 25% at three different levels of C . It is clear that the value of

P

- for populations varies over a smaller range than the values for the C individuals within it, and that for the understanding of ecosystems much more work at the population level is desirable. Most of the results discussed above relate to the food chain phytoplankton-zooplankton-fish. However, in many situations, particularly those involving macrophytes, primary production passes first to the decomposers and is later consumed by animals feeding on either suspended organic matter or on bottom deposits. The details of this pathway of energy flow are not at all understood, even at the descriptive level, for the organisms involved have in many cases not been identified. It seems likely that organic debris is acted upon mainly by bacteria and fungi, and that bottom deposits have their own pyramid of primary and secondary consumers. When a macro-organism feeds on detritus it is liable to ingest micro-organisms from a number of trophic levels simultaneously. Lindeman’s (1942) model was concerned with energy flow between trophic levels, but we have seen that considerable insights have been obtained by studying the turnover of nutrients in ecosystems. Much of the transfer between micro-organisms is likely to be in the form of soluble organic compounds, and dissolved organic matter represents a major reservoir of energy and materials. Kuenzler’s (1961a, b) study of the mussel Modiolus revealed that its activities in trapping particulate phosphorus were ecologically more significant than the transformation of energy. Gerking (1962)studied the food and growth relationships of a fish population entirely in terms of nitrogen. The labelling of food materials with radio-isotopes has proved to be one of the best ways of studying ingestion and assimilation. For these reasons the model illustrated in Fig. 1 shows both the flow of energy and the cycling of materials, and the two are best thought of as equally valid, but complementary aspects of the functioning of ecosystems. However, the practical difficulties of producing budgets for nitrogen, phosphorus or carbon appear to be greater than for energy budgets. The techniques

70

K. H. MANN

for assessing production, respiration, and the other terms of the balanced energy equation are now available, and measurements of these values in natural populations are badly needed. They can be used to construct energy flow charts for a variety of ecosystems, thus laying the foundations of a comparative study, and they can be used as appropriate values to insert in mathematical models, through which it should be possible to explore the properties of ecosystems and the interactions of their components.

ACKNOWLEDGEMENTS The author is indebted to colleagues in the Marine Ecology Laboratory, Dartmouth, and particularly to Drs L. M. Dickie and R. J. Conover for giving generously of their time and knowledge in discussion. Mr J. A. Mathias and Drs K. W. Cummins, T. R. Parsons, W. E. Ricker and F. E. Smith, as well as others acknowledged in the text, kindly made available unpublished material. The work on the River Thames, here discussed in some detail, was supported by a grant from the Natural Environment Research Council. Drs G. A. Riley and L. M. Dickie provided valuable criticisms of the manuscript. A Bedford Institute Contribution No. 146.

NOMENCLATURE LIST O F SYMBOLS U S E D WITHOUT BEING D E F I N E D O N EACH OCCASION

A

B C F Kl

K, N P

R

U W or w

assimilation; food consumed in a specified time interval, less food egested. biomass of a population. consumption; total intake of food in a specified time-interval. egestion; faeces production in a specified time-interval. P gross growth efficiency, C' P net growth efficiency, A' number in population. production (defined in section 11);P p primary production; Pa secondary production. respiration; Rp respiration of primary producers; R8 respiration of secondary producers. excretion; material released from the body as urine or through the gills or skin a specified period of time. weight of an individual organism.

AQUATIC ECOSYSTEMS

71

ADDENDUM While this review was in press, the International Biological Programme Symposium volume “Secondary Production of Terrestrial Ecosystems” (Petrusewicz, 1967) became available. Many of the basic problems are common to both terrestrial and aquatic systems. Thus, Evans discussed the difficulty of assigning secondary producers to any one trophic level, and noted that while the grazing and detritus food chains had received a good deal of attention there were others, such as those involving sucking herbivorous arthropods and those associated with parasitism and hyperparasitism, that deserved more attention. Petrusewicz defined terms and concepts, using essentially the same symbols in the present article. He made a useful distinction between production removed by predators or decomposers, which he called elimination ( E ) ,and production of the survivors, leading to an increase of biomass (AB). Macfadyen made a detailed comparison between studies of energy flow in populations of river fish (Mann, 1965) and in populations of grasshoppers (Wiegert, 1966). The insects were sampled more intensively so that better estimates of day-to-day changes in population size were available. On the other hand the terrestrial ecosystem had a much more diverse set of microclimatic conditions, with marked diurnal fluctuations in temperature and humidity. Since the metabolic rate of an animal subjected to fluctuating conditions is very different from that of an animal kept at the mean daily temperature and humidity, it was extremely difficult to evaluate the metabolic rate of the insects in nature. Diurnal fluctuations in river temperature were relatively small, but, as in all studies of population energetics, the most intractable problem was that of extrapolating metabolic data from the laboratory to the field.

REFERENCES Allen, K. R. (1961). Bull. m r . Dep. N . Z . Fish No. 10. The Horokiwi Stream. Amren, H. (1964). 2001.Bidr. Upps. 36, 162-191. Ecological studies of zooplankton populations in some ponds in Spitzbergen. 80,266-307. Anderson, R. 0. and Hooper, F. F. (1966). Trans. Am. mkrosc. SOC. Seasonal abundance and production of littoral fauna in a southern Michigan Lake. Assman, A. V. (1963). T m d g vses. gidrobiol. Obahch. 5, 138-167. Rol’ vodoroslevykh obrastaniu v obrazovanii oragnicheskogo veshchestva v Glubokom ozere. Atkins, W. R. G. (1922). J. mar. bwl. Am. U.K. 13, 764-771. The hydrogen ion concentration of open sea water and its variation with depth and season. Backiel, T. and Le Cren, E. D. (1967). In “The Biological Basis of Freshwater Fish Production” (S. D. Gerking, ed.), pp. 261-293. Oxford. Some density relationships for fish population parameters. Ball R. C. and Hooper, F. F. (1963). In “Radioecology” (V. Schultz and A. W. Klement, Jr. eds), pp. 217-228. Reinhold, New York and A.I.B.S. Washington. Translocation of phosphorus in a trout stream ecosystem.

72

K. H. MANN

Baylor, E. R. and Sutcliffe, W. H. Jr. (1963). Limnol. Oceanogr. 8, 369-371. Dissolved organic matter in seawater as a source of particulate food. Beamish, F. W. H. and Dickie, L. M. (1967). I n “The Biological Basis of Freshwater Fish Production” (S. D. Gerking, ed.), pp. 215-242. Blackwell, Oxford. Metabolism and biological production in fish. Beklemishev, C. W. (1957). Trudg uses. gidTobio1. Obshch 8, 354-358. Superfluous feeding of zooplankton and the problem of sources of food for bottom animals. Beklemishev, C. W. (1962). Rapp. P.-v. Rkun. Cons. perm. int. Explor. Mer. 153, 108-1 13. Superfluous feeding of marine herbivorous zooplankton. Berezina, N. A. (1957). Trudg mosk. tekhnol. Inst. qjb. Prom. Khoz. 58-61. (Energy balance of dragonfly larvae Aeshna grandis L.). Birge, E. A. and Juday, C. (1922). “Wisconsin Geological and Natural History Survey”, Vol. 64, 1-222. The inland lakes of Wisconsin. The plankton. I. Its quality and chemical composition. Blinks, L. R. (1955). J . mar. Res. 14, 363-373. Photosynthesis and productivity of littoral marine algae. Boney, A. D. (1965). “A Biology of Marine Algae”, pp. 216. London. Borutzky, E. V. (1939a). Tmdg limnol. Sta. Kosine 22, 199-195. (Dynamics of the biomass of Chironomua plumosua in the profundal of Lake Beloie.) Borutzky, E. V. (1939b). Trudg limnol. Sta. Kosine 22, 196-218. (Dynamics of the total benthic biomass in the profundal of Lake Beloie.) Translation reproduced by Michigan Dept. Conservation. Borutzky, E. V. (1950). Trudg uses. gklrobiol. Obshch 2, 43-68, Materialy PO dinamike biomasy makrofitov. Boysen Jensen, P. (1919). Rep. Dan. biol. Stn 26, 1-24. Valuation of the Limfjord 1. Burkholder, P. R. and Bornside, G. H. (1957). Bull. Torrey bot. Club 84, 366-383. Decomposition of marsh grass by aerobic marine bacteria. Carefoot, T. H. (1967). J . mar. biol. Ass. U.K. 47, 335-350. Studies on a sublittoral population of Aplysia punctata. Chapman, D. W. (1967). I n “The Biological Basis of Freshwater Fish Production” (S. D. Gerking, ed.), pp. 3-29. Blackwell, Oxford. Production of fish populations. Chapman, G. and Taylor, A. G. (1968). Nature, Lond. 217, 763. Uptake of organic solutes by Nereia Virens. Clarke, G. L. (1946). Ecol. Monogr. 16, 323-335. Dynamics of production in a marine area. Coffi, C. C., Hayes, F. R., Jodrey, L. H. and Whiteway, S. G. (1949). Can. J . Res. 27, 207-222. Exchange of materials in a lake as studied by the addition of radioactive phosphorus. Collier, A. S., Ray, S. M., Magnitzky, A. W. and Bell, J. 0. (1953). Bull. U.S. Fhh. Wildl. 54, 167-185. Effect of dissolved organic substances on oysters. Conover, R. J. (1964). Limnol. Oceanogr. 11, 346-354. Factors affecting the assimilation of organic matter by zooplankton and the question of superfluous feeding. Conover, R. J. (1968). Am. 2001.8, 107-119. Zooplankton-life in a nutritionally dilute environment. Conover, R. J. and Corner, E. D. S. (1968). J . mar. biol. Ass. U.K. 48, 49-75. Respiration and nitrogen excretion by some marine zooplankton in relation to their life cycles.

AQUATIC ECOSYSTEMS

73

Cooper, L. H. N. (1933). J. mar. biol. Ass. U.K. 18,677-753. Chemical constituents of biological importance in the English Channel. Cooper, L. H. N. (1958). Rapp. P A . Reun. Cons. perm. int. Explor. Mer. 144, 35-37. Consumption of nutrient salts in the English Channel as a means of measuring production. Cooper, W. E. (1965). Ecol. Monogr. 35, 377-394. Dynamics and productivity of a natural population of a fresh water amphipod Hyallella azteca. Corner, E. D. S., Cowey, C. B. and Marshall, S. M. (1967). J. mar. biol. Ass. U.K. 47, 259-270. On the nutrition and metabolism of zooplankton. V. Feeding efficiency of Calanus finmarchicus. Corner, E. D. S. and Cowey, C. B. (1968). Biol. Rev. 43, 393-424 Biochemical studies on the production of marine zooplankton. Cummins, K. W., Coffman, W. P. and Roff, P. A. (1966). Verh. int. Ver. Limnol. 16, 627-638. Trophic relationships in a small woodland stream. Curl, H. (1962). Rapp. P.-v. Cons. perm. int. Explor. Mer. 153, 183-189. Standing crops of carbon, nitrogen and phosphorus and transfer between trophic levels in continental shelf waters south of New York. Cushing, D. H. (1959). Pishery Invest. Lond. 22,l-40. On the nature of production in the sea. Cushing, D. H. and Nicholson, H. F. (1966). Nature, Lond. 212, 310-311. Methods of estimating algal production rates at sea. Cushing, D. H. and Vucetic, T. (1963). J. mar. biol. ,488. U.K. 43, 349-371. Studies on a Calanus patch. 111. The quantity of food eaten by Cahnus finmarchicus. Darnell, R. M. (1968). Am. Zoologkt 8, 83-93. Animal nutrition in relation to secondary production. Davis, G. E. and Warren, C. E. (1965). J. Wildl. Mgmt. 29, 846-871. Trophic relations of a sculpin in laboratory stream communities. Digby, P. S. B. (1950). J. mar. b i d . Ass. U . K . 29, 393-438. The biology of the small planktonic copepods of Plymouth. Dugdale, R. C. (1967). Limnol. Oceanogr. 12, 685-695. Nutrient limitation in the sea: dynamics, identification and significance. Dugdale, R. C. and Goering, J. J. (1967). Lirnnol. Oceungr. 12, 196-206. Uptake of new and regenerated nitrogen in primary productivity. Edmondson, W. T. (1960). Mem. Ist. Ital. Idrobiol. 12, 21-77. Reproductive rates of rotifers in natural populations. Edwards, R. R. C. (1968). Nature, Lond. 216, 13361337. Estimation of the respiratory rate of young plaice (Pleuronectes platema L.) under natural conditions, using zinc-65. Edwards, R. W. and Owens, M. (1962). J. Ecol. 50, 207-220. The effect of plants on river conditions. IV.The oxygen balance of a chalk stream. Fogg, G. E. (1963). Br. phycol. Bull. 2, 1 9 6 2 0 5 . The role of algae in organic production in aquatic environments. Gaarder, T. and Gran, H. H. (1927). Rapp. P A . Rdun. Cons. perm. int. Explor. Mer. 42, 1-48. Investigations of the production of plankton in the Oslo

Fjord.

Gerking, S. D. (1954). Ecology 35, 490-498. The food turnover of a bluegill population. Gerking, S. D. (1962). Ecol. Monogr. 32, 31-78. Production and food utilization in a population of Bluegill Sunfish. Gerking, S. D. (Ed.) (1967). “The Biological Basis of Freshwater Fish Production”, 495 pp. Blackwell, Oxford.

74

K. H. MANN

Gilmartin, M. (1964).J. Fkh. Rm. Bd. Can. 21,505-538.The primary production of a B.C. Fjord. Goldman, 0. R. (1963). I n “Proceedings of the Conference on Primary Productivity Measurement, Marine and Freshwater” (M. s. Dotty, ed.), pp. 103-113.Univ. Hawaii, Honolulu. The measurement of primary productivity and limiting factors in freshwater with carbon-14. Goldman, C. R. (Ed.) (1966).Mem. I&. Ital. Idrobiol. 18 Suppl. Primary productivity in aquatic environments. University of California Press, Berkeley. Greze, V. N. (1965).Gidrobiol. Zh. 1, 3542. Fish. Res. Bd. Can. Translation No. 897. (Growth rate and production potential of fish populations). Greze, V. N. and Baldina, E. P. (1964).Trudg sevmtopol’ biol. Sta. 18. Fish. Res. Bd. Can. Translation 893. (Population dynamics and the annual production of AcartiQ chuai Giesbr. and Centropages kroyem’ in the neritic zone of the Black Sea.) Hall, D. J. (1964).Ecology 45,94-112.An experimental approach to the dynamics of a natural population of Daphnb galeuta mendotae. Harris, E. (1959).Bull. Binghum oceunogr. Coll. 17, 31-65. The nitrogen cycle of Long bland Sound. Harvey, H. W. (1950).J. mar. biol. -488. U.K. 29, 97-138. On the production of living matter in the sea off Plymouth. Hayes, F. R. and Coffi, C. C. (1951).Endeavour 10,l-4.Radioactive phosphorus and exchange of lake nutrients. Hayes, F. R. and Phillips, J. E. (1958).Limnol. Oceanogr. 3,459-475.Lake Water and Sediment. IV. Radiophosphorus equilibrium with mud, plants and bacteria under oxidized and reduced conditions. Hayne, D. W. and Ball, R. C. (1956).Linznol. Oceanogr. 1, 162-175. Benthic productivity as influenced by fish predation. Heinle, D. R. (1966).Chesapeake Sci. 7, 59-74. Production of a Calanoid copepod Amrtb tmm, in the Patuxent River Estuary. Hellebust, J. A. (1967).I n “Estuaries” (G.H. Lauff, ed.), pp. 361-366. American Association for the Advancement of Science. Excretion of organic compounds by cultured and natural populations of marine phytoplankton. Hepher, B. (1962).Limml. Oceunogr. 7,131-136.Primary production in fishponds and its application to fertilizer experiments. Hillbricht-Ilkowska,A., Gliwicz, Z. and Spodniewska, I. (1066). Verh. Int. Ver. Limnol. 16,432-440.Zooplankton production and some trophic dependences in the pelagic zone of two Masurian Lakes. Horton, P. A. (1961).J. Anim. Ecol. 30, 311-338. The bionomics of brown trout in a Dartmoor stream. Hoskin, C. M. (1959).Pub18 Inst. mar. Sci. Univ. Tex. 6 , 180-192. studies of oxygen metabolism of streams of North Carolina. Hutchinson, G. E. and Bowen, V. T. (1947).Proc. natn. A d . Sci. U.S.A. 33, 148-163. A direct demonstration of the phosphorus cycle in a small lake. Hutchinson, G. E. and Bowen, V. T. (1950).Ecology 31, 193-203. Lhological studies in Connecticut. IX. A quantitative radiochemical study of the phosphorus cycle in Linsley Pond. Ivlev, V. S. (1939a).Int. Rev. gee. Hydrobiol. u. Hydrogr. 38, 449-458. (Transformation of energy by aquatic animals.) Ivlev, V. S. (193913).Dokl. Akad. Nauk. SSSR 25, 87-89. (The energy balance of the growing larvae of Sihru8 ghndia.) Ivlev, V. S. (1939~). Dokl. Akad. Nauk. SSSR 25, 90-92.(The effect of fasting on the conversion of energy in fish growth.)

AQUATIC ECOSYSTEMS

75

Ivlev, V. S. (1939d). Zool. Zh. 18, 303-318. (Energy balance in the carp.) Ivlev, V. S. (1945). Usp. sowem. Biol. 19, 98-120. (The biological productivity of waters.) (Published in translation in J. Fwh. Rea. Bd. Can. 23, 1727-1759, 1966.) Ivlev, V. S. (1960). Bull. Math. Biophys. 22, 371-389:OnLthe utilization of food by planktophage fbhes. Ivlev, V. S. (1961). Trudg sevastopol’ biol. Stcc. 14, 188-201. Fish. Res. Bd. Can. Translation 447. (On the utilization of food by plankton eating fishes.) Jackson, D. F. and McFadden, J. (1954). Ecology 35, 1 4 . Phytoplankton photosynthesis in Sanctuary Lake, Pymatuning Reservoir. Johannes, R. E. (1964). Limnol. Oceanogr. 9, 224-234. Uptake and release of dissolved organic phosphorus by representatives of a coastal marine ecosystem. Jmgensen, C. B. (1966). “Biology of Suspension Feeding”, pp. 357. Pergamon, Oxford. Juday, C. (1940). Ecology 21, 438-450. The annual energy budget of an inland lake. Ketchum, B. H. and Corwin, N. (1965). Limnol. Oceanogr. 10 (Suppl.), R148R161. The cycle of phosphorus in a plankton bloom in the Gulf of Maine. Klekowski, R. Z. and Shushkina, E. A. (1966). Verh. Int. Ver. Lintnol. 16, 399-418. Ernahrung. Atmung, Wachstum and Energie-Umformung in Macrocyclops albidus (Jurine). Krogh, A. (1916). “Respiratory Exchanges of Animals and Man.” London. Kuenzler, E. J. (1961a). Limnol. Oceanogr. 6 , 191-204. Structure and energy flow of a mussel population in a Georgia salt marsh. Kuenzler, E. J. (1961b). Limnol. Oceanogr. 6 , 400-415. Phosphorus budget of a mussel population. Kuznetsov, S. T. (1959). “Die Rolle der Mikroorganismen im Stoffkreislauf der Seen.” VEB Deutsch. Verlag d. Wissensch. Berlin. (Translated into German from Russian by A. Pochmann.) Lasker, R. (1966). J. Fbh. Res. Bd. Can. 23, 1291-1317. Feeding, growth, respiration and carbon utilization of a euphausid crustacean. Lindaman, R. L. (1942). Ecology 23, 399-418. The trophic-dynamic aspect of ecology. Macfadyen, A. (1948). J. Anim. Ecol. 17, 75-80. The meaning of productivity in biological systems. Macfadyen, A. (1964). I n “Grazing in terrestrial and marine environments”, Crisp, D. (Ed.). Blackwell, Oxford. Macfadyen, A. (1967). I n “Secondary Productivity of Terrestrial Ecosystem”, K. Petrusewicz, (Ed.). PafLstwowe Wydawnicto Naukowe, Warsaw. McIntire, C. D. and Phinney, H. K. (1965). Ecol. Monogr. 35,237-258. Laboratory studies of periphyton production and community metabolism in lotic environments. McLaren, I. A. (1963). J. Fkh. Reg. Bd. Can. 20, 685-727. Effects of temperature on growth of zooplankton and adaptive value of vertical migration. Maciolek, J. A. and Kennedy, H. D. (1964). Verh. int. Ver, Limnol. 15, 386-393. Spatial variation in periphyton production in a mountain lake at fall overturn. Mann, K. H. (1964). Verh. int. Ver. Limnol. 15, 485-495. The pattern of energy flow in the fish and invertebrate fauna of the River Thames. Mann, K. H. (1965). J. Anim. Gcol. 34, 253-275. Energy transformation by a population of fish in the River Thames.

76

K. H. MA”

Mann, K. H. (1967). In “The Biological Basis of Freshwater Fish Production” (S. D. Gerking, ed.) pp. 243-257. Blackwell, Oxford. The cropping of the food supply. Margalef, R. (1967). A . Rw. Oceanogr. Mar. Biol. 5 , 257-289. Some concepts relative to the organization of plankton. Marshall, S. M. and Orr, A. P. (1955). J . mar. biol. Ass. U.K. 34, 495-529. On the biology of Cahnus Jinmarchicus VIII. Food uptake, assimilation and excretion in adult and stage V CaZanus. Marshall, S. M. and Orr, A. P. (1956). J . m r . biol. Ass. U.K. 35, 587-603. On the biology of CaZanus Jinmarchicus IX. Feeding and digestion in the young stages. Marshall, S. M. and Orr, A. P. (1961). J . mar. biol. Ass. U . K . 41, 463-488. On the biology of Calanus finmrchicus XII. The phosphorus cycle: excretion, egg production, autolysis. Martin, N. V. (1966). Trans. Am. Fish. SOC.95,415-422. The signi6cance of food habits on the biology, exploitation) and management of Algonquin Park, Ontario, Lake Trout. Mathews, C. P. and Kowalczewski, A. (1969). ( J . Ecol). The decomposition of leaf litter in the River Thames. (In the press). Meien, V. A., Karzinkin, G . S., Ivlev, V. S., Lipin, A. N. and Sheina, M. P. (1937). Zool. Zh. 16,209-223. (Utilization by two-year-oldcarp of the natural food supply of a pond.) Menzel, D. W. (1967). Deep Sea Res. 14, 229-238. Particulate organic carbon in the deep sea. Nees, J. and Dugdale, R. C. (1959). Ecology 40, 425-430. Computation of production for populations of aquatic midge 1a.rvae. Negus, C. L. (1966). J . Anim. Ecol. 35, 513-532. A quantitative study of growth and production of Unionid mussels in the River Thames a t Reading. Odum, E. P. (1962). Jap. J . Ecol. 12, 108-118. Relationships between structure and function in the ecosystem. Odum, E. P. and Smalley, A. E. (1959). Proc. natn. Acad. Sci. U.S.A. 45,617-622. Comparison of population energy flow of a herbivorous and a deposit-feeding invertebrate in a salt marsh ecosystem. Odum, H. T. (1956). Limnol. Oceanogr. 1,102-117. Primary production in flowing waters. Odum, H. T. (1957). Ecol. Monogr. 27,56112. Trophic structure and productivity of Silver Springs, Florida. Odum, H. T. and Hoskin, C. M. (1957). Pubh Inst. Mar. Sci. Univ. Tez. 4, 116-133. Metabolism of a laboratory stream microcosm. Odum, H. T. and Hoskin, C. M. (1958). Publs Inst. m r . Sci. Univ. Tex. 5 , 16-46. Comparative studies of metabolism in marine waters. Odum, H. T. and Odum, E. P. (1955). Ecol. Monogr. 25, 291-320. Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ophel, I. L. (1963). I n “Radioecology” (V. Schultz and A. W. Klement Jr., eds), pp. 213-216. Reinhold, New York and A.I.B.S. Washington. The fate of radiostrontium in a freshwater community. Owens, M. and Edwards, R. W. (1962). J . Ecol. 50, 157-162. The effects of plants on river conditions. 111. Crop studies and estimates of net productivity of macrophytes in four streams in southern England. Owens, M. and Edwards, R. W. (1963). Proc. SOC.V a t . Treat. Exam. 12, 126-145. Some oxygen studies in the River Lark.

AQUATIC ECOSYSTEMS

77

Paloheimo, J. E. and Dickie, L. M. (1965). J . Fish. Res. Bd. Can. 22, 521-542. Food and growth of Gshes, I. A growth curve derived from experimental data. Paloheimo, J. E. and Dickie, L. M. (1966a). J . Fish. Res. Bd. Can. 23, 869-908. Food and growth of Gshes 11.Effects of food and temperature on the relation between metabolism and body size. Paloheimo, J. E. andDickie, L. M. (1966b). J . Fish. Res. Bd. Can. 23, 1209-1248. Food and growth of fishes. 111.Relations among food, body-size and growth efficiency. Park, K., Hodd, D. W. and Odum, H. T. (1958). Publs Inst. mar. Sci. Uniw. Tex. 5 , 47-64. Diurnal pH variation in Texas Bays and its application to primary production estimation. Parsons, T. R., Stephens, K. and LeBrasseur, R. J. (1969a), J . ezp. mar. Biol. Ecol. 3. Production studies in the Strait of Georgia. I. Primary production under the Fraser River plume, Feb. to May, 1967. Parsons, T. R., LeBrasseur, R. J. and Fulton, J. D. (1969b). J . ezp. mar. Biol. Ewl. 3. (In the press.) Production studies in the Strait of Georgia. 11. Secondary production under the Fraser River Plume, Feb. to May, 1967. Pavlova, E. V. (1967). I n “Structure and dynamics of aquatic communities and populations”, pp. 66-85. (Food utilization and energy conversion by Black Sea Cladocera populations.) Institut Biologii Yuzhnykh Morei. Fish. Res. Bd. Can. Translation 974. Pease, A. K. (1968). “The Use of Estimates of Ribonucleic Acid to Predict the Growth Rates of Zooplanktonic Organisms.” M.Sc. Thesis, Dalhousie University. Pechen, G. A. and Shushkina, E. A. (1964). Sb. Biologicheskie Osnovy Rybnogo Khozyaktra na Vnutrennikh Vodoemakh Pribaltiki, pp. 249-256. Minsk. Produktsiya planktonnykh rakoobraznykh v. ozerakh razlichnogo tipa. Petrusewicz, K. (ed.) (1967). “Secondary Productivity of Terrestrial Ecosystems (Principles and Methods),” pp. 879. Panstwowe Wydawnictwo Naukowe, Warsaw. Penfound, W. T. (1956). Limnol. Oceanogr. 1, 92-101. Primary production of vascular aquatic plants. Petipa, T. S. (1965). I n “Plankton Investigations in the Black and Azov Seas”. Acad. nauk. Uk. S.S.R. 102-110. (The food selectivity of Calanus heligohndkus (Claus).)(Translation N.S. No. 72 Ministry of Agriculture, Fisheries & Food, London.) Petipa, T. S. (1966). I n “Physiology of Marine Animals”. Acad. nauk. S.S.S.R. 60-81. On the energy balance of Calanus heligolandicus (Claus) in the Black Sea. (In Russian, translated by M. Paranjape, University of Washington.) Pieczynska, E. and Szczepanska, W. (1966). Verh. int. Verein. Limnol. 16, 372-379. Primary production in the littoral of several Masurian lakes. Pomeroy, L. R. (1959). Limnol. Oceanogr. 4, 386-397. Algal productivity in salt marshes. Pomeroy, L. R. (1963). I n “Radioecology” (V. Schultz and A. W. Klement Jr., eds), pp. 163-166. Reinhold, New York, and A.I.B.S. Washington. Ekperimental studies in the turnover of phosphates in the marine environment. Pomeroy, L. R., Mathews, H. M. and Hong Shik Min (1963). Limnol. Oceanogr. 8, 60-55. Excretion of phosphate and soluble organic phosphorus compounds by zooplankton.

78

I(. H.

MANN

Pomeroy, L. R., Smith, E. E. and Grant, C. M. (1965). Limnol. Oceanogr. 10, 167-172. Exchange of phosphate between estuarine water and sediments. Putter, A. (1909). “Die Ernahrung der Wassertiere und der Stoffhaushalt der Gewasser.” Fischer, Jena. Raymont, J. E. G. (1966). Adv. Ecol. Res. 3, 117-204. The Production of Marine Plankton. Redfield, A. C. (1941). Biol. Bull. 80, 88-110. The effect of the circulation of water on distribution of the Calanoid community in the Gulf of Maine. Redfield, A. C., Smith, H. P. and Ketchum, B. H. (1937).Biol. Bull. 73,421-443. The cycle of inorganic phosphorus in the Gulf of Maine. Richards, S. W. and Riley, G. A. (1967). Bull. Bingham Oceanogr. Coll. 19, 89-135. The benthic epifauna of Long Island Sound. Richman, S. (1958). Ecol. Monogr. 28, 273-291. The transformation of energy by Daphnia &ex. Ricker, W. E. (1946). Ecol. Monogr. 16, 374-391. Production and utilization of 6eh populations. Ricker, W. E. (1968). I n “Methods for Assessment of Fish Production in Fresh Waters”. IBP Handbook No. 3 pp. 313. Blackwell, Oxford. Ricker, W. E. and Foerster, R. E. (1948). Bull. Bingham Oceanogr. Coll. 11, 173-211. Computation of f%hproduction. Rigler, F. H. (1956). Ecology 37,550-562. A tracer study of the phosphorus cycle in lake water. Rigler, F. H. (1961). Can. J . 2001.39, 857-868. The relation between concentration of food and feeding rate of Daphnia magna Straus. Riley, G. A. (1941). Bull. Bingham Oceanogr. Coll. 7, 1-73. Plankton studies. IV. George’s Bank. Riley, G. A. (1966). Bull. Bingham Oceanogr. Coll. 15, 324-343. Oceanography of Long Island Sound 1952-1954. IX. Production and utilization of organic matter. Riley, G. A. (1963). I n “The Sea” (M. N. Hill, ed.), Vol. 2, pp. 438-463. New York and London. Theory of food-chain relations in the ocean. Ruttner, F. (1964). “Fundamentals of Limnology.” Third edition, pp. 295. Translated from German to English by D. G. Frey and F. E. J. Fry, University of Toronto Press. Ryder, R. A. (1965). Trans. Am. Fwh. SOC.94, 214-218. A method for estimating the potential f%hproduction of north temperate lakes. Ryther, J. H. (1956a). Limnol. Oceanogr. 1, 61-70. Photosynthesis in the ocean aa a function of light intensity. Ryther, J. H. (1956b). Limnol. Oceanogr. 1, 72-84. The measurement of primary production. Ryther, J. H. and Yentsch, C. S. (1957). Limnol. Oceanogr. 2, 281-286. The estimation of phytoplankton production in the ocean from chlorophyll and light data. Sanders, H. L. (1956). Bull. Bingham Oceanogr. Coll. 15, 345-414. Oceanography of Long Island Sound 1952-1954. X. The biology of marine bottom communities. Sheldon, R. W. and Parsons, T. R. (1967). “A Practical Manual on the Use of the Coulter Counter in Marine Research.” Coulter Electronics Sales Co., Canada. Shul’man, G. E. (1962). Dokl. A M . Nauk SSSR 147,724-726. (Nitrogenbalance and food consumption of the Azov Anchovy, Engraulk encr&blus mzeotkw Pusanov.)

AQUATIC ECOSYSTEMS

79

Silliman, R. P. (1968). Fkh. Bull. 66, 425-439. Interaction of food level and exploitation in experimental fish populations. Sladeckova, A. (1966). Verh. int. Verein. Lirnnol. 16, 753-758. The significance of the periphyton in reservoirs for Theoretical and Applied Limnology. Slobodkin, L. B. (1959). Ecology 40, 232-243. Energetics in Daphnicr p h populations. Slobodkin, L. B. (1962). Adw. Ecol. Bee. 1, 69-101. Energy in Animal Ecology. Smalley, A. E. (1959). Proc. Salt Marsh Conf. Sapelo Island, Ueorgia. T h e growth cycle of Spartina and its relations to the insect populations in the mctrsh. Smalley, A. E. (1960). Ecology 41, 672-677. Energy flow of a salt marsh emhopper population. Smith, F. E. (1969). “Effect of Enrichment in Mathematical Models.” Proceedings of Symposium on Eutrophication, Madison, Wisc. (In the press.) Sorokin, J. I. (1966). Int. Revue ges. Hydrobiol. Hydrogr. 51, 209-224. Carbon-14 method in the study of the nutrition of aquatic animals. Stanczykowska, A. (1966). Verh. int. Verein. Limnol. 16, 1761-1766. Einige Gesetzmassigkeiten des Vorkommens von Dreiaaena p o l y m p h a Pall. S b l e , J . H. (1958). Mar. Res. 7, 1-36. Plant production in the northern North Sea. Steele, J. H. (1965). ICNAF Spec. Publ. 6 , 463-476. Some problem in the study of marine resources. Steemann Nielsen, E. (1963). I n “The Sea” (M. N. Hill, ed.), Vol. 2. Interscience, New York. pp. 554. Productivity, Definition and Measurement. Stephens, G. C. (1967). I n “Estuaries” (G. H. Lauff, ed.), pp. 367-373. American Association for the Advancement of Science. Dissolved organic material a nutritional source for marine and estuarine invertebrates. Strmkraba, M. (1963). Rozpr. csl. Akad. Ved. 73 (13) 1-64. Share of the littoral region in the productivity of two fishponds in southern Bohemia. Strickland, J. D. H. (1960). Bull. Fkh. Res. Bd. Can. 122, 1-172. Measuring the production of marine phytoplankton. Strickland, J. D. H. (1965). I n “Chemical Oceanography” (J. P. Riley and G. Skirrow, eds), Vol. I, pp. 477-610. Academic Press, New York. Production of organic matter in the primary stages of the marine food. Stross, R. O., Neess, J. C. and Hasler, A. D. (1961). Ecology 42, 237-245. Turnover time and production of the planktonic crustacea in limed and reference portion of a bog lake. Sushchenya, L. M. (1963). Trudg sewastopol’ bid. Sta. 16, 256-276. Ecological and physiological features of filter feeding in planktonic crustacea. (Fish. Res. Bd. Can. Translation No. 884.) Sushchenya, L. M. (1967). In “Structure and Dynamics of Aquatic Communities and Populations”. Acad. Nauk. Ukr.S.S.R. Institute of Biology of Southern Seas, pp. 12&135. Production and annual flow of energy in a population of Orcheetia bottae. (In Russian.) Fish. Res. Bd. Can. Translation No. 978. sushchenya, L. M. and Claro, R.(1966). I n “Issledovaniya Tsentral’ n o - A m e h n shikh Morei”. No. 1, “Naukova Dumka” Press, Kiev, pp. 217-230. Quantitative laws governing feeding, and their relation to energy balance in the commercial crab Menippe rnercenaria (Say.). Fish. Res. Bd. Can. Translation No. 931. sutcliffe, W. H. Jr., Baylor, E. R. and Menzel, D. W. (1963). Deep Sea Res. 10, 233-243. Sea surface chemistry and langmuir circulation. Sutcliffe, W. H. Jr. (1965). Gmnol. Oceanogr. 10 (suppl.) R253-R258. Growth &,imatesfrom ribonucleic acid content in some small organisms.

80

K. H. MANN

Talling, J. F. (1957).Proc. R . SOC.Lond. B 57-83. Diurnal changes of stratification and photosynthesis in some tropical African waters. Talling, J. F. (1965). Int. Revue ges. Hydrobiol. Hydrogr. 50, 1-32. The photosynthetic activity of phytoplankton in East African lakes. Teal, J. M. (1957). Ecol Monogr. 27, 283-302. Community metabolism in a temperate cold spring. Teal, J. M. (1958). Ecology 39, 185-193. Distribution of fiddler crabs in Georgia salt marshes. Teal, J. M. (1959). Physiol. 2002.32, 1-14. Respiration of crabs in Georgia salt marshes and its relation to their ecology. Teal, J. M. (1962). Ecology 43, 614-624. Energy flow in the salt marsh ecosystem of Georgia. Teal, J. M. and Kanwischer, J. (1961).Limnol. Oceanogr. 6,388-399. Gas exchange in a Georgia salt marsh. Teal, J. M. and Kanwischer, J. (1966). J . mar. Res. 24, 4-14. The use of pCOs for the calculation of biological production, with examples from waters off Massachusetts Trama, F. B. (1957). “The Transformation of Energy by an Aquatic Herbivore Stenonem pulchellum (Ephemeroptera).” Ph.D. Thesis, University of Michigan. Warren, C. E., Wales, J. H., Davis, G. E. and Doudoroff, P. (1964). J. WiZdZ. Mgmt. 28, 617-660. Trout production in an experimental stream enriched with sucrose. Warren, C. E. and Davis, G. E. (1967). In “The Biological Basis of Freshwater Fish Production” (S. D. Gerking, ed.), pp. 175-214. Blackwell, Oxford. Laboratory studies on the feeding, bioenergetics and growth of fish. Waters, T. F. (1966). Ecology 47, 595-604. Production rate, population density and drift of a stream invertebrate. Webb, K. L. and Johannes, R. E. (1967). Limnol. Oceanogr. 12, 37&-381. Release of dissolved amino acids by marine zooplankton. Westlake, D. F. (1963). Biol.Rev. 38, 385-425. Comparisons of plant productivity. Westlake, D. F. (1966). J . Ecol. 54, 745-753. The biomass and productivity of Glyceria maxima. I. Seasonal changes in biomass. Wetzel, R. G. (1964). Verh. int. Verein. LimnoZ. 15, 426-436. Primary productivity of aquatic macrophytes. Wiegert, R. G. (1965). Oikos 16, 161-176. Energy dynamics of the grasshopper populations in oldfield and alfalfa field ecosystems. Wieser, W. and Kanwischer, J. (1961). LimnoZ. Oceanogr. 6, 262-270. Ecological and physiological studies on marine nematodes from a small salt marsh near Woods Hole, Massachusetts. Williams, W. P. (1963). “A Study of Freshwater Fish in the Thames.” Ph.D. Thesis, University of Reading. Williams, W. P. (1965). J . Anim. Ecol. 34, 173-185. The population density of four species of freshwater &h, roach (Rutilus rutilus (L)) bleak (Alburnus alburnua (L.)) dace (Leucbcus Zeuciscus (L.)) and perch (PercaJEuwiatilk(L.)) in the River Thames a t Reading. Williams, W. P. (1967). J . Anim. Ecol. 36, 695-720. The growth and mortality of four species of fish in the River Thames at Reading. Winberg, G. G. (1940). Dokl. Akad. Nauk SSSR 26, 666-669. On the measurement of the rate of exchange between a water basin and the atmosphere. Winberg, G. G. (1955). Trudy Vses. gidrobiol. Obshch. 6, 46-49. Signficance of

.

AQUATIC ECOSYSTEMS

81

photosynthesis for oxygen enrichment of water during self-purification of polluted waters. Winberg, G. G. (1956). “Intensivnost obmena i pischevye petrebrosti ryb. Nauchnye Trudy Belorusskovo Gosudarstvennovo Universiteta imeni V. I. Lenina, Minsk.” Fish. Res. Bd. Can. Translation No. 194. Rate of metabolism and food requirements of fish. Wood, J. F. (1965). “Marine Microbial Ecology.” Chapman and Hall, London. Yablonskaya, E. A. (1962). Rapp. PA. Rdun. Cons. perm. int. Explor. Mer. 153, 224-226. Study of the seasonal population dynamics of the plankton copepods as a method of determination of their production. Zaika, V. E. and Malovitskaya, L. M. (1967). In “Structure and dynamics of aquatic communities”. Acad. Nauk. Ukr. S.S.R. Institute of Biology of Southern Seas. pp. 86-94. Paper No. 5. Characteristics of variability of productivity per unit biomass for some zooplankton populations. Fish. Res. Bd. Can. Translation 975.

This Page Intentionally Left Blank

Integration, Identity and Stability in the Plant Association ARTHUR N. LANGFORD

Department of Biological Sciences, Bishop’s University, Lennomille, Quebec, Canada AND MURRAY F. BUELL

Department of Botanical Sciences, Rutgers University, New Brumwick, N.J., U.S.A.

.

. 84 . 92 . 92 . 93 . 96 . 96 . 96 . 98 . 101 . 104

I. Introduction 11. The Biotic Community and the Theory of the Climax A. The Organismic Concept of the Association B. Other Clementsian Concepts and their Modification 111. The Individualistic Concept of the Association, the Continuum and Ordination A. The Linear Continuum as a Quantitative Substantiation of Clements’ Concepts of Succession B. A Criticism of the Linear Continuum . C. Recent Reassessments of the Controversy IV. Neutral Approaches to Community and Association Study V. A Modern View of the Association . A. Tansley’s Broadening of the Climax Concept . B. The Influence of Dominants . . C. The Integrated Association . D. Homeostasis in the Plant Association . E. Ecotones VI. The Question of Critical Levels along Gradual Environmental Gradients A. Introduction B. Mycorrhiza . C. Edaphic and Climatic Factors D. Ecotypes E. The Universality of Divisiveness F. Geographical Aspects of the Association Concept, with Special Reference to Stability. VII. The Special C&BBB of Auto-intoxication, Synergism and Allelopathy A. Early Work and the Period of Concentration upon Single Factor Explenations of Biological Events . B. The Emergence of an Understanding of the Complexity of Biochemical Interactions among the Higher Plants MI. Concluding Statement . References 83

.

.

.

.

.

.

.

.

. .

.

.

.

.

.

. . . .

.

.

.

.

.

. .

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

. .

104 106 107 107 111 112 112 113 114 116 117

. . . . . . . . 118

. 122 122

. 124 . 128 . 131

84

A. N. LANOFORD AND M. F. BUELL

I. I N T R O D U C T I O N Any scientist who sets out to write an introductory textbook is confronted with important decisions as to how far to take initial explanations of some aspect or other of his subject. For example, a modern geneticist, discussing meiosis as a preparation for understanding cases of independent assortment, may for simplicity choose to pass over cytological crossing over. On the other hand he may present the general idea of crossing over at the outset but not explain that the crossing over is between non-sister chromatids, leaving the impression that whole chromosomes are involved. He may, of course, seek to carry the initial explanation of normal meiosis as far as he can. The geneticist of fifty years ago, however, was not disturbed by this problem. So also plant ecologists of a like period found themselves less cluttered with facts and conflicting concepts, though they still faced the problem of choosing the depth for a textbook presentation. With the publication of Weaver and Clements, “Plant Ecology” in 1929, undergraduates using the English language had access to one of the earliest textbooks of plant ecology and probably the most influential one of its day, a textbook giving students, even in small and obscure universities with minimal library facilities, an excellent account of the ecological concepts of the day and particularly of the dynamics of vegetation, as seen through the eyes of Clements. Students in general had enough awareness of vegetation to appreciate the relatively simple stories of hydroseres and xeroseres and in most localities could see one or more examples near by. Teachers undoubtedly simplified this subject-matter, for instructional purposes, using pigeon-hole systems of thought and speech that were narrower than any of those conceived by Clements. On page 55 Weaver and Clements wrote: “As vegetation develops, the same area becomes successively occupied by M e r e n t plant communities. This process is termed plant succession. Within a region, the same finalor climax stage results from this series of successive stages whether they start in open water, on solid rock, or on denuded land. Although the movement from initial stage to climax is usually continuous, when one group of dominant phnts reaches its maximum the change is clearly marked. This is especially true when one life-form, such as that of floating plants, gives way to another, such as reeds and rushes.”

...

Even before Weaver and Clements set forth in textbook form their ideas of succession and their system of classification of vegetation, particularly that of North America, into major formations with constituent plant associations which they believed to be clearly recognizable, though with relatively narrow ecotonal boundaries, views contrary to those of Clements had been expressed, particularly by Gleason (1917, 1926) and

85

INTEGRATION, IDENTITY AND STABILITY

the polarization of viewpoints-the integrated view of the association and the individualistic nature of the association-was becoming strong. Whittaker (1962, pp. 50-55) has documented this development in great detail. At first glance it would appear that the concept of the vegetational continuum (Curtis and McIntosh, 1951; Brown and Curtis, 1952) arose as a quantitative extension of Gleason’s hypothesis of the individualistic nature of the association, giving the coup de grdce to the views of Clements and of Nichols (1929) as to the definiteness and classifiability of climax plant associations. Curtis and McIntosh (1951) made a brief reference to Clements in delimiting the “tension zone” in Wisconsin, but it is surprising that neither these authors nor Brown and Curtis (1952) nor even McIntosh (1967) in his extensive review, “The Continuum Concept of Vegetation”, made any reference to a single article by Clements. This is strange in the light of the appropriate reference elsewhere by Whittaker (1962, p. 55): “The Clementsian system has been immensely influential in the development of British and American ecology. Much discussion of terrestrial natural communities, especially in the two decades 1916-1935, concerned that system and its application or the suggestion of limitations and criticisms of it.

. . .”

I n the discussions accompanying the promulgation of the continuum concept there was no reference to the fact that the associations of Clements, as distinct from the seral associes, were considered as end points of seral developments, largely governed by climate. (Clements’ system also recognized slow changes in climax vegetation accompanying slow long-term shifts of climate.) It follows that the demonstration of vegetational continua, using Wisconsin methods, does not of itself require the abandonment of the view that there are distinct, recognizable climax associations. A great deal of the variation demonstrated by Curtis and McIntosh and by Brown and Curtis is surely due to variation in the successional status of the forest stands studied. I n papers by these men no attempt whatever is made to assess whether or not the various stands were changing in composition, through succession, in the direction of a much more uniform vegetation which would be more in harmony with the concepts of Clements. I n discussing the environmentd changes measured, Curtis and McIntosh did write (p. 492): “The presence in certain of these environmental factors of some indication of a gradient or trend related to the tree gradient is further indication that these forests represent a continuous cline from initial stages composed of pioneer species to terminal stages composed of climax species.”

Brown and Curtis, discussing the upland conifer-hardwood forests of northern Wisconsin, wrote (p. 231):j

A. N . LANOFORD AND M. F. BUELL

86

“. . .

the results indicated that all stands studied were parts of one great community complex, arranged along a gradient from pioneer conditions of low moisture, high light, low soil organic matter and low soil base content to climax conditions of medium moisture, low light, high soil organic matter and high base content. The stands formed a vegetational continuum, with a continuously varying series of species, sorting themselves along an environmental gradient whose main controlling features result from the interactions of the plants themselves.”

. ..

It remained, however, for Bray and Curtis (1957) to clarify fully the successional nature of the stands studied by Curtis and McIntosh (1951). I n discussing their 3-dimensional ordination, they wrote (p. 343): “Thus, in general, the z [or first] axis duplicates the original linear continuum

of Curtis and McIntosh. The order of species along the z axis is basically determined by an over-all linear direction in the many paths of community development within the upland forest. These paths follow a network of successional patterns which are mainly related neither to primary nor secondary succession but to recovery from past disturbance. [Surely recovery from past disturbance is secondary succession!] The coincidence that Quercus macrocarpa is both the most initial and fire resistant species, and that Acer saccharurn is the most terminal and fire susceptible species, suggests that the ultimate explanation for the composition of a forest stand in upland Wisconsin is largely an historic one. The longer a stand has been free of fire (and other disturbance forces) and the more favorable the habitat in which it occurs, the more likely it can develop to a maple-basswood forest.”

.. .

It may be argued, then, that most if not all of the stands of Curtis and McIntosh, if allowed to develop the full potential associated with their situation, would fit nicely into a single association, with Acer saccharurn as a dominant species if not the dominant species. Some workers have compared tree composition and sapling composition in a variety of stands pertinent to the present discussion. Whitford and Salamun (1954), for example, followed the methods of Curtis and McIntosh (1951) in their study of 22 forested stands in the vicinity of Milwaukee, Wisconsin, determining continuum index numbers for both trees and saplings. In these stands, collectively, three species of Quercus accounted for 35.4 yo of the total “Importance Values’’ of trees, while three species considered as more characteristic of climax forests of the area, Acer saccharurn, Fagus grandifolk and Tilth arnericana, accounted for 33.1 yoof the same total. Although Whitford and Salamun do not present actual figures for saplings, it is apparent from the scatter diagram of the correlation between oontinuum index numbers based on trees versus saplings that, with three exceptions, the shift in sapling composition has been in the direction of species classedasapproaching those of the climax forest. This is in no way surprising when one examines their map of Milwaukee County which shows that nearly all of the areas studied were classed in 1835-36 as oovered by a maple-basswood forest. The nature of today’s vegetation,

INTEGRATION, IDENTITY AND STABILITY

87

conforming roughly to the concept of a linear continuum, does not shed unfavorable light on the concept of a single climax association embracing virtually all of the area under study. Washington, D.C., is located at the boundary between the Piedmont and the Coastal Plain. There, on the eastern edge of the Piedmont, in an area mapped by Braun (1950) as the extreme edge of the oak-chestnut climax association, Dix (1957) studied a single stand, unlike any others in the area, the property of the National Park Service for 67 years. It had been protected by a high mesh fence for 42 years prior to this study and had no history of fire, cutting or grazing during the 67-year period. Dominated by Quercus alba, four species of oak accounted for 62 % of the total Importance Values of the trees, Fagus grandifolia accounted for 22 % and Acer saccharum for 1yo.The comparative percentages of total Importance Values, based on saplings were: Quercus alba, zero; four species of oak, 3.7 %; Fagus grandifolia, 33.4%; Acer saccharum, 14.0%. Tilia americana was present as a sapling (1.1%) and 13.0% of the recorded stems were of Cornus JEoridaand Carpinus caroliniana. The coming shift towards a stand characteristic of a beech-maple climax association is very plain. Dix suggested that the long-continued absence of grazing and fire may be responsible for the shift to the relatively more mesophytic condition indicated by the understory composition. With a single stand of this nature to study, Dix made no sweeping generalizations but suggested the wisdom of studying other undisturbed forests in the area. In the upland forests of northern New Jersey, in an area mapped by Braun (1950) as “oak-chestnut”, with the boundary of the hemlocknorthern hardwood forest close enough to suggest that various of its components might be present, Buell et al. (1966) carried out extensive studies of both tree and sapling components of 60 stands, using continuum methods (Curtis, 1959), slightly modified. These stands were dominated overwhelmingly by oak trees, in spite of the occurrence among them of 13 stands in which Tsuga canadensis was a leading dominant, average Importance Value of oak being 59-9%,where l00was the maximum. I n 33 of the stands a species of Quercus was the leading dominant. Some species of Quercus was the second in position among the dominants in 21 of the remaining 27 stands. In contrast, Quercus saplings (0.95-3.95 in. dbh) in the same stands were much reduced in “importance”, but made their best showing on the most generally unfavorable sites on ridge tops. Perhaps the most striking illustration of the successional trends in these New Jersey forests was revealed by graphs setting forth the ratios, “importance value of saplings/importance value of trees” for five stands that were representative of the range of situations encountered (Fig. 1). These stands, with continuum index numbers 32, 43, 68, 75 and 89,

88

A. N. LANGFORD AND M. F. BUELL

'1

-5

.3t

.Oil 1

a.c.

I

I

I

I

I

2

5

10

50

100

(FIQ.1. See legend on p. 90.)

89

INTEGRATION, IDENTITY AND STABILITY

Stand C Continuum index No.68

*I

I 2

1

I 5

I 10

I

I

50

100

-

10

Stand D Continuum index No. 75 F.G.

6 -

4A.R. 2-

/

I.V.of Trees

-

.5

T.C.

B.L.

I -

L .T. a .v.

F.A .

.3 -

-

.2

I

~

.2

.5

1.0

2

5

10

(FIQ.1. See legend on p. 90.)

50

100

A. N. LANOFORD AND M. F. BUELL

90

Stand E Continuum hdeK No. 89

3t-

.I

II

I

2

I 5

I

I

I

10

50

100

FIG.1. Graphs showing the successional shift of upland forest stands of northern New Jersey away from dominance by species of Quercus in five representative stands with continuum index numbers as calculated by Buell et al. (1966) and on substrata as follows: A, Shawangunk conglomerate; B, Brunswiok formation; C, Kittatinny limestone; D, Byram gneiss; E, basalt. In each graph the main horizontal axis displays Importance Values, based on trees, with the contact of each designated solid line with the central horizontal line giving the value, e.g. 47 for Quercus velutina in stand C. Broken vertical lines represent species found as saplings but not as trees. Solid vertical lines represent species found aa trees but not as saplings. The free ends of all sloping lines have been set at a uniform distance t o the right of their “bases” and represent the ratio, “Importance Value of saplings/Importance Value of trees”. In Tilia americana of stand C and in Betula lutea of stand D values baaed on saplings and trees were identical. All values are expressed logarithmically. Abbreviations are as follows: A., Amelanchier; A.R., Acer rubrum; A.S., Acer amcharurn; B.L., Betula lenta; B.LU., Betula lutea; C.C., Carya cordifomnie; C.D., Caatanea dentata; C.F., CornusJlorida; C.O., Carya ovalis-glabra; C.T., Carya tmentoea; F.A., Fraxinus americana; F.G., Fagus grandifolia; L.T., Liriodendron tulipifera; N.S., Nysaa sylvatica; O.V., Oetrya wirginiana; P., Pinus atrobus; P.A., Prunua awium; P.G., Populua grandidenkzta; P.S. Prunus aerotina; Q.A. Quercus alba; Q.C. Quercus wccinea; Q.P., Quercus prinua; Q.R., Quercus rubra; Q.V., Quercus velutina; S.A.,Saasafras albidum; T.A., Tilia americana; T.C., Tsuga canadensis.

where the possible range was from 10 to 100, were calculated essentially like those of the Wisconsin school, the most xeric at the 32 level, the most mesic at the 89 level. Considering, in this figure, the four species of highest Importance Values in each of the five stands, we found that 10 of the 20 values represented species of Quercus. None of these ten units showed an increased importance in the sapling class, relative to the tree class. I n five of the ten instances the oak species were not even represented in the sapling class. Only on ridges where the substratum is conglomerate (e.g. Stand A of Fig. 1) did the oaks show any suggestion of retaining any significant importance in these forests. We recognize the variable life expectancy of saplings, from species to species, but it is the

INTEGRATION, IDENTITY AND STABILITY

91

consistently overwhelming proportion of tree species other than oaks in the great majority of these stands that points to a drastic reduction in the future importance of Quercus if cutting and fire, which favor regeneration by stump-sprouting, are not active. I n our stands, as a whole, Quercus is being replaced by a variety of more mesic species, including Tsuga canadensis and Acer sacchrum. I n discussing this whole situation more fully elsewhere (Buell et al., 1966), we have stressed the significance of the process (a successional development) rather than the slowness of the process, particularly to the extent that it is dependent upon the physiographic processes of erosion. In considering further the antagonistic relationship between vegetational continua and the concept of discrete associations it is important, at the outset, to consider a key paragraph in the writings of Clements (1928, p. 100) which seems to have been overlooked by those who offered continuum data to refute Clements, whether by name or indirectly through their support of Gleason (1917, 1926, 1939). Discussing the nature of “life-history stages” leading to stabilization and climax, Clements wrote: “While the movement from initial stage to climax or subclimax is practically continuous, there are typically certain periods of comparative or apparent stabilization. These correspond to population or invasion maxima, which mark more or less well-defined stages or comrnunitiea. As noted elsewhere, such stages usually appear much more distinct than they really are, owing to the fact that the study of succession so far has been little more than the arrangement in probable sequence of stages contemporaneous in different areas. However faint their limits, real stages do exist as a consequence of the fact that each dominant or group of dominants holds its place and gives character to the habitat and community, until effectively replaced by the next dominant. The demarcation of the stages is sharper when the change of population is accompanied by a change of life-form, as from grassland to scrub or forest. I n some 8eCOndary serea there is little or no change of life form and the stages are few und indistinct. (These constitute a continuum, either in time or in space or in both, in our opinion.) I n rare cases the dominants of the entire sere may be present the h t year after a burn, for example, and the well-markedstages are due solely to the 7ccte of growth, which causes the dominants to appear and characterize the area in sequence.” (Our italics.)

It thus becomes clear that vegetational continua, to the extent that t h y express differences in successional status of the examples of vegetation studied (and this we believe they do in large measure) are not, as would appear at first glance, quantitative affirmations of Gleason’s hypothesis but rather findings which are very much in harmony with the views of Clements as to the gradual nature of succession. When we turn to organismic views of the association we will have no agreement with Clements, but this does not prevent our recognition of the understanding of developmental processes set forth in his 1928 article.

A. N. LANGFORD AND M. F. BUELL

92

11. T H E BIOTICCOMMUNITY AND O F T H E CLIMAX A.

THE

THEORY

THE ORGANISMIC C O N C E P T O F THE ASSOCIATION

Hult (1885), following a study of the vegetation of Blekinge, southern Sweden, set forth clearly the idea of succession and the idea of a climax vegetation, to which, in the absence of disturbance, developmental stages lead. It is not particularly important that Clements (1936) gave Hult credit for the climax concept. The term climax, according to Clements, came to be “applied to a more or less permanent and final stage of a particular succession and hence one characteristic of a restricted area.” Clements certainly introduced the concept of the climax as an organism in 1916 in these words: “The unit of vegetation, the climax formation, is an organic entity. As an organism, the formation arises, grows, matures and dies. Its response to the habitat is shown in processes or functions and in structures that are the record as well as the result of these functions. Furthermore, each climax formation is able to reproduce itself, repeating with essential fidelity the stages of its development. The life-history of a formation is a complex but definite process, comparable in its chief features with the life-history of an individual plant. The climax formation is the adult organism, of which all initial and medial stagesare but stages of development.

. . .”

Clements indicated clearly (1936) that he regarded climax and plant .formation as synonyms. Although neither the 1929 nor 1938 edition of Weaver and Clements’ textbook makes any reference to the climax as an organism, Clements repeated his organismic views of the climax in 1936, modifying his 1916 views (quoted above) only to the extent of substituting “biome” for “climax”. Philips (1935) presented the most intense concept of the community as a complex organism. Referring to this concept, he wrote optimistically: “At first given little or no attention, for a season somewhat derided, for another treated with condescension by most ecologists, this concept is gradually being accepted by a few, has gradually met with ever-increasing respect from a large number of others”. Philips’ optimism was unjustified and the concept of the community or of the association as a complex organism has lost what little hold it had in the minds of ecologists and may be dismissed, although it must be recognized that Margalef (1957), a zoologist of considerable mathematical competence, has argued that the comparison of the community with an organism goes beyond external similarity and rhetoric, and that developmental processes in both systems lend themselves to description in terms of information theory and entropy. It is difficult enough to deal with the concept of the individual organism in various coelenterates or to set the bounds for an individual organism in a genus

INTEGRATION, IDENTITY AND STABILITY

93

such as Populus, with its extensive root-suckering. Grafting such a term as “complex organism” into the system of ecological nomenclature would be of no help. Rejection of the organismic view of communities or associations, however, in no wise demands rejection of the climax concept.

B.

OTHER C L E M E N T S I A N CONCEPTS A N D T H E I R MODIFICATION

I t is surely plain to all who have studied vegetation intensively that no one has found a way of describing it, and particularly the variation in vegetation, that has any assurance of being accepted universally or nearly so. I t cannot be forced into any of the “pigeon holes” designed for it, not even the continuum “pigeon hole”. Surely we must agree with Tansley (1949, p. vii, who, dealing with the modern theory of vegetation, writes: “Schematisation is always necessary when we are trying to bring observed facts togetherandarriveat a comprehensive view. But the conceptionswhich we form and the terms we employ or invent in the process should never be mistaken for facts of nature. They are simply creations of the human mind which assist in the understanding and correlation of the facts of nature. As such they are inevitably subject to differences of opinion, for different minds will always tend to prefer different criteria in constructing classifications.Ultimately the c h s i f i cations that do least violence to the facts will survive and the beds of Procrustes will be discarded.” (Our italics.)

In this same work Tansley sets forth the different concepts which different workers or groups of workers hold for the terms “formation” and “association” and Whittaker (1962, pp. 70-72) distinguishes six different concepts of the term “association”. Returning to the term “climax”, we encounter variation in this concept as well. Clements (1936) came to use it as an “exact synonym” of formation and when he carved the North American continent into twelve climaxes, excluding the tropical ones (Weaver and Clements, 1929, pp. 425-426), it was on the basis of potential vegetation, as revealed by a study of existing vegetation. Since he thought in terms of process, the slownessof various physiographic changes did not present an obstacle to his total concept of vegetation. For purposes of his classification, “. . . each climax consists not merely of the stable portions that represent its original mass but also of all successional areas, regardless of the kind or stage of development” (Weaver and Clements, 1929, p. 422). Clements saw a cause and effect relationship between climate and climax, with the climax in turn influencing climate. He felt the relationship was so intimate that “. . . the climax must be regarded as the final test of a climate rather than human

94

A. N. LANOFORD AND M. F. BUELL

response or physical measurements”. Clements was fully aware of the considerable variability within his climaxes and of the ecotonal gradations at their boundaries and, notably, of the oscillation of climax boundaries in response to long-term and even relatively short-term oscillations in the controlling climates. These same considerations are equally applicable to the climax associations into which nearly all of his climax formations were divided (see particularly Clements, 1928, pp. 109-110).

Clements recognized very clearly that, within a climax formation, either natural or artificial factors might hold vegetation indefinitely at a stage which was successionally below the ideal regional climax. His preoccupation with the successional process and with climate as the paramount and ultimate factor controlling vegetation, however, seems to have prevented him from using the expression climax for such areas of vegetation. On two outstanding scores, then, the concepts of Clements have proven widely unacceptable: the rigid connection he made between climate and climax and his organismic view of the plant association. One must acknowledge, however, the prodigious contribution he made towards an understanding of vegetation and particularly of the vegetation of North America. Braun’s (1950) masterly treatment of the deciduous forest formation was based on much more intimate knowledge of the smaller area in question. Recognizing concrete associations and associations in the abstract, it stands as a logical refinement of the approach of Clements but one which will doubtless be refined further as knowledge is extended. Unlike Clements, Tansley (1949) was less bound by questions of climate and of process, though appreciative of the dynamic view of vegetation as set forth by Clements and by the very great influence of climate. A climax (formation), in the hands of Tansley, “. . . represents a well-marked position of rehtiwe vegetational stability, which may persist indehitely in equilibrium with relatively stable environmental conditions”. Tansley considered a complex of climatic factors as the stabilizing condition for deciduous summer forest in Britain, a stable water-level at a certain height above the soil for a reedswamp climax. Tansley even considered pastured grassland as a sort of climax, maintained through the continuing influence of man and domesticated animals. His formations (characterized by a difference of dominant life forms) and his associations (characterized by a difference of species) are not necessarily controlled preponderantly by climatic factors but, in addition, “. . . there are edaphic or biotic factors, not depending or only partly and indirectly depending on climate, permanently at work to stabilize the community”. We wish to consider, then, the nature of the climax plant association,

95

INTEGRATION, IDENTITY AND STABILITY

in either or both of the senses of Clements and Tansley. Both of these imply a considerable degree of stability and permanence of climax associations, and reasonably specific floristic composition. We would insist that the physiographic processes of erosion should have proceeded far enough to provide well-developed soil of a depth sufficient to support the climax association, and we would see no reason to argue that such extreme situations as flat wet peatlands in southern Quebec or northern Michigan, for example, should support a hemlock-northern hardwoods association, even though this be considered the climax association of the area.

111. THE INDIVIDUALISTIC CONCEPTO F T H E ASSOCIATION, T H E CONTINUUMA N D ORDINATION A. T H E L I N E A R C O N T I N U U M A S A Q U A N T I T A T I V E S U B S T A N T I A T I O N O F CLEMENTS’ CONCEPTS O F SUCCESSION

Whittaker (1962) and McIntosh (1967) have documented the development of the individualistic concept of the association, both making it clear that Ramensky and Gleason independently brought the concept into the active forum of ecological debate. I n reading and re-reading the writings of Clements and Gleason, one gains the impression of the development of two “camps77,each expressing views more extreme than would be expected in the absence of their mutual opposition. Gleason’s (1917) first statement of the individualistic nature of the association followed hard upon Clements’ enunciation of his organismic view of the association; the polarization of views was established and later intensified. Clements’ organismic view of the association is extreme and has been rejected widely: Gleason, in a personal communication in 1948 to one of us, expressed the opinion, in the light of the resurgence of interest in biochemical interactions among the higher plants (Went, 1942; Gray and Bonner, 1948), that he may have pushed the individualistic concept too far. Gleason (1926) set his concept of the plant association in opposition to “. . . the usual concept. . .”,certainly held by Clements, that it is “. . an area of vegetation in which spatial extent, describable structure, and distinctness from other areas are the essential features . , .,,, Gleason wrote of the association that “. . . the fundamental idea is neither extent, unit character, permanence, nor definiteness of structure. It is rather the visible expression, through the juxtaposition of individuals, of the same or different species and either with or without mutual influence, of the result of causes in continuous operation. . . . The effect o f . . . primary causes is therefore not to produce large areas of similar

.

96

A. N . LANGFORD AND M. F. BUELL

vegetation, but to determine the plant life on every minimum area.” I n 1939 he described the vegetation unit as “. . . a temporary and fluctuating phenomenon, dependent, in its origin, its structure, and its disappearance, on the selective action of the environment and on the nature of the surrounding vegetation. Under this view, the association has no similarity to an organism and is scarcely comparable to a species.” The original vegetational continuum of Curtis and McIntosh (1951) was set forth as a quantitative substantiation of Gleason’s hypothesis of the individualistic nature of the association. Drawing attention again to the fact that the association of Clements was based on potential, on the consideration of stands of vegetation that had had ample time to develop to a mature status, we consider that the findings of Curtis and McIntosh (1951) and of Brown and Curtis (1952) give, as explained in the introduction, quantitative substantiation of the views of Clements regarding variation within the sera1 communities of an association. They do not shed effective light on the question of the objective reality of mature plant associations. After drawing the conclusion that the upland hardwoods of Wisconsin constitute a continuum, Curtis and McIntosh stated (p. 492), “This conclusion would appear to substantiate the individualistic association hypothesis of Gleason (1926) and its emendation by Cain (1947)”. Brown and Curtis (1952), referring to Gleason, stated, “The idea of a vegetational continuum as opposed to a series of discrete plant associations, associes or communites is not new”. Viewing these two statements, we stand at the crossroads of the confusion. The demonstration of a continuum of concrete communities, chosen from one association in the sense of Clements, has been transformed into a demonstration of the fallacy of the climax association concept, with Gleason’s views of the association transferred to the level of the stand.

B.

A CRITICISM O F T H E L I N E A R CONTINUUM

Like Clementsian ecology, continuum analysis has resulted in some extreme views. Comparing continuum indices with angstrom units for precision of statement, Brown and Curtis (1952) stated that, “Recognition of the fact that there is a gradient in forest composition correlated with an observable cline in habitat factors permits the designation of a particular stand or series of stands with any degree of precision requisite to the study”. Buell et al. (1966), studying upland forest stands in northern New Jersey, testing continuum methods faithfully, compared 52 pairs of stands, each member of a pair differing from the other by less than one continuum index unit, where the full scale ran from 10 to 100

INTEGRATION, IDENTITY AND STABILITY

97

units. Coefficients of vegetative difference, based on tree species, ranged from 11 to 97, with an average of 56, indicating very clearly the inadequacy of continuum index numbers to designate the nature of a stand. Bray and Curtis (1957) had recognized this sort of diversity years earlier and changed the direction of continuum analysis from the unidimensional approach to the pluridimensional approach or ordination. Vegetation within any association, selzsu Clements, disturbed as it is today in one way or another almost universally, generally exists in the form of a pluridimensional continuum, though there may be some situations so dominated by graded expressions of a single factor as to approach a unidimensional continuum. Continuum analysis gives quantitative expression to qualitative differences that may be expected on the basis of the claims of Clements. Two brief criticisms of the numerical calculations must be made, however. First, whenever, particularly as in early continuum analysis, a single figure is to be used to place a sample of vegetation in an appropriate position, the stand of vegetation sampled must show a high degree of homogeneity. We do not claim that heterogeneous vegetation should not be studied; we simply claim that the method of determining a single numerical expression, e.g. a continuum index number, is unsuitable if there is considerable variation within the units of study. The more variation there is in such units the more certain it is that a series of grading figures will be produced. Second, whereas the toleration of heterogeneity contributes to the continuity of an array of figures characterizing vegetation, the use of composite indices, such as Importance Values, tends to obscure differences between plant communities. Our students have taken the data from several of the stands used in our 1966 New Jersey study (Buell et al., 1966), changing the relative dominance and relative density figures considerably, without changing the composite measures (also relative): in some cases the total basal area per acre has been raised SO-SO%. Working back from relative figures to precise figures for individual trees, they have produced artificial populations quite different from the natural populations, yet giving exactly the same Importance Values. The use of composite measures for community comparisons has been discussed by Grieg-Smith (1964, p. 142) and Lambert and Dale (1964, p. 68). Grieg-Smith cautioned against the uncritical use of composite measures while Lambert and Dale dislike them on theoretical grounds. (Importance Values still appear in the literature when inter-stand comparisons are at issue, for example in the 1966 work of West.) Bray and Curtis (1957), introducing their ordination technique, used 39 individual measures, pertaining to 26 species, for their extensive calculations of inter-stand differences. Basal area of tree species and density of tree species were not combined; thus the tests were more discriminating than E

A. N . LANOFORD AND Y. F. BUELL

98

would have been the case with Importance Values. We conclude that whenever one seeks to reveal inter-community differences it is best to use single rather than composite measures. This is particularly so when such composite measures for an important species in two communities are nearly equal, but the result of unequal individual measures. For example high relative density and low relative basal area in stand a and low relative density and high relative basal area in stand b could readily indicate equal importance of a single species in two unlike communities. If’, on the other hand, two stands being compared are highly distinctive, calculations of coefficient of vegetative difference (Cantlon, 1953) from individual measures are likely to be virtually identical with those from summed measures. Table I illustrates these two situations. TABLEI Measurea from arti$cial populations selected to show the possible concealment of &&wficant interstand differences through the use of compo&te measures. The relative masures, “D” and “B” and “ D f B ” , are for three species in stands a and b, with identical composite measurea, and stand c, whose composite meaaures differ greatly from those of both a and b. Species

No. 1

2

3

Measures for stand(s)

a

D +B D B

60

D+B D B

30

D+B D B

10

b

a-b

60

30 30

0

20 30

10 8

2

Sums of differences based on:

c. R E C E N T

5 5

35 15 10

70

25 5 10

0

composite measures single measures

Coefficient of vegetative difference

10 10

3 7

25 30 30

30

0

15 15

a-c

C

60

10 10

40

25 5

a

15 20 40

30

5

40

35

5

5

8

1

2

4

7 2

_ _ _ _ _ _ _ _ _ _ _ - - - - 80 ---

0

50

__________________

0 25

84

40 42

R E A S S E S S M E N T S OF T H E C O N T R O V E R S Y

We have referred to Whittaker’s (1962) assessment of the great contribution which Clementsian concepts have made to the development of

INTEGRATION, IDENTITY AND STABILITY

99

ecological theory. Though we feel that continuum and ordination analysis, both emanating largely from the Wisconsin school of ecologists led by Curtis, have not disposed of the question of the nature of the plant association, the fruits of the Wisconsin studies in ecology, like those Wisconsin studies in plant pathology many years ago (Jones et d.,1926), have been rich indeed. Articles relating to “The continuum concept of vegetation”, pro, con and neutral, have appeared in great numbers, as documented thoroughly by McIntosh’s (1967) excellent review. His assessment of the current state of the continuum problem is most interesting. It gently sets objective classifications and ordinations close together, agrees that they may be complementary rather than mutually exclusive, calls for further clarification of the “community-type hypothesis and the continuum hypothesis” and repeats the 1959 injunction of Curtis that the task of phytosociologistsis to find out how combinations of plants have come into being, “ ‘. . .how they maintain themselves and to relate them to their physical environment and to reach an understanding of the material and energy changes which occur within them”’. The most surprising feature of McIntosh’s article (1967), however, is the complete absence of any reference to Clements or to the plant association in the sense of Clements. The references to Gleason are the closest approach to Clements available. As one hunts for Clements at the appropriate point (p. 133) it comes as a shock to see Gleason’s 1926 and 1939 articles titled “The individualistic hypothesis of vegetation”, though they are correctly given in the “Literature Cited” as “The individualistic concept of the plant association”. This is the confusion mentioned above. Vegetational continua are found in nature, continuum analysis and ordination techniques have been very effective in the presentation of quantitative data measuring the variation in related communities or stands of vegetation. But, as has been pointed out in various quarters, e.g. by Lambert and Dale (1964, p. 76), the stands studied have, by and large, been members of some subjectively chosen plant association, from the upland forest of the prairie-forest border region of Wisconsin (Curtis and McIntosh, 1951) to the montane forest vegetation of the Oregon Cascades (West, 1966). We are forced to the conclusion that continuum analysis and ordination, useful though they may be in the attack, have not done much to resolve the problem as to which of (a) the individualistic concept of the association or ( b ) the concept of discrete associations, bordered by ecotones, gives the most reasonable interpretation of the nature of mature or climax vegetation. Even Curtis’ (1959) comparisons among the 28 arbitrarily delimited communities of Wisconsin (p. 486 ff.) fail to resolve the problem. McIntosh (1967, p. 168) stated, “It should be noted that continuity is not restricted to sera1 communities, as is explicitly asserted by Curtis

100

A. N. LANOFORD AND M. F. BUELL

(1955,1959) and Whittaker (1956)”. This is tantamount to declaring that continuity exists within and between climax associations. I n our opinion, however, this problem of continuity cannot be resolved by comparing stands or communities that have not attained a climax condition. The choice of areas of vegetation to be analysed quantitatively is commonly a very subjective one and lack of knowledge of the details of such choices complicates the problem of judging various synecological studies, and perhaps particularly those that seek to shed light on the nature of plant associations. After many years of investigation of this problem, the area of uncertainty in the interpretation of results is still great. Continuum supporters might feel that the residual 23 stands of Daubenmire’s 1966 study were too few in number and not fully representative of the gradient of habitat factors across his 153 mile long belt in the eastern part of the state of Washington. On such grounds they might not accept his study as giving evidence of the existence of discrete associations. Daubenmire presented quantitative data for the 34 species that attained, even in a single stand, a cover value of at least 5 yo. He concluded that four steppe zones were clearly recognizable, representing “. . . ecosystem types with consistent environmental differences, furnishing the basis for mapping mutually exclusive bioclimatic areas, and allowing one to relate climate to vegetation structure in rather precise terms”. Daubenmire stated that in these stands “. . . only 3 per cent of the species show changes in dominance that resemble the swarms of independently staggered, bell-shaped curves that have been offered in support of a vegetation continuum”. It is with reference to the forests just east of these steppe stands, however, that Daubenmire issued his strongest challenge to continuum workers, insisting that they must assess more than “species distribution and relative abundance” (we must note that relative basal area or some other measure of dominance has frequently been used by continuum workers) and “come to grips with matters of more fundamental biologic importance, especially population structure and dynamics”. He presented data on population structure, showing that the species composition of various stands was in a process of change and that “In nearly all cases, population structure in homogeneous stands . . .” of forests in his study area “. . . shows that one tree species is clearly superior to all others (with continued change pointing to increasing dominance by that species), with the superiority shifting from one species to another along the climatic gradient”. He theq showed how his own data could indicate the existence of a continuum if the dynamics of his stands were overlooked. He treated his data in continuum fashion, ignored individuals with dbh less than 10 cm, calculated Importance Values from relative density and relative basal area. A plot of the figures so obtained is wholly in harmony

INTEGRATION, IDENTITY AND STABILITY

101

with a corresponding plot of the major species found in the original linear continuum of Curtis and McIntosh (1951). When one reflects upon Daubenmire’s statement “. . . that even where undisturbed vegetation is sampled, methods of analysis or of subsequent data manipulation can completely determine the nature of the conclusions reached”, it would seem highly desirable that one or two strong proponents of the individualistic concept of the association and one or two strong proponents of the vegetation-unit concept should meet, agree on a suitablestudyarea, suitable methods and suitable treatment of data and then conduct the project together. Unfortunately, this is unlikely to happen.

L T O COMMUNITYA N D IV. N E U T R A APPROACHES ASSOCIATION STUDY Each of the papers of McIntosh (1967) and Lambert and Dale (1964) includes a section on “Ordination and Classification”. These topics, in relation to vegetation, have been set in mutual opposition for years as have the terms “integrated community (or association)” and “individualistic community (or association)”. Ponyatovskaya (1961) considered that an absolute contrast between them waO not necessary; Goodall (1963) stated that these pairs of theories have tended to be confounded; Lambert and Dale (1964) have claimed that ordination and classification are equally precise as methods and that there is no reason for considering them mutually exclusive (p. 73). McIntosh (1967), referring to this claim, stated that both methods “. . .are in such a state of flux that it is difficult to make effective comparison”. This would seem to be the point for mathematical ecologists or ecologically-inclined mathematicians unprejudiced in one direction or another, to set forth criteria and procedures to bring us all closer to an appreciation of the elusive truth. Lambert and Dale (1964) discussed two ordination techniques, “principal component analysis” and “factor analysis” as providing the most fundamental approaches to ordination so far available. They favor factor analysis, for comparing units of vegetation that have considerable similarity, because it is the axes revealed by the analysis which form the basis for the generation of hypotheses, but they found virtually no acceptable applications of these methods. The work of Dagnelie (1960) appears to be the most satisfactory treatment of the problem, from the viewpoint of Lambert and Dale. Dagnelie, it is interesting to note, has applied a factorial analysis to the published data of Bray and Curtis (1957). His first extracted factor (p. 172) expresses degrees of floristic

102

A. N . LANGFORD AND M. F. BUELL

similarity in the 59 stands. Extraction of the second factor led him to a classification of 58 of the stands in four groups, though he lacked stand detail to enable an ecological interpretation of his groupings. It must also be pointed out that Dagnelie’s graphic configurations of the 59 stands in 3-dimensionalspace do not demand but rather allow distribution into four groups. Other workers might deny the discreteness of the groups, especially since the 59 chosen represent a selection only from a greater number of possible stands which might well provide intermediate positions in 3-dimensional space. Some recent findings by P. J. Webber of York Univ., Canada, (unpub. mss) seem to justify citing his approach as a neutral one, particularly in the light of Daubenmire’s 1966 criticism of his work in southeastern Ontario. Webber’s manuscript, “An ordination of vegetation from Baffin Island, N.W.T.”, was presented at the 1967 Ottawa meetings of the Can. Bot. Ass. and dealt with his findings as the first biologist to visit the extreme environment near the northwestern margin of the Barnes Ice Cap. He sampled 82 acceptably homogeneous stands of vegetation, where completely closed vegetation was limited to moist sites with fine materials as substrate. Webber saw no conflict between the individualistic and the association-unit concepts of vegetation but chose to apply ordination techniques. Using essentially the method of Bray and Curtis (1957) but rejecting any “. . . rare or rudimentary stand that has no relationship with any other stand . . .” and is thus useless as a reference point, he ordinated one objectively chosen large group of 42 stands. His three ordination axes were most strongly correlated with water availability (first axis), grain size of soil (second) and snow cover (third). Although Webber accepted the suggestion of various workers that reduced competition in barren Arctic situations reduces the number of clearly defined communities, he had made qualitative observations of preferred combinations of species among his stands. His objective analysis showed five moderately distinct clusters of stands (groups of 4 , 4 , 5 , 1 4and 15), these much more clearly isolated from each other than those resulting from Dagnelie’s (1960) re-analysis of the data of Bray and Curtis (1957). On the classification side of the ledger, Lambert and Dale (1964) argued for the superiority of primary analysis, which has the aim of extracting maximum information from the raw data (as opposed to “discriminant analysis”, which allots units to existing classes) and for hierarchial classifications that result from subdivisive analysis. Association analysis, which includes their preferences, has been developed extensively by Williams and Lambert ( 1959), applied to simple heathland communities, found useful as an aid in ecological interpretation, and then programmed for a digital computer. This allowed the applica-

INTEGRATION, IDENTITY AND STABILITY

103

tion of the method to more complex communities (Williams and Lambert, 1960), substantiating their opinion that these more complex communities would yield to the analysis. Possibly most important of all, the analysis directed attention to previously unrecognized ecological factors contributing to the diversity of vegetation observed. Grieg-Smith (1964) has reviewed in detail the various ordination and objective classification techniques that have been developed recently, discussing the limits of their applicability, e.g. the unsuitability of association-analysis for the comparison of samples of widely divergent floristic composition. He rated the association-analysis of Williams and Lambert as ". . . essentially an approximation to factor analysis based on presence and absence of species". Gittins (1965), as a student of Grieg-Smith, went to the laboratory of Williams and Lambert and applied both the ordination technique of Bray and Curtis (1957) and the association-analysis of Williams and Lambert (1959, 1960) to extensive quadrat data from a limestone grassland community in Anglesey, Wales. Gittins concluded that essentially identical ecological conclusions resulted from the interpretations of the two analyses. None the less, he expressed his preference for ordination technique as giving ". . . a more informative and ecologically more satisfying model of vegetation structure than normal association-analysis", but with the requirement of more elaborate data. Gittins discussed the minor advantages and disadvantages of each method and the possibility, in some instances, of combining the two methods to yield maximum. information. It is plain that valid ecological conclusions are the desired output from the continuing research in biotic communities. It is plain, too, that a far greater mathematical sophistication than has characterized most students of these communities in the past is essential for the future, particularly if such things as the present virtual restriction of association-analysis to qualitative data is to be removed. It appears, also, that virtually all the methods devised for the comparison of vegetation from place to place are best suited for inter-stand comparisons or for assessing variability within restricted contiguous areas (e.g. Williams and Lambert, 1959). Quite possibly the climax associations of the recent past have lost most of their relevance in the practical world except in the eyes of those who cherish their continued existence, at least in small patches, just as they cherish the continued existence of the Whooping Crane and the Mississippi Kite (as interesting products of evolution), and in the eyes of those who recognize the potentialities of applying elsewhere the undermature associastanding gained from a study of tions.

104

A. N. LANGFORD AND M. F. BUELL

v. A MODERN V I E W A.

O F THE ASSOCIATION

TANSLEY’S BROADENING OF THE CLIMAX CONCEPT

Widespread concrete climax associations in the sense of Clements are mainly of theoretical and historical interest today wherever the influence of man has been strong. This is particularly so in relation to the geographical areas of study that have received the major attention of plant geographers and ecologists. It is none the less still of interest, fifty years later, to consider briefly the reasonableness and unreasonableness of some of the views of Clements, modifying them if necessary. The concept that shines through with greatest strength to this day is that of great stretches of virgin country dominated by one to several species of like growth form wherever the processes of succession have had time to reach a more or less permanent end point. Within these areas were successional situations, ponds filling, rock outcrops undergoing the slow processes of erosion, high hills gradually being reduced and other similar situations, e.g. sand dunes undergoing stabilization or vice versa. The full expression of the climax association might be expected only in upland, reasonably well-drained sites that have had time to develop a good soil cover. These sites could be considered mesophytic, with respect to the range of conditions found within any association area. We must thus distinguish between the concrete, mature climax association and the area in which it was deemed capable of developing. The term “association-area” seems appropriate for this latter area. Although Clements was very clear as to his concept of the climax of an area as “. . . the highest type of vegetation possible under its particular climate . . .” (Weaver and Clements, 1929, p. 421), he also used the term in the sense of “climax area” (our term), “. . . each climax consists not merely of the stable portions that represent its original mass but also of all successional areas, regardless of the kind or stage of development”. We view his “formation-areas” as divided into “association-areas”. Similarly, we view his concrete examples of climax formations (e.g. those sections of the deciduous forest of North America that have reached the climax condition) as divided into concrete examples of climax associations (e.g. beech-maple and oak-chestnut forests). At the boundaries of the associations and formations Clements recognized ecotones, of relatively narrow extent in relation to that of the “association-areas” or “formation-areas”. As his terminology was tied to a monoclimax hypothesis he could not use the terms “climax” or “association” with respect to edaphic situations which otherwise really fulfilled his own criteria of climax. This presented, as explained above, no particular difficulty for Tansley (1949), who used the term climax for a well-marked position of relative vegetational stability. Rejecting the

INTEGRATION, IDENTITY AND STABILITY

105

organismic view of the association and setting aside the monoclimax hypothesis in favor of the views of Tansley regarding associations that are stable for many years but not necessarily for millennia, what is or what was the status of an association as circumscribed above? At the outset we must state that the views of the association held by Clements may be modified and refhed as judgment is made, just as continuum analysis has been modified and refined. Thus any shortcomings of an unidimensional continuum do not constitute grounds for objection to modern sophisticated ordination techniques. We are investigating, then, the validity of the concept of the plant association as a recognizable unit covering a considerable area, many miles in extent, as having a definite floristic composition (but not anything close to absolute uniformity) and as being distinct from adjacent associations. Our concept leaves room for variability and recognizes gradual change in any association; it stresses integrity, relative stability, important interrelationships among constituent species. I n considering opposing viewpoints of the association the bare quotation by Nichols (1929) of Gleason’s question (1926, p. 16) as to the justification for consideringan association as “merely a coincidence” does not do justice to Gleason. On page 26 of the same article Gleason elaborated upon the nature of this coincidence when he wrote that “Plant associations . . . depend solely upon the coincidence of environmental selection and migration over an area of recognizable extent and usually for a time of considerable duration”. We shall, however, set our view opposite that indicated by Gleason’s 1939 statement that, “The vegetation unit is a temporary and fluctuating phenomenon, dependent, in its origin, its structure, and its disappearance, on the selective action of the environment and on the nature of the surrounding vegetation” and opposite that which suggests that a continuum characterizes whole “associations” and the ecotones between them. This last viewpoint is supported by the work of Maycock and Curtis (1960), for example, who studied “boreal conifer-hardwood forests” of the Great Lakes region and considered that, “They can best be considered as a portion of a vegetational gradient representing a part of a vegetational complex which in the southern areas of the Great Lakes region is composed entirely of broadleaf tree species and in the areas northward becomes predominantly needle-leaved in character”, and, again, that they “. . . . are considered to form a vegetational continuum and to be inseparably related to all neighbouring vegetakional types”.

B.

T H E INFLUENCE OF DOMINANTS

If vegetation were simply the resultant of the availability of propagules and the many factors of the abiotic environment, usefully

106

A. N. LANOFORD AND M. F. BUELL

diagrammed, together with biotic factors, by Billings (1952) so as to show the manifold interrelationships among them, we might indeed expect “associations” to be as characterized by Gleason. However, it is commonly found in nature that one or a few species of plants can grow very successfully over a considerable range of environmental conditions and occupy a dominant position in the climax vegetation. For example, Acer saccharurn is such a species in the deciduous forest formation of North America; Stipa comata and Bouteloua gracilis are dominant throughout a very great extent of climax grassland, and Fagus sylvatica throughout most of the south-eastern section of Britain, especially on chalk soils (Tansley, 1949). It is also widely recognized that plants themselves constitute a very important part of the environment of plants, except in the earliest stages of priseres and, as Gleason himself stated (1939), “. . . their persistence always tends to reduce the effect of a variation in the physical environment”. This is a central problem; how extensive are the effects of the dominant elements of the vegetation in smoothing out environmental variations so that, within an area, their unifying control is greater than the residual divisive control of varied abiotic environmental factors? Here we use the term dominant in the sense of Weaver and elements (1929, p. 42l), who pointed out, particularly with reference to the prairie, that the real dominants, controllers of the situation, were not necessarily the most obvious. Whittaker (1962, p. 101) has noted the rise of the idea of the joint evolution of species, from Du Rietz, who proposed the idea of combinations of species that have become selectively fixed, to Mason, who wrote of most species as free to change their associational relationships with other species and to Dice (1952, pp. 461-462) who considered the association “. . . a very important unit of ecologic evolution’’with all its member species “. . . adjusted more or less perfectly to one another and . . . able to exist in the same community”. He considered the fluctuations in composition “. . . a normal part of the process of maintenance of community equilibrium”. With Dice, we are not far away from the modern terminology of homeostasis and “positive feed back” as used by Goodall (1963) in a stronger statement in support of his concept of “the joint evolution of species”. We may quote Goodall:

“. . .

it seems reasonable to suppose that, in general, species are more likely to become adapted to the commoner types of site. If a number of species tend constantly to grow together, the conditions at the various sites where this happens will tend to become, under their mutual influence, uniform, and this particular set of conditions will become commoner than others deviating somewhat from it. Thus the creation of an integrated community is a process which is likely to increase the pressure on other species to become adapted to it; it is a self-intensifying,self-acceleratingprocess. In this sense, the plant commiinity may sometimes be said with justice to have evolved as a whole.”

. ..

INTEGRATION, IDENTITY AND STABILITY

c. T H E

107

INTEGRATED ASSOCIATION

This is the sort of view of the association which we have been developing since 1959 when we started to relate our New Jersey studies (Buell et ol., 1966) to modern and not so modern concepts of vegetation. We believe that the balance of the evidence favors the integrated view of the climax association. Others, for example Ehrlich and Holm (1963, p. 86), using the terminology of geneticists, support strongly the views of Gleason (1939), though it is not apparent that they are dealing with climax associations in the sense of Clements. We agree that successional continua are widespread. Baker (1966), supporting the integrated view of the “community” or an organized view of the ecosystem, deals with Clements, Gleason and the continuum and shows the inadequacy of Gleason’s (1917) rather extreme statement, “Phenomena of vegetation depend completely upon the phenomena of the individual”. Baker rated the demonstration of a significant measure of homeostasis within a community as unchallengeable evidence of “organization” and gave evidence of its existence. Reviewing the century since Darwin, he stated, “Characters, individuals, and populations have followed each other as the units upon which natural selection is deemed to act. Now the stage is set for the next step in synthetic evolutionism, the study of the evolution of biotic communities, even of ecosystems.” We embrace the view of homeostatic plant associations of wide extent. Our concept of the association, however, it must be reiterated, is based on potential (see p. 104). Baker expressed the probability that the closeness of organization decreases continuously in the progression: cell, organ, individual, population, biotic community or ecosystem and that chance plays a greater role at the ecosystem end of the progression. D.

HOMEOSTASIS I N T H E P L A N T ASSOCIATION

We now turn to a more detailed consideration of homeostasis as an essential characteristic of the association concept. Although we do not wish to equate the climax association with an organism or with a species, we believe there are some further analogies between the association and the species that may be drawn. Our knowledge of the nature of species, and particularly of genetic variability within them, has grown considerably since the exchange of views by Gleason (1926) and Nichols (1929) as to the nature of the association. With the coming of hybrid corn, ever closer scrutiny was made of the heterozygous condition. The case of sickle cell anemia in man, with the superiority of the heterozygote over both homozygotes in the presence of

108

A. N . LANGFORD AND M. F. BUELL

tertian malaria, is so well documented now as to be afrequently repeated classic, with details in almost any modern textbook of genetics (e.g. Sinnott et al., 1958; Herskowitz, 1965). Such balanced heterosis is believed to be widespread and Crow, according to Sinnott et al., has argued that it may be responsible for about 95% of the improved yields in hybrid corn. (See also Crow, 1952.) Such balances need not be restricted to single allele pairs but may extend to groups of genes which are kept virtually intact so that we may have as possibilities an inversion heterzygote and two types of homozygotes for any chromosome section involved. Laboratory tests have demonstrated the selective advantage of specific inversion heterozygotes in Drosophila pseudoobscura under specific laboratory conditions. From our point of view the important point to recognize is that adaptable species often have a high degree of built-in genetic variability and it may be concluded that these are best able to respond to the vicissitudes of changing environmental conditions. Dobzhansky and his associates (seeSinnott et al., 1958 or, for more specificreferences to the general topic, Dobzhansky, 1956 and 1962) have shown the very considerable variability in the frequency of various identifiable chromosomes in Drosophila pseudoobsoura in a single California locality during a March to October season, together with much greater frequency differences in races collected from California to Texas. I n Drosophila persirnilis Dobzhansky ( 1956) has also shown significant changes in chromosome composition over a period of years and made the still unproven but reasonable suggestion that the observed changes may have been largely the result of climatic fluctuations. In no case did this variation prevent recognition of the unit with which he was working, a given species of Drosophila. We do see,however, the element of stabilityor homeostasis made possible by this genetic variability. We may visualize such a species, with its short life-cycle, as constantly changing in response to changing conditions, fluctuating in response to fluctuating conditions, yet retaining its essential identity as a describable unit, though still subject to the long-term processes of speciation. In the climax plant association the internal variability is at a different level. The dominants of climax communities are probably always perennials, often long-lived and with such a range of physiologic tolerance that the variations in environmental conditions will seldom be great enough to remove a particular genetic combination from the association except, perhaps, occasionally, at its edge. We may, however, think of plant associations as responding verymuch in the same way as a population of Drosophih with flexible polymorphism, though at a much slower pace. I n the plant association we may consider that much of the variability in capacity to respond lies in the differences among groups of species

INTEGRATION, IDENTITY AND STABILITY

109

whose requirements are similar but not with exactly the same optima. In considerable stretches of the deciduous forest of North America, for example, though Acer saccharum and Fagus grandifolia may, ecologically, be the most important trees of the mature forest, fluctuating environmental conditions may now favor one, again the other, and a t times favor Tilia americana or Betula lutea without changing the fundamental nature of the forest greatly. Successionalstudies from a very wide variety of habitats indicate, however, that, given time, Acer saccharurn would achieve the number one position over a very wide area of the deciduous forest as mapped by Weaver and Clements (1929). A t the western edge of the deciduous forest association, for example, in what we can agree is an ecotonal region, Buell and Cantlon (1951), working in Minnesota, found well-developed wooded areas dominated by Acer saccharum. Far to the east, in northern Cape Breton Island, Nova Scotia, Greenidge (1961) was particularly impressed by the abruptness of the “line” marking the limit of sugar maple and by the fact that there was “. . . no gradual transition in size toward a depauperate form or a marked decrease in vigour upon approaching the limit of the range of the species”. Sugar maple was often the species of highest density and greatest basal area in Greenidge’s stands. Some specimens exceeded 100 ft in height and attained 35 in. dbh. We have already made reference to the evidence of Dix (1957) that sugar maple would increase in importance with lack of disturbance and the passage of time in the vicinity of Washington, D.C. From this relatively southern position, moving to the west again, we have some figures kindly provided by Dr F. Glenn Goff of the School of Forestry, University of Missouri. These figures, for both trees and saplings, indicate that there, too, the shift in vegetational composition of some Quercus-dominated stands is away from oak end towards increasing significance of sugar maple. In the lower strata of the deciduous forest, as well as in the canopy layer, we may expect similar variation in composition, favored by environmental fluctuations, with groups of near homologous herbs sharing the space on the floor of the forest. The climatic conditions may now favor one, now another species but with the whole remaining remarkably stable, a varied yet steady state. The stability of the entire unit so conceived must, of course, be dependent upon the ability of the dominant or co-dominants to exert both a long-term and a short-term levelling of the degree of environmental (non-seasonal)fluctuation which would exist in the absence of the dominant vegetation. In an area where the abiotic factors are particularly severe, e.g. in the tundra (Muller, 1952), competition may be absent and biotic factors controlling the nature of the vegetation of practically no significance. I n such a case the dominant vegetation may be unable to exercise any

110

A. N. LANGFORD AND M. F. BUELL

homogenizing or unifying influence. The relationship between abiotic factors and plant genotypes alone will determine the vegetation. Gleason’s discussion (1939) of the tremendous variation in the development of desert annuals in the Mohave desert affords an excellent illustration of this situation. I n those extensive areas in which plant succession is an important phenomenon, we might hope to assess the homogenizing power of the dominants. However, quantitative records sufficient for this purpose are unfortunately lacking since the natural climax associations have been disturbed so widely. Even where we set aside, for study, areas that are in a condition as near to the climax as can be found we can no longer be sure that all species appropriate to a given climax will even have the opportunity to reach these areas. Where human population .density is high today or where man’s influence on the land is extensive, the climax association may, by and large, be considered a thing of the past, though it may still be studied in the hinterlands of the world. We can, however, accept varioushistorical records as to the nature of vegetation long ago and these do indicate great sweeps of country with relatively uniform vegetation. Tansley (1949), for example, speaks of the natural climax of England, on relatively favorable soils and in the presence of relatively favorable conditions of life, as deciduous summer forest for several millennia in the past. It is of passing interest that Roe (1955), a historian, using different source material, also reached the conclusion that England was almost completely forested in mediaeval times. He does not deal particularly with the problem of species composition in the forest but such incidental references to species as occur are to oak. Though the forest has been disturbed for centuries, Tansley believed that if man and his creatures were to leave the country, beech would become dominant over most of the chalk and perhaps over some other southeastern soils while oak would again come to dominate the rest of the area in question. We hold no brief for the degree of precision which Clements gave for his units of vegetation, as already mentioned in connection with Braun’s (1950) more detailed studies of the deciduous forest of North America, but rather for his association concept itself. Dice (1952, p. 462), writing with reference to stands, communities and associations, all within a single paragraph, characterizes the fluctuations in population density of member species as a part of the normal process of maintenance of community equilibrium. Braun (1950, p. 6) gave estimates of the tremendous variation, throughout the deciduous forest formation, in the time that the land has been available for plant growth. Rowe (1967), using an estimate of approximately 10 000 years since the last glaciation in Canada, speculated on the migration of forest trees to the north and was convinced that even without climatic change another 10 000 years would

INTEGRATION, IDENTITY AND STABILITY

111

see significant changes in the phytogeographic zonation of the country, where the flora may be characterized as relatively young. Wemay agree, then, that there will be continuing gradual shifts in the composition of climax associations but that our associations still have the relative stability demanded by Tansley (1949). As further stabilizing influences in a plant association we visualize positive associations, such as mycorrhizal relationships and synergisms, whether with macro-organisms or micro-organisms and negative “associationsy’such as antibiosis or allelopathy. These relationships will be treated in a later section. They may, of course, be applied at the community level as well as at the association level. All these relationships, however, contribute to the view of the association as an organized unit. Odum (1963), in a short treatise “Ecology”, did not deal with the term “association”, but he did deal with the question of the stability of climaxes, expressing theview that amature or climax community “ . . .is often able to buffer the physical environment to a greater extent than the young community. . . . Thus, the achievement of a measure of stability or homeostasis . . . may well be the primary purpose (that is, the survival value) of ecological succession when viewed from the evolutionary standpoint.”

E.

ECOTONES

Special reference must be made to the ecotone between two climax associations, particularly in the light of Whittaker’s (1967) gradient analysis, with its evidence (p. 229) that in many mountainside gradients graphic representations of the contribution of various species show a series of intersecting bell-shaped curves, in harmony with the continuum concept of vegetation but entirely divorced from it, physiographically. Whittaker’s study sites are not chosen from within a single association, in the sense of Clements, and are in linear groups running, for example, along a topographic moisture gradient from mesic to xeric. What is lacking, however, is a gradient analysis through an extensive climax association, across an ecotone and far into a second adjacent extensive climax association. We might expect rather smooth curves for the great majority of species within either association and, through the ecotone, a series of variously intersecting sigmoid curves. This would be, of course, entirely in harmony with the view of Clements (1928), just as is the demonstration of continua among successional communities. Clements wrote (p. 109): “The effect of climatic oscillations may be seen from year to year in the ecotone between two climatic associations. In short, the ecotone is largely a record of the effects of small variations of climate. If accumulated or allowed to act in one direction, the latter are sufficient

112

A. N. LANOFORD AND M. F. BUELL

to give the advantage to one of the contiguous associations.” Since we are dealing largely with perennials and not with the two-week cycle of Drosophilae, the record of fluctuations is long-lasting and reflected in the sigmoid curves that would be revealed by transects across the ecotone. Such data do not in any way lead us to the rejection of the association concept. Perhaps the closest approach to an ideal analysis, from the standpoint of our topic, is that of Scott and Holway (1967, and personal communication from Scott). They used a continuum treatment for a linear ordination of 115 stands chosen at 500 ft intervals between altitudes of 1000 f t and 4500 ft on Whiteface Mountain in New York State. Their plot of indices against altitude did not result in a straight line, as would be demanded by continuously changing vegetation. The form of the plot indicated to these workers a situation intermediate between those appropriate to a continuum and truly discontinuous vegetation. Their data gave evidence of a maple-beech-hardwoods “association” at 15002500 ft, a spruce-& “association” at 3000-4500 ft and an “ecotone” between. Scott realized that altitude is not a true measure of environment and has made plans to assess the total environmental gradients more critically in continuing studies. Further refinement of the concept of the plant association, in the sense of Clements, and of the numbers and boundaries of associations is highly desirable, using quantitative measures, and may possibly be accomplished, particularly in undisturbed regions of the world, but the major attention of ecologists will be directed, not to the concept of the plant association as we have defended it but to the study of existing aggregations of plants, some extensive, some of restricted extent; some relatively mature, some successional and even some in areas where succession scarcely seems to be a problem.

VI. THE QUESTIONO F C R I T I C A L LEVELSALONU GRADUALE N V I R O N M E N TGRADIENTS AL A.

INTRODUCTION

Proponents and opponents of the individualistic concept of the plant association are united in recognizing definite plant communities of measurable extent and in describing exceedingly sharp boundaries between various communities. Such sharp boundaries, found for example as one steps from a gravel moraine into the level expanse of a closed Sphagnum bog, afford no support for the concept of discrete, integrated associations. Following a discussion of boundaries Curtis (1959) wrote, “Usually these abrupt boundaries between dissimilar communities are

INTEGRATION, IDENTITY AND STABILITY

113

associated with equally abrupt changes in the habitat, mostly due to topographic features”. We may then turn to a consideration of discontinuities of vegetation or animal life along gradual environmental gradients, seeking thereby to shed light on the concept of discrete climax associations and on the concept of distinct units of lower rank. From the point of view of theory, reference to Hutchinson (1953) is appropriate. Hutchinson wrote that “The production of a discontinuous discrete type of biological zonation in a continuous gradient of salinity, soil moisture or other physical variable is easily understood in terms of competition theory, since the direction of competition will change at a definite point on the gradient, below which one species, above which another species, will be successful . . .”. Commenting upon the frequent discovery of wider salinity tolerances in the laboratory than in nature, Hutchinson suggested that “. . . when two species of slightly different tolerances compete in a salinity gradient, selection will cause the optima of values of the salinity of the two species to diverge”. We turn now to consider some gradient phenomena.

B. MYCORRHIZA Our ignorance of the significance of mycorrhizae in connection with the spread of tree species into new areas is perhaps best illustrated by the calculation of Rowe (1967) that spruce in the Keewatin District of the Northwest Territories of Canada, more than 1000 miles from the nearest refugium of the last glaciation, must have attained an average migrational speed of approximately one mile per ten years to reach this part of its range. It is difficult to conceive of mycorrhizal fungi, in company with spruce roots, extending northwards at the rate of 500 feet per year. None the less, at least under some circumstances, the presence or absence of mycorrhizae at a certain point on an environmental gradient may be the most important operative factor controlling the extension or non-extension of tree species from the edge of a forest association to, for example, a grassland. Dr S . A. Wilde (personal communication) believes there is sufficient evidence to claim that the absence of mycorrhizae-forming fungi in prairie soils sharply delineates the boundary of forest cover. He writes that at least in Wisconsin, where his studies have been concentrated, invasion of prairie by trees is usually confined to the narrow forest border, the soil of which is penetrated by root systems of trees carrying mycorrhizal fungi but that scattered trees are occasionally established from fungus-inoculated seed, planted by rodents or carried by a strong wind. Mikola (1953) placed seeds of Pinus banksiana and P. strobus in prairie soils taken at different distances from shelter belts. He found,

114

A. N . LANGFORD AND M. F. BUELL

four and five months later, that seedlings in soil collected more than 6.5 m west from plantation trees of Pinus sylvestris failed to become mycorrhizal. The evidence, then, is that the absence of mycorrhizal fungi in soils close to the trees of the forest-prairie boundary may be the outstanding single factor preventing the haphazard and irregular extension of tree species into the prairie, even when other factors, notably water supply, shift temporarily in such a way as to favor the extension of the forest. The presence or absence of mycorrhizal fungi, then, would seem to function as a homeostatic factor, giving added sharpness to the forest-prairie transition.

c. E D A P H I C A N D

CLIMATIC FACTORS

The Great Basin Desert (Jaeger, 1957) of south-western United States, centered on Nevada and Utah, would seem to present a good opportunity for examining vegetation changes along environmental gradients, including salinity gradients. Billings (1949), influenced by Clements and Gleason but not by Curtis, considered the basin sagebrush association of Weaver and Clements (1929) as readily divided into two zones on the basis of macroclimate, with each of the zones dotted with edaphically-modified communities. He designated the cooler and more moist zone as “intermountain sagebrush zone”, the warmer and drier zone as “shadscale zone” and addressed himself chiefly to the latter. Artemisia tridentata was the chief dominant of the sagebrush zone, Atriplex confertifolia the most characteristic species of the shadscale zone. Billings believed that the moisture factor was a critical determinant factor and explained the line of large sagebrush on the shoulders of an abandoned stretch of paved road in an otherwise typical shadscale zone as due to the additional supplies of water running off the pavement. Billings recognized considerable floristic and quantitative variation within the various shadscale areas studied and thus acknowledged the individualistic nature of each stand of shadscale vegetation. He considered the shadscale zone as a climatic phenomenon, expected on this basis a broad ecotone with the sagebrush zone, acknowledged that) the shadscale boundary was not precise but none the less recognized the shadscale desert as a vegetational unit. Recalling the situation, in 1968 (personal communication), Billings wrote, “I was impressed by my observations of sharp local boundaries and gradual regional changes”. Gates et al. (1956) carried out more intensive studies in the Great Basin Desert, in Utah, where they were impressed from the outset by the generally abrupt transitions from one vegetation type to another. They determined soil pH values; total soluble salts; base exchange capacity; total calcium, magnesium, sodium; soil moisture and a variety of addi-

INTEGRATION, IDENTITY AND STABILITY

115

tional soil features, at various depths, in areas dominated by Artemisia tridentata or one of four other species. Adjacent pure stands of all combinations of these five species, in twos, were found, with the transition often so sharp as to be completed over a distance of from one to three feet. Only occasionally were broad transition zones found. I n other cases mixtures were found. Gates et al. concentrated on the pure stands and sharp transitions. Although some significant differences in five of the many edaphic factors tested were found when soils occupied by the different species were compared, it was impossible to account for species distribution on this basis. “Overlap of each soil factor measured was found under all species studied. Within certain ranges for each edaphic factor, all five species appeared to be well adapted. Within this range it would be logical to find mixtures of the various species. This was not true.” Noting that Gates et al. had neglected any intensive investigation of physical soil factors, Mitchell et al. (1966) complemented their study by investigating the physical properties of soils associated with adjacent pure stands of Eurotia lanata and Atriplex confertifolia, in the same general area. They used sophisticated methods, including X-ray diffraction analysis of fine clays, but found “complete homogeneity of all properties examined”. Remembering that in these cases we are dealing with community or stand boundaries and not with Clementsian association boundaries, it is established that very sharp biotic boundaries may exist in situations where there are no comparable non-biotic boundaries. Gates et al. pointed to the possibility that the situation they observed may be due to inhibitory products of the five dominants concerned, these products enabling early invaders to hold the ground against others which might show themselves better adapted to the area if given the same start. I n the light of Muller’s work (1966) an intensified search for allelopathic influences (see Section VII) as contributing to the stability of vegetation, either at the stand level or the association level, may well prove rewarding.

D.

ECOTYPES

Consultation of the distribution map of the seven most important shrubby species of the shadscale zone (Billings 1949), showing a range from relatively restricted distributions to one (Eurotia lanata) extending into Canada and Mexico, would not seem to offer any comfort to those inclined to accept the concept of discrete or integrated associations. However, we have little knowledge of the successional status of the vegetation existing in the areas in question and little definite knowledge concerning ecotypes. I n a later paper Billings (1952) discussed the likelihood that unique environments may be occupied by unique physiological

116

A. N. LANGFORD AND M. F. BUELL

biotypes and referred to the opinion of Clausen (1951, pp. 52-53) that a few generations may suffice to develop a new ecologicalrace or to change an old one to fit new conditions in rapidly changing environments. Environmental changes have probably not been at all rapid in the area in question, but doubtless there has been ample time for the extensive development of ecotypes throughout this area. Gates et al. (1956), whose work was discussed above, pointed to the lack of investigation of ecotypic variation within the salt-desert shrubs of their study. They suggested that, “if ecotypic variation is a logical explanation for the wide adaptation within each species, then the worth of the species as an indicator is considerably reduced”. They noted the possibility that they may have been dealing with “. . . an unknown number of ecotypes which were not identifiable morphologically”. Clausen et al. (1958) noted that the races of Achillea in a section of the sagebrush zone discussed herein were distinct from those at comparable altitudes on the western slope of the Sierra Nevada but did not give data for a range of localities within the area mapped by Billings (1949) or studied by Gates et al. (1956). They did, however, give ample data on the dynamics of race formation in Achillea, including evidence of a distinct zonation of biotype mixtures, correlated with different climatic situations. Recognizing that diversity is greater in some groups of plants than others, they suggested that the total number of ecological races within the three species of the Achillea millefolium complex may easily run into the hundreds. Felger and Lowe (1967), investigating the columnar cactus Lophocereus achottii, in Mexico, presented evidence of the evolution of coldadapted, xerophytic ecotypes at the northern and drier limit of the range of the species. Southern stems are smaller and with more ribs. The massiveness of the northern forms is a clear adaptation for the more rigorous climate found there. Felger and Lowe spoke of a cline from north to south but investigated eight localities only, not enough to indicate clearly the extent to which the ecotypes are distinctive as contrasted to continuously varying. However, it may surely be agreed that the overwhelming evidence from genetical studies to date indicates clearly that in species as a whole race formation is the rule. The divisive process is at work. The work of McMillan (1964,1965 and earlier references given therein) is of particular significance because of its very extensive nature and ecological perspective. McMillan has studied the behaviour of numerous transplants of North American grasses from a wide geographical range of sites. He has not only demonstrated extensive ecotypic differentiation but has correlated much of this variation with habitat variation. He has developed not only the concept that such differentiation results in the

INTEGRATION, IDENTITY AND STABILITY

117

harmony of vegetation and habitat but that it result,s in continuity of community-type over considerable habitat diversity. McMillan views his work as indicating the individualistic evolution of plant communities.

E.

THE UNIVERSALITY OF DIVISIVENESS

Speciation and race formation are manifestations of the same divisive process in life as a whole but to different degrees and, of course, at different levels in the hierarchial system of classification. Wherever there is genetic variation, selection is at work, operating not upon single genes but upon the whole genotype. The result is that the continuum of differences that may be visualized within any small segment of a species at any moment is subject to the divisive process which is the result of the combination of genetic variation and natural selection. Species pointed to early extinction may constitute an exception. The result is that more and more discrete units emerge from any earlier unit, each unit itself somewhat variable, but, as a whole, adapted more precisely for a narrower range of environmental conditions than was the earlier unit from which it emerged. There is no worldwide uniformity in the rate of these divisive processes and so we may recognize relatively stable units in some situations and relatively high rates of race formation in others, e.g. in Achilleu (Clausen et ul., 1958). Our view of the association is that it, too, is largely a product of the divisive processes of variation and natural selection and that the whole force of evolution is to bring about discrete recognizable units, each of these containing the “seeds” of further variation. The analogy with speciation leads us to expect that some association units will be more sharply defined than others, that some are in a period of relative stability while others are less stable. The analogy with speciation does not, of course, lead us to the view that the elements of an association of the present are derived wholly from the elements of a single earlier association which may have occupied the same general area or a contiguous area with abiotic controls similar to those of the present. We are quite aware of the evidence (Chaney, 1925) that the elements of a modern association may have been derived, though likely following some modification, from earlier elements of a number of geographically distinct sources. We do believe, however, that an existing association provides the best milieu for the slow and continuing evolution of that association. This is the “joint evolution of species” of Goodall (1963). Students of speciation have long been busy unearthing the nature of isolating mechanisms and stabilizing factors in both the plant and the animal kingdoms. In this paper we have given some attention to this question of stability and

118

A. N. LANGFORD AND M. F. BUELL

conclude that the influence of a wide-ranging dominant, dominant in the physiognomic sense and in the physiological sense as well, is a very strong one, imposing a considerable portion of the framework within which evolution occurs for a particular association. These views are in harmony with those of Baker (1966) that “. . . the stage is set for the next step in synthetic evolutionism, the study of the evolution of biotic communities . . .”. Our consideration of the significance of ecotones leads us to believe that a widespread association, e.g. the maple-beech forest of Clements, may well be subject to the same divisive forces and that only the most careful analysis on the order of that employed by Clausen and his associates (1958) or by McMillan (1965) might be expected to reveal emerging associations. The concept of the association that we support is assuredly not simply Clementsian (see p. 105). Continuum analysis has not, however, in our opinion, shown the fallacy of Tansley-modified,nonorganismic Clementsian concepts of associations. It has, however, given quantitative expression to the sort of variation which Clements described qualitatively as pertaining to any successional series within a climax association area.

F.

GEOGRAPHICAL ASPECTS O F T H E ASSOCIATION CONCEPT, W I T H S P E C I A L R E F E R E N C E TO S T A B I L I T Y

Even in the days of Clements, the term “climax association”, applied to a broad sweep of country, was an abstraction. The activities of man have so changed and so continue to change the entire landscape that the mature climax association, as a slowly evolving unit, today has little concrete reality, sound though it may be in principle. The groupings of species that led to the concept of discrete associations were apparently more obvious in the non-arid temperate zones of the world than in the tropics and this, of course, is where its proponents grew up and, largely, lived as research workers. By contrast, for example, the tropical rain forest was known to have great diversity and richness and these attributes were adduced by Gleason (1926) as a reason for rejecting the concept of discrete, integrated associations. In 1952, Richards, still uninfluenced by the quantitative drive to substantiate the individualistic concept of the association, none the less concerned himself with the climax concept. He concluded at that time that the knowledge of tropical vegetation was insufficient to justify a f d discussion of climax theory as applied to the tropical rain forest. However, he rejected the monoclimax hypothesis and favored that of polyclimax. He recognized, for example, five primary forests of the

119

INTEGRATION, IDENTITY AND STABILITY

Moraballi Creek area of Guyana, but saw “. . .no reason to consider any one of the five as less stable than the others”. The distinctiveness of these forests he ascribed to different, permanent combinations of soil and topography. He also referred to them as constituting a “. . . catena of climaxes”. I n 1963 Richards expressed a preference for the newer ordination methods, rather than attempts to set up “associations”, for the presentation of a meaningful picture of rain forest floristic composition. He exempted from this view the distinctive “single-dominant types” which he considered as belonging on special soils under special topographic conditions, with the entire habitat rather unfavorable. Richards also reviewed work carried out by Schulz in Surinam, indicating a relatively large number of “leading species” in a certain “mesophytic forest”, with considerable variation from large plot to large plot. The conclusion was none the less that average floristic composition was more or less the same in a single geographical region. I n terms of the occurrence of two hundred or more species of large trees in the forest in question, the restriction of the “leading species” to twenty or less does not seem very different, relatively, from the situation in temperate forests. Variations in soil and topography, re-emphasized years after publication of his “Tropical Rain Forest”, together with those in microclimate, were set forth by Richards as chief determinants of the nonrandom element of variation in tropical rain forest vegetation. He characterized the responses to variations in these environmental factors as amazingly sensitive and complex. All must admit the complexity of the tropical rain forest. Dobzhansky (1950) has discussed the effect of mild tropical environments upon evolution and compared these effectswith those of physically harsh environments, such as the Arctic tundra. In spite of the availability of food and moisture in the tropical rain forest, Dobzhansky considers the environment there as “harsh and exacting”. He wrote of the “. . tremendous intensity of the competition for space among plants in tropical forests .. .” and of the complex interrelationships among the many species present. He pointed out that,

.

“The effectiveness of natural selection is by no means proportional to the severity of the struggle for existence, as has so often been implied, especially by some early Darwinists. On the contrary, selection is most effective when, instead of more or less random destruction of masses of organisms, the survival and elimination acquire a differential character. Individuals that survive end reproduce are mostly those that possess combinations of traits which make them attuned to the manifold reciprocal dependencies in the organic community. Natural selection becomes a creative process which may lead to emergence of new modes of life and of more advanced types of organization.”

A t this point we conclude that the integrity of the tropical association

120

A. N . LANGFORD AND M. F. BUELL

is an expression of, a resultant of, these complex interrelationships and that its stability in non-successional situations may be very high. We had been inclined to think that the farther one moved away from the tropical rain forest the simpler the picture of the plant association would become, partly because of the ever-smaller number of species present and partly because of the critical nature of the environmental conditions, the chief cause, of course, of the species depauperization that occurs. Weaver and Clements (1929) placed Picea ghuca and Abies balsamea as the two dominants of the Picea-Larix association of the boreal forest. Rowe (1961) called on his extensive first-hand experience in the boreal forest west of Hudson Bay in refutation of a concept that the upland soils of northern Alberta support a climax with white spruce dominant but including small amounts of balsam poplar (Populus balsamifera) and fir. Rowe found no static spruce-poplar-fir association but described an optimal phase with tall white spruce dominant, lasting for about one hundred years; an ageing phase, even more dominated by white spruce, but without regeneration of tree species; and finally a degenerating phase, followed by a young phase when tree species, notably white spruce, again find conditions suitable for development. Rowe estimated that this full cycle takes about two hundred years. White spruce fails to qualify as a true climax species with Rowe because it is not strongly self-perpetuating. Nor did he accept any other species as having characteristics that enable it to participate in a self-perpetuating climax. Rowe regarded this forest in Alberta as a disturbance forest, commonly maintained in youth and health by frequent fires. If fire and extensive windthrow were absent it appears that the persistent cover of the area in question would not be a good stand of white spruce but an open, unhealthy forest of mixed species. Could such a forest or forest cycle be classed as climax? We can give no h a 1 opinion. We can say, however, that this forest is not a highly organized, stabilized forest. Its white spruce lacks the sort of features that enable Acer saccharurn to participate in a self-perpetuating climax. On the other hand, Rowe (1961) recognized that in the eastern Canadian boreal forest, where moisture conditions are much more favorable than in northern Alberta, there are distinctive, irregularly-structured spruce forests which have persisted for several generations. Here we could certainly speak of a lasting climax forest. If frequent fire and windthrow are considered as normal elements of the environment, it would be possible to conceive of this whole cyclic manifestation in northern Alberta as the climax condition for this area. This whole cyclic situation is reminiscent of the idea of “regeneration complexes” as treated by Watt (1947), who described a cyclic development in a bog at Tregaron, Wales, from open pools through three species

INTEGRATION, IDENTITY AND STABILITY

121

of Sphagnum to a hummock that is taken over by Calluna and other species but finally returns to the pool condition, largely because of differential rates of vertical growth in adjacent patches. Watt discussed the opposed opinions of the aggregate of vegetation as ( a ) a single community or ( b ) an aggregate of communities. The central point is that “. . . the immediate cause [of the cyclic development] does not reside exclusively in the patch itself but in the spatial relation between patches and their relative changes in level”. Watt regarded “. . .the regeneration complex as a community of diverse phases forming a space-time pattern. Although there is change in time at a given place, the whole community remains essentially the same; the thing that persists unchanged is the process and its manifestation in the sequence of phases.” Watt’s data from a dwarf Calluna community on exposed slopes of the Cairngorms of Scotland not only provide another “regeneration complex” but offer auseful comparison in connection with our consideration of the nature of the plant association in diverse areas, such as the tropical rain forest and the boreal forest of northern Alberta. He presented clear evidence of a three-phase system; narrow Calluna strips spreading away from the prevailing wind, gradually dying out behind and growing forward over protected strips of Arctostaphylos uva-ursi which, in turn, keep advancing, spreading into bare strips resulting from the earlier death of the Calluna of an adjacent strip. We may consider this vegetation as climax in character with a very clear and meaningful pattern in the distribution of its components. It also makes us wonder if the open, uneven forest of Rowe (1961) might not also be considered climax and but slightly organized. Watt (1947) also gave an excellent and pertinent review of the findings of Tragsrdh (1923) concerning the periodic extensive damage to central European conifer forests by the nun moth, which also attacks but causes far less damage to pine in northern Sweden. The presence in these open forests of Calluna and other food species of caterpillars which, as well as the nun moth, are parasitized by species of Pimpla, confers stability upon the Swedish pine forest. Watt’s point is that a complex interrelationship between ericads, lepidopterans, ichneumons and conifers results in greater stability in vegetative cover than exists in a system where the ericads are absent. Concerned with the wholeness of communities, Watt traced the shattering of the unified system embraced by Tansley’s (1935) term “ecosystem”, all the way from the separation of the biome from the nonliving habitat to Gleason’s (1936) characterization of the plant association as “. . . merely a fortuitous juxtaposition of plant individuals”. Watt fully recognized, however, that Gleason’s concept was of plant and environment forming one interlocking system. Discussing Gleason’s

122

A. N . LANGFORD AND M. F. BUELL

illustration of a two-layered community, a t’reeand an herb beneath it, Watt wrote,

“. . .

it is divorced from its spatial moulding context and set in a moment in time. In time, both will change (Gleason recognized this) and their successors be influenced by their collective surroundings.In short, Gleason has minimized the sign5cance of the relations between the components of the community in horizontal space and in time. These relations constitute a primary bond in the maintenance of the integrity of the plant community; they give to it the unity of a co-ordinatedsystem.”

Watt recognized the unlikelihood of the research worker, concerned with discovering the modus operandi of an ecosystem as a whole, having “. . . an equal equipment (of skills and understanding) in all branches of knowledge concerned”. He favored, however, “. . . the ultimate even if idealistic objective of fusing the shattered fragments into the original unity . . .” as both important and practical.

VII. T H E SPECIALC A S E S O F AUTO-INTOXICATION, SYNERGISM A N D ALLELOPATHY A.

E A R L Y WORK A N D T H E P E R I O D O F C O N C E N T R A T I O N U P O N S I N G L E FACTOR E X P L A N A T I O N S O F BIOLOGICAL E V E NTS

It is amazing that the investigation of synergism and antagonism, at the level of the higher plants, has been so slow in developing. This is particularly so in the case of antagonistic influences, as reviewed by Martin (1957). Martin pointed out that whereas De Candolle wrote clearly in 1832 regarding the production of peach-inhibiting substances by peaches and regarding the inhibition of certain plants by the growth of Cirsium,Erigeron and Euphorbia and thus opened the door to investigation of allelopathy (sensu Muller, 1966), Liebig closed this door effectively through the strength and wide acceptance of his claim that effects such as those observed by De Candolle were simply due to the exhaustion of mineral nutrients. The frown of the mighty Liebig, standing behind his useful “law of the minimum” (or principle of limiting factors) seems to have been enough to impede progress in this field for a full fXty years, following which new bits of evidence appeared that gradually brought us through Juglans nigra and its juglone (Davis, 1928) to our present state, with a rapid proliferation of incisive studies of allelopathy by investigators in the group associated with C. H. Muller (see references in Muller, 1966, and Muller and Hauge, 1967) in California. I n 1950, however, Bonner could write: “From the time of

INTEGRATION, IDENTITY AND STABILITY

123

Liebig until the present day plant growth interactions have been almost unanimously interpreted in terms of mineral nutrition effects, or more recently in terms of water competition”. Liebig’s concentration upon the over-riding significance of a single factor as the limiting factor in a complex situation had been a great advance from the days when success or failure in growing a particular crop was vaguely ascribed to various combinations of environmental factors. Concepts of disease were in just about the same stage of confusion, prior to the establishment of the germ theory of disease, as documented in almost any good textbook of plant pathology (e.g. Walker, 1957) and the result of the establishment of this germ theory of disease was similar. A single factor, usually a bacterial or fungal pathogen, was assigned over-riding significance in the development of a disease situation and, for years, environmental considerations received far less attention than hitherto as the search for the specific causes of disease continued. Jones and his associates at Wisconsin (Jones et al., 1926) made the greatest single contribution to elucidate the essentially complex picture of the disease condition, involving a single causal organism, bringing about a renewed appreciation of the role of environmental factors in disease development, but it remained for others to show that, at least in soil-borne pathogens, the interaction of two or more micro-organisms might determine the incidence of disease. Sanford (1926) was very early in this field. Garrett (1959), reviewing these developments, wrote, “Thus was ended the despotism of Koch’s postulates-a despotism which began beneficially by insuring the essential observance of strict rules of evidence in the conduct of inoculation experiments, and ended by restricting enterprise”. It is tempting to think of the wholehearted acceptance of the law of the minimum, of Koch’s rules of proof of pathogenicity and the precise units of Clements as all restricting enterprise. This could not be said of Gleason’s individualistic concept of the plant association, with its emphasis on the interaction between an individual plant and its environment, as stated and elaborated over a period of time: it could, however, apply to the wholehearted acceptance of the concept that vegetation is simply a continuum. Wolf and Wolf (1947, p. 281) chronicled clear demonstration of the reciprocal influence of metabolic products of pairs of cultured fungi as far back as 1892. Cook’s (1921) demonstration of the inhibitory action of black walnut upon tomato and potato and the demonstration by Davis (1928) that the toxic product of walnuts is 5-hydroxy-a-naphtha-quinoneare in the same general period as a series of demonstrations of both antagonism and synergism in microorganisms, conveniently summarized by Wolf and Wolf (1947, Vol. 11,

124

A. N. LANGFORD AND M. F. BUELL

p. 280 ff.). Inability to identify specific metabolites responsible for antagonism or synergism did not prove to be an obstacle to progress in these fields among the microbiologists, as may be seen from the writings of Wolf and Wolf or from a brief review by Garrett (1959). I n the higher plants, however, progress has been slow and acceptance of the significance of antagonism and synergism has been delayed, relatively. Bonner (1950), dealing with Davis (1928), pointed out that Davis did not show that juglone is liberated into the soil by the roots of black walnut, that he did not establish that the injurious effects of black walnut in the field were due to the liberation of any toxic substance and that he merely correlated the existence of a toxic substance in the plant with the fact that walnut trees did cause inhibition. Massey (1925), however, working earlier than Davis, seeing wilted tomato plants distributed along a line which was later shown to be the same as the line of growth of a walnut root, removed the soil carefully from such tomato plants and found that “in every case there was close contact between the tomato roots and those of the walnut”. Bonner’s (1950) requirement, “Final demonstration of production by a given plant of a substance inhibitory to the same or other species can be only by isolation of the compound in pure form and demonstration that the substance isolated is actually the agent by which the inhibition is achieved”, seems to carry with it some of the “despotism” that Garrett associated with Koch’s Postulates and possibly a restriction of enterprise. Bonner reviewed his laboratory’s work with guayule, with the clear demonstration of the production of toxic trans-cinnamic acid and its outwards passage from live roots. Bonner also reported the rapid disappearance of cinnamic acid from moist unsterilized soil, presumably through the action of soil micro-organisms. He concluded:

“. . .

no soil accumulation of toxic substances could be demonstrated in any field planting where guayule had been shown to grow successfully guayule does give off, or lose to the surrounding medium, a toxic compound. Under conditions of good agricultural practice, however, this substance does not appear to accumulate and it may be destroyed as rapidly as it is produced. In any case the production of the toxic substance appears to be of significance only in pot culture or perhaps in nurseries where plants are grown in crowded conditions for long periods of time.”

B.

. ..

THE EMERGENCE O F A N UNDERSTANDING OF THE COMPLEXITY O F BIOCHEMICAL INTERACTIO NS AMONG T H E H I G H E R P L A N T S

We may accept the high probability that various toxic exudates of the vascular plants are likely to be destroyed fairly rapidly by the action

INTEGRATION, IDENTITY AND STABILITY

125

of soil micro-organisms. However, Massey’s (1925) demonstration of the close contact between walnut roots and inhibited tomato roots should encourage a more extensive search for allelopathic influences, quite apart from the difficulties of demonstrating the specific metabolites involved, desirable though such demonstrations may be. A re-examination of the somewhat remarkable and surprising situation revealed by the experiments of Korstian and Coile long ago (1938) with “trenched plots” under natural oak and pine forest canopies in the Duke Forest of North Carolina might prove to be very interesting. The original article is probably not very widely distributed and the reference to it in Oosting’s text (1956) under the heading of “shade tolerance” always seemed a satisfactory assessment of the situation. When tree roots entering such plots were severed, the development of “shadeintolerant” species was much greater than in equivalent check plots. Certainly competition with the trees for water and minerals was eliminated and certainly shade alone could not have been responsible for the poor showing of “shade-intolerant” species in the check plots, but the complete explanation for the observed effects has not been given with certainty. Three and four years after the trenching, no significant differences were found between the chemical analyses of trenched and untrenched plots, with respect to four tests: total organic carbon, total nitrogen, nitrates and ammonia. Increased soil moisture seems to have been an important factor stimulating the extra development in the trenched plots, but in an appreciable number of cases the measures were not significantly different. Furthermore, unfortunately, the most important type of test, an untrenched plot to which was added enough water to maintain the soil moisture values constantly above those in the trenched plots, was not included in the experiment. Our present knowledge of the production of inhibitory metabolites, together with Massey’s findingswith black walnut and tomato, suggest the wisdom of a search for allelopathic and /or synergistic influences in this and similar situations. The occurrence of relationships among the roots of various seed plants, intimate enough to allow the passage of materials from one plant to another thereby, has been shown by Bormann (1957). We may confidently predict that many additional antagonistic and synergistic influences will be demonstrated among the vascular plants. We must note, however, that in 1960 Borner, reviewing the entire problem of the liberation of organic substances from higher plants, and following considerable research of his own, held the opinion that allelopathy is relatively unimportant in vegetation as a whole. Borner stated that such organic “materials as do diffuse from roots probably are restricted to the immediate rhizosphere and do not exercise a direct influence on other plants”. Borner did not, however, recognize the importance of Massey’s

126

A. N. LANOFORD AND M. F. BUELL

(1925) demonstration of close associations of walnut roots and the roots of wilted tomato plants. I n the light of this demonstration he may have underestimated the significance of allelopathy. Brown’s Michigan studies (1967) were undertaken in an attempt to find an explanation for the highly uneven distribution of stems of Pinus banksiana in apparently uniform sites, where variations in the usually recognized range of environmental factors failed utterly to account for the variation observed. Brown not only showed that extracts of seven species of vascular plants of the jack pine community, e.g. Solidago juncea, inhibited germination of jack pine seeds, but that extracts of Cornus canadensis stimulated germination while extracts of 28 others were without effect. I n the field he chose, subjectively, 1 m2 plots, each dominated by as dense and as nearly pure a stand of certain species (including Pteridium q u i l i n u m , Pinus resinosa, Cornus canadensis and several ericads) as he could find. I n each plot vegetation was clipped to a height of 1-2 in., the soil surface was scratched with a rake and 400 seeds of jack pine sown. The three lowest figures for seedling emergence were from plots under the influence of the three species whose water extracts proved inhibitory in laboratory tests. The three highest figures were from plots influenced by Pteridium aquilinum (neutral in its effect in laboratory tests) and the two species that were stimulatory in laboratory tests. Brown recognized that some of the variation observed in his experiments might be due to variation in available mineral nutrients. However, the correlation between the behaviour of extracts and of field plots dominated by the corresponding species indicates strongly the occurrence of biologically active chemicals influencing germination and growth of jack pine and, thus, the composition of vegetation in jack pine stands. Studies of barley, Hordeum wulgare, by Overland (1966) showed clearly the inhibition of both germination and growth in several species, notably Stellaria media, under laboratory conditions by leachates from dead roots, living roots and seeds of barley. The alkaloid gramine is considered the probable inhibitor, but this has not been proven, nor did Miss Overland demonstrate the magnitude of such inhibitory effects under field conditions. Once again, however, grave doubt has been cast upon the standard explanation that the effectiveness of barley as a “smother crop” is due to simple competition for nutrients and water. Shades of Liebigl Muller and his co-workers (Muller, Muller and Haines) from 1964 to the present have intensified their investigation of volatile inhibitors produced by Salvia leucophylla and other species. The most complete treatment of the subject is that of Muller in 1966, which includes references to earlier work. Muller demonstrated that on certain clay soils

INTEGRATION, IDENTITY AND STABILITY

127

the inhibition of various elements of annual grassland vegetation is, in certain years, complete for the first one or two metres from the Salvia, resulting in a continuous bare zone. Progressively less inhibition was demonstrated for a total distance of up to ten metres from the Salvia. Muller isolated toxic products, cineole and camphor, in the air surrounding Salvia, demonstrated the uptake of these terpenes by dry soil particles, and demonstrated their toxicity not only to the main test plant, Cucumis sativus, but to a whole series of species of the adjacent grassland, including Bromus mollis, Erodium cicutarium, Festuca megalura and Stipa pulchra. The inhibitory influence extended well beyond the limit of Salvia roots, in an uphill direction as well as downhill. Laboratory tests of nine other aromatic species in unrelated families showed the presence of chemical inhibitors, as did tests of certain nonaromatic components of chaparral vegetation, including Adenostoma fasciculatum. Muller’s thoughts on the evolution of biochemical inhibitory mechanisms are particularly interesting. The center of his thesis is that while we have all realized for many years that micro-organisms pass metabolites into their environment freely and that many of these are autointoxicants or antibiotic in effect, we have not appreciated fully the comparable processes in the higher plants. Muller considers the escape of auto-intoxicants from vascular plants, either as volatile compounds or as compounds that diffuse from roots into the soil, as a prime and necessary attribute but states, “If. . . the plant also inhibits a competitor or resists a pathogen or repels a browsing animal, the added advantage, no matter how slight, would constitute significant selective pressure with the passing of successive thousands of generations”. To “inhibits a competitor”, we could add, “favors an associate”. Rice (1964), in an article that includes references to earlier detailed studies, has shown that early colonists of abandoned fields in Oklahoma, having low requirements of nitrogen, are assisted in maintaining a competitive advantage over species with higher nitrogen requirements in an indirect fashion. For example, Aristida oligantha, which dominates the annual grass stage of succession for from 9 to 19 years, yielded extracts which proved to be strongly inhibitory to nodulation of bean plants by Rhizobium and further, in sand culture, reduced nodulation of inoculated bean plants. Rice concluded that this suppression of nitrogen supplies enabled Aristida to maintain its dominance over more robust potential competitors having higher nitrogen requirements. Muller (1966), investigating the production by Salvia leucophylla of volatile terpenes that inhibit the development of annual grasses close to the Salvia, noted in the same study that seedlings of Salvia rarely developed among mature Salvia shrubs, even where there was abundant

128

A. N. LANQFORD AND M. F. BUELL

open space. These findings suggested strongly to Muller that “the same allelopathic influence that restricts the growth of annual herbs is also causing the deterioration of the shrubs and inhibiting the establishment of their seedlings. This auto-toxicity is probably of wide significance in plant succession in many kinds of vegetation.” It is interesting to note that Hough and Forbes (1943), who studied very old forest stands in Pennsylvania, concluded that “climax” forests of hemlock eventually break up and deteriorate, only to return once more, gradually, as the dominant form of vegetation. We have good evidence, then, that both antagonism and synergism are to be recognised as stabilizing influences in the plant association or in the plant community, while auto-intoxication may well be a cause of plant succession. What the relationships among these three processes, synergism, inter-species antagonism, and auto-intoxication are in various climax associations remains to be seen.

V I I I . CONCLUDINQ STATEMENT Clements and Gleason proposed two very extreme views of the nature of the plant association. Neither view, as stated, is justifiable today. We cannot accept the association either as an organism or as merely a fortuitous juxtaposition of plant individuals. Since the bitter controversies of the 1920’8, ground has been shifted but the polarity of viewpoints has persisted. Strength has been gathered on both sides of the controversy and attempts to reconcile different viewpoints have been made. On the one hand, and perhaps the more vigorous development, has been the series of ingenious methods for marshalling quantitative data in support of the individualistic concept, namely continuum analysis and the more sophisticated 3-dimensional ordination techniques. On the other hand, almost unnoticed, there have been many unconcerted efforts that have, quite incidentally, strengthened the alternative concept of integrated associations. Testing continuum methods in relatively undisturbed upland forests in northern New Jersey, largely dominated by Quercw, we found successional trends which added strength to our growing conviction that many forests over a very broad area were shifting towards dominance by more mesic species, particularly Acer saccharurn. We concluded that the widespread demonstration of vegetational continua failed to dispose of the essential and non-organismic views of climax associations as held by Clements and modified by Tansley. I n spite of the fact that wide-ranging climax associations are largely historical in nature, the intellectual exercise of examining the possible defence of Tansley’s concept of the

INTEGRATION, IDENTITY AND STABILITY

129

association seemed a promising one, and particularly so in the light of evidences that were unavailable to the early protagonists in this field. We agree with Lambert and Dale that those making comparative quantitative studies of vegetation should have no advance assumptions concerning continuity or discreteness in communities or associations, believing that hypotheses will emerge from the treatment of appropriate data. On the other hand, it appears to us that nearly all comparative studies have been directed to intra-community comparisons. Our knowledge of ecotypic variation is relatively slight but enough to indicate that ecotypes may be precisely enough delimited so that one may be adapted particularly for the environmental conditions found in one particular association or even one particular community while others may be found in neighbouring groupings of plants. Furthermore, as numbers of species and species diversity increase with ecological approach to the tropical rain forest, the likelihood increases that individual groups of species will occupy near-identical ecological roles in the constitution of vegetation, so that the precise species present may be of decreasing significance along this gradient to the rain forest. For these two reasons our interest shifted away from a pre-occupation with precise figures intended to assess the importance of individual species in a community or association, as a criterion for judging the nature of the association. At the same time our interest shifted towards the problem of integration and stability a t various levels in the ecosystem, but particularly at the association level. The tremendous unifying influence exerted by a few dominant species, or even by one species, propelled us in this direction, as did the knowledge that there are sudden transitions in vegetational composition along gradual environmental gradients. We considered further the possible parallels between certain homeostatic mechanisms which are operative particularly in various species with a short life history, buffering them against environmental fluctuations and thus promoting a varied but steady state, and mechanisms that lead to stability of the association. Had he been provided with modern data on genetic variation, Nichols might have made more cogent comparisons of species and associations. We examined the question of critical levels or response thresholds along gradual environmental gradients. We became convinced that not only various plant-animal interrelationships and such relatively obvious things as mycorrhizae but also biochemical reactions among the higher plants may be of significance there, giving integrity and stability to the association. The importance of synergisms has not been assessed extensively, but recent work on chemical inhibition (allelopathy) as a stabilizing influence is promising indeed and it is tempting to predict that we B-

130

A. N . LANGFORD AND M. F. BUELL

are just at the threshold of knowledge of integration and stability in plant communities. We would expect the most highly integrated and stable associations to be found in the wet tropics, where there are many suitable “candidates” for virtually similar positions. I n alpine, boreal and other related situations there is evidence of less stable communities. We consider that evolution towards stability is commonly still in progress, that it may have been achieved in some harsh situations and is imperfect in others. The essentially divisive process of evolution continues in virtually all living things, at all levels. The result is adaptation and stability (for any set of conditions) for the species, for the community, for the association until it is segmented, chiefly through the activities of man. “Crashes” in various northern animal populations and degeneration of certain undisturbed boreal forests are expressions of a lack of such stability. I n moist, temperate areas, interacting biotic factors combine to favor the development of a high degree of stability. The relatively low diversity of this temperate vegetation, compared with the high diversity and complex interrelationships of the wet tropics, makes this stability more obvious. I n the arid regions of the Great Basin Desert of the United States, however, stability of vegetation is commonly found, but not necessarily a t the association level, a fact well reflected by the work of Gates et al. (1956). Whereas biotic influences play an outstanding role in determining the nature of climax vegetation in moist temperate areas, abiotic factors are outstandingly pre-eminent in controlling vegetation in arid or very cold regions. I n such regions succession, which is essentially due to modification of the environment by organisms, with its direction or course somewhat variable according to the availability of various propagules, may be almost absent. Muller (1940,1952)dealt with two such extremes in which competition was absent, and in which the pioneers following disturbance were virtually the components of the stable community. Muller introduced the term “non-selective autosuccession” to describe the action following disturbance in such extreme areas. The concept of the plant association, even in the non-organismic sense, and with the modifications introduced by Tansley, cannot be applied to a vegetated area in which competition and dependence are not found. We agree with Muller that the vegetation he described as illustrating auto-succession is indeed individualistic in its nature. I n view of the various considerations discussed above, it is perhaps not surprising that the concept of discrete, stable climax associations should have flourished to such a great extent in central and eastern North America and found favor in other regions with a full cover of vegetation. The climax association, in the sense in which we have discussed and

INTEGRATION, IDENTITY AND STABILITY

131

defended it, is now largely an abstraction of an historical phenomenon, albeit an interesting one, but the processes that shaped it are operative today in existing aggregations of species. Ecologists of today can acknowledge their great debt to both Clements and Gleason and recognize the usefulness of the fruits of the controversies which their divergent views engendered. We believe that climax associations, as undisturbed by man, had achieved a high degree of integrity and stability wherever time was sufficient and abiotic factors were not so severe as to prevent aggregation of organisms, with the resultant modification of the environment (reaction).We agree with Baker that thestage is now set for the next step in synthetic evolutionism, the study of the evolution of biotic cwmmunities, even of ecosystems, but the task will not be easy and progress will depend largely upon the extension of our knowledge of those lesser units of vegetation below the rank of association as discussed in this paper. I n such community study, investigation of the processes involved in the interactions among organisms will surely yield rich rewards.

REFERENCES Baker, H. G . (1966). Bioscience 16, 35-37. Reasoning about adaptations in ecosystems. Billings, W. D. (1949). Am. Midl. Nut. 42, 87-109. The shadscale vegetation zone of Nevada and eastern California in relation to climate and soils. Billings, W. D. (1952). &. Rev. Biol. 27, 251-265. The environmental complex in relation to plant growth and distribution. Bonner, J. (1950). Bot. Rev. 16, 51-65. The role of toxic substances in the interactions of higher plants. Bormann, F. H. (1957). PI. Physiol., Lancaster 32, 48-55. Moisture transfer between plants through intertwined root systems. Borner, H. (1960). Bot. Rev. 26, 393-424. Liberation of organic substances from higher plants and their role in the soil sickness problem. Braun, E. L. (1950). “Deciduous Forests of Eastern North America.” Blakiston, Philadelphia. Bray, J. R. and Curtis, J. T. (1957). Ecol. Monogr. 27, 325-349. An ordination of the upland forest communities of southern Wisconsin. Brown, R. T. (1967). Ecology 48, 542-546. Influence of naturally occurring compounds on germination and growth of jack pine. Brown, R. T. and Curtis, J. T. (1952). Ecol. Monogr. 22, 217-234. The upland conifer-hardwood forests of northern Wisconsin. Buell, M. F. and Cantlon, J. E. (1951). Ecology 32, 2 9 4 3 1 6 . A study of two forest stands in Minnesota with an interpretation of the prairie-forest margin. Buell, M. F., Langford, A. N., Davidson, D. W. and Ohmann, L. F. (1966). Ecology 47, 416-432. The upland forest continuum in northern New Jersey. Cain, S. A. (1947). Ecol. Monogr. 17, 185-200. Characteristics of natural areas and factors in their development. Cantlon, J. E. (1953). Ecol. Monogr. 23, 241-270. Vegetation and microclimates on north and south slopes of Cushetunk Mountain, New Jersey.

132

A. N. LANOFORD AND M. F. BUELL

Chaney, R. W. (1925). Carnegie Inat. Wash. Publ. 349,l-22. A comparative study of the Bridge Creek flora and the modern redwood forest. Clausen, J. (1951). “Stages in the Evolution of Plant Species.” Cornell Univ. Press, Ithaca. Clausen, J., Keck, D. D. and Hiesey, W. M. (1958). “Experimental Studies on the Nature of Species 111. Environmental Responses of Climatic Races of Achillea.” Carnegie Inst. Waah. Publ. 581. Washington. Clements, F. E. (1916). “Plant Succession.” Carnegie Inst. Wash. Publ. 242, Washington. Clements, F. E. (1928). “Plant Succession and Indicators.” Wilson, New York. Clements, F. E. (1936). J. Ecol. 24, 252-284. Nature and structure of the climax. Cook, M. T. (1921). Phytopathlogy 11, 346. Wilting caused by walnut trees. Crow, J. F. (1952). I n “Dominance and Overdominance in Heterosis” (J. W. Gowen, ed.), pp. 282-297. Ames, Iowa State College Press. (1964 Reprint, New York: Hafner). Curtis, J. T. (1955). Ecology 36, 558-566. A prairie continuum in Wisconsin. Curtis, J. T. (1959). “The Vegetation of Wisconsin.” Univ. Wisconsin Press, Madison. Curtis, J. T. and McIntosh, R. P. (1951). Ecology 32, 476-496. An upland forest continuum in the prairie-forest border region of Wisconsin. Dagnelie, P. (1960). Bull. Sew. Carte phytogkogT., Centr. Natl. Rech. Sci., Paris SBr. B.5,7-71 and 93-195. Contribution 8.l’btude des communautbs vBg6talea par l’analyse factorielle. Daubenmire, R. (1966). Science N . Y . 151, 291-298. Vegetation: identification of typal communities. Davis, E. F. (1928). Am. J . Bot. 15, 620. The toxic principle of Jughns nigra as identified with synthetic juglone and its toxic effects on tomato and alfalfa plants. De Candolle, A. P. (1832). “Physiologie vBgBtale, ou Exposition des forces et des fonctions vitales des vBt6taux.” Vol. 111. BBchet jeune, Paris. Dice, L. R. (1952). “Natural Communities.” Univ. Michigan Press, Ann Arbor. Dix, R. L. (1957). Ecology 88, 663-665. Sugar maple in the climax forests a t Washington, D.C. Dobzhansky, T. (1950). Am. Scient. 38, 209-221. Evolution in the tropics. Dobzhansky, T. (1956). Evolution 10, 82-92. Genetics of natural populations. XXV. Genetic changes in populations of Drosophih pseudoobscura and Drosophih persimilis in some localities in California. Dobzhansky, T. (1962). Am. Nat. 96, 321-328. Rigid vs. flexible chromosomal polymorphisms in Drosophih. Ehrlich, P. R. and Holm, R. W. (1963). “The Process of Evolution.” McGrawHill, New York. Felger, R. S. and Lowe, C. H. (1967). Ecology 48, 530-536. Clinal variation in the surface-volume relationships of the columnar cactus Lophcereus schottii in northwestern Mexico. Garrett, S. D. (1959). Biology and ecology of root-disease fungi. I n “Plant Pathology-Problems and Progress 1908-1958”, pp. 309-316. Univ. Wisconsin Press, Madison. Gates, D. H., Stoddart, L. A. and Cook, C. W. (1956). Ecol. Monogr. 26, 155-175. Soil as a factor influencing plant distribution on salt-deserts of Utah. Gittins, R. (1965). J. Ecol. 53, 411-425. Multivariate approaches to a limestone grassland community. 111.A comparative study of ordination and association-analysis.

INTEGRATION, IDENTITY AND STABILITY

133

Gleason, H. A. (1917).Bull. Torrey bot. Club. 44, 463-481. The structure and development of the plant association. Gleason, H. A. (1926).Bull. Torrey. bot. Club 53,7-26. The individualistic concept of the plant association. Gleason, H. A. (1936).Ecology 17, 444-451. I s the synusia an association? Gleason, H. A. (1939).Am. Midl. Nat. 21, 92-110. The individualistic concept of the plant association. Goodall, D. W. (1963). Vegetatio 11, 297-316. The continuum and the individualistic association. Gray, R. and Bonner, J. (1948).Am. J . Bot. 35, 52-57. An inhibitor of plant growth from the leaves of Encelia farinoaa. Greenidge, K.N. H. (1961).Am. Midl. Nat. 66, 138-151. Patterns of distribution of sugar maple, Acer saccharum Marsh., in northern Cape Breton Island. Greig-Smith, P. (1964). “Quantitative Plant Ecology”, 2nd ed. Butterworths, London. Herskowitz, I. H. (1965).“Genetics.” Little Brown & Co., Boston. Hough, A. F. and Forbes, R.D. (1943).Ecol. Monogr. 13, 299-320. The ecology and silvics of forests in the high plateaus of Pennsylvania. Hult, R. (1885). Meddel. af Societas pro Fauna et Flora fennica 12, 163-247. Blekinges vegetation. E t t bidrag till vaxtformationeras utvecklingshistoria. Hutchinson, G. E. (1953).Proc. Acad. nat. Sci. Philad. 105, 1-12. The concept of pattern in ecology. Jaeger, E. C. (1957). “The North American Deserts.” Stanford Univ. Press, Stanford. Jones, L. R., Johnson, J. and Dickson, J. G. (1926).Univ. Wiac. Agric. Expt. Stn. Rea. Bull. 71. Wisconsin studies upon the relation of soil temperature to plant disease. Korstian, C. F. and Coile, T. S. (1938). “Plant Competition in Forest Stands” Bull. 3. Duke Univ. School of Forestry, Durham. Lambert, J. M. and Dale, M. B. (1964).I n “Advances in Ecological Research” (J.B. Cragg, ed.), Vol. 2,pp. 55-59. The use of statistics in phytosociology. Margalef, D. R. (1957).M e m Acad. Cienc. Artea Barcelona 23, 373-449. Information theory in ecology. (Transl. Wendell Hall.) Martin, H. (1957). “Chemical Aspects of Ecology in relation to Agriculture.” Publ. 1015. Can. Dept. Agr., Sci. Serv., Ottawa. Massey, A. B. (1925). Phytopathology 15, 773-784. Antagonism of the walnuts (Juglana nigra and J . cinerea L.) in certain plant associations. Maycock, P. F.and Curtis, J. T. (1960).Ecol. Monogr. 30,1-35.The phytosociology of boreal conifer-hardwood forests of the Great Lakes region. McIntosh, R. P.(1967).Bot. Rev. 33, 13&187. The continuum concept of vegetation. McMillan, C. (1964).Am. J . Bot. 51, 1119-1128. Ecotypic differentiation within four North American prairie grasses. I. Morphological variation within transplanted community fractions. McMillan, C. (1965).Am. J . Bot. 52, 55-65. Ecotypic differentiation within four North American prairie grasses. II. Behavioral variation within transplanted community fractions. Mikola, P.(1953).Karstenia 2, 33-34. An experiment on the invasion of mycorrhizal fungi into prairie soil. Mitchell, J. E., West, N. E. and Miller, R. W. (1966).Ecology, 47, 627-630. Soil physical properties in relation to plant community patterns in the shadscale zone of northwestern Utah.

134

A. N. LANGFORD AND M. F. BUELL

Muller, C. H. (1940). Ecology 21, 206-212. Plant succession in the h r r e a Flourenah climax. Muller, C. H. (1962). Bull. Torrey bot. Club 79, 296-309. Plant succession in arctic heath and tundra in northern Scandinavia. Muller, C. H. (1966). Bull. Torrey bot. Club 93, 332-361. The role of chemical inhibition (allelopathy) in vegetational composition. Muller. C. H., Muller, W. H. and Haines, B. L. (1964). Science N . Y . 143,471-473. Volatile growth inhibitors produced by aromatic shrubs. Muller, W. H. and Hauge, R. (1967). Bull. Torrey bot. Club 94, 182-191. Volatile growth inhibitors produced by SalwiQleucophylla:effect on seedling anatomy. Nichols, G. E. (1929). Proc. Int. bot. Congr. (1926), 1, 629-641. Ithaca, N.Y. Plant associations and their classification. Odum, E. P. (1963). “Ecology.” Holt, Rinehart and Winston, New York. Oosting, H. J. (1966). “The Study of Plant Communities.” Freeman, San Francisco. Overland, L. (1966). Am. J . Bot. 53, 423-432. The role of allelopathic substances in the “smother crop” barley. Philips, J. (1936). J. Ecol. 28, 488-608. Succession, development, the climax, and the complex organism: an analysis of concepts. Part 111. The complex organism: conclusions. Ponyatovskaya, V. M. (1961). Vegetatio 10, 373-386. On two trends in phytocoenology. (Translated by J. Major.) Rice, E. L. (1964). Ecology 46, 824-837. Inhibition of nitrogen-fixing and nitrif e g bacteria by seed plants. Richards, P. W. (1962). “The Tropical Rain Forest.” Cambridge Univ. Press, Cambridge. Richards, P. W. (1963). J. Ecol. 51, 231-241. What the tropics can contribute to ecology. Roe, F. G. (1966). Tram. R. SOC.Can. 3rd Ser., Sec. 11,49, 67-93. “Forests” and woods in mediaeval England. Rowe, J. S. (1961). Can. J . Bot. 39, 1007-1017. Critique of some vegetational concepts as applied to forests of north-western Alberta. Rowe, J. S. (1967). I n “The Evolution of Canada’s Flora” (R. L. Taylor and R. A. Ludwig, eds.), pp. 12-27. Univ. Toronto Press, Toronto. Phytogeographic zonation: an ecological appreciation. Sanford, G. B. (1926). Phytopathlogy 16, 626-647. Some factors affecting the pathogenicity of Actinornyces scabies. Scott, J. T. and Holway, J. G. (1967). Bull. ecol. SOC.Am. 48, 70. On the discrete and continuous nature of the forested vegetation in northeastern United States. Sinnott, E. W., Dunn, L. C. and Dobzhansky, T. (1968). “Principles of Genetics.” McGraw-Hill, New York. Tansley, A. G. (1936). Ecology 16, 284-307. The use and abuse of vegetational concepts and terms. Tansley, A. G. (1949). “The British Islands and their Vegetation”. Vol. I. Cambridge Univ. Press, Cambridge. Traghrdh, I. (1923). M a n . St. Skogsj&s Amt. 20, Ziele und Wege in der Forstentomologie. Walker, J. C. (1967). “Plant Pathology”, 2nd ed. McGraw-Hill, New York. Watt, A. S. (1947). J . Ecol. 35, 1-22. Pattern and process in the plant community. Weaver, J. E. and Clements, F. E. (1929). “Plant Ecology.” McGraw-Hill, New York.

INTEQRATION, IDENTITY AND STABILITY

135

Weaver, J. E. and Clements, F. E. (1938). “Plant Ecology”, 2nd ed. McGrawHill, New York. Went, F. W. (1942). Bull. Torrey bot. Club 69,100-1 14. The dependence of certain annual plants on shrubs in Southern California deserts. West, N. E. (1966). Ecology 47, 976-980. Matrix cluster analysis of Montane forest vegetation of the Oregon Cascades. Whitford, P. B. and Salamun, P. J. (1964). Ecology 35, 633-640. An upland forest survey of the Milwaukee area. Whittaker, R. H. (1966). Ecol. Monogr. 26, 1-80. Vegetation of the Great Smoky Mountains. Whittaker, R. H. (1962). Bot. Rev. 28, 1-239. Classification of natural communities. Whittaker, R. H. (1967). Biol. Rev. 42, 207-264. Gradient analysis of vegetation. Williams, W. T. and Lambert, J. M. (1969). J . Ecol. 47, 83-101. Multivariate methods in plant ecology. I. Association-analysis in plant communities. Williams, W. T. and Lambert, J. M. (1960). J . Ecol. 48, 689-710. Multivariate methods in plant ecology. 11. The use of an electronic digital computer for association-analysis. Wolf, F. A. and Wolf, F. T. (1947). “The Fungi.” 2 vols. Wiley, New York.

This Page Intentionally Left Blank

Ecological Conditions Affecting the Production of Wild Herbivorous Mammals on Grasslands A . DE VOS

Forestry and Forest Industries Division F.A.O., Rome, Italy

.

I. Introduction 11. Basic Ecological Considerations 111. Definitions . IV. Descriptions of Grasslands and Savannaa A. The North American Grassland Biome . B. The African Grassland Biome . V. The Ecology of Drought Cycles VI. The Ecology of Fire . A. Environmental Alteration . B. Effects on the Vegetation C. Effects on Animals . D. Changes in Productivity of the Vegetation VII. Animal Influences on the Grassland Environment . A. The Effects of Wild Ungulates on Grasslands B. The Role of Rodents and Lagomorphs in Altering the Grassland Ecosystem . C. The Role of Rodent Mounds and Termitaria . VIII. Biomass and Energy Production of Herbivorous Mammals A. Basic Considerations . . B. Available Evidence on Productivity C. A Comparison between Africa and North America in Terms of Biomass Production . D. The Effects of Degradation of the Environment on the Productivity of Wild Herbivorous Mammals . IX. Management Considerations . A. Game Ranching and Utilization . B. Range Management for Wild and Domestic Herbivores . X. Recommendations and Research . Summary and Conclusions . References .

.

.

.

.

.

.

.

137 138 140 141 143 144 146 147 147 148 149 149 150 151 155 160 163 163 166 169 170 171 171 174 177 177 179

I. I N T R O D U C T I O N During recent years, with an ever-increasing protein scarcity in the world as a result of rapidly expanding human populations, there has been much discussion, mostly among biologists, about the possibility 137

138

A. DE VOS

of a rational exploitation of wild herbivorous mammals for their meat and other products. Many statements have been made about the actual and potential production of wild herbivores and about the economic and social problems athached to the harvesting of these animals. In this paper an effort will be made to review various ecological considerations dealing with energy production in natural grasslands, culminating in the production of mammals, and to point out how carefully data must be collected, interpreted and applied. The influences of light, temperature and soils will not be discussed, since these factors have already been reviewed. I n this paper stress will be laid on the need for conservation and management of unimproved grasslands and for a variety of wild herbivorous mammals to make optimum use of these lands. Considering the voluminous and scattered literature on the subject, I have found it impossible to deal with all of the world’s grasslands. Rather, I have emphasized a comparison between the grasslands of North America and Africa, based on selected literature and first-hand knowledge. However, where pertinent, reference is made to Russian literature.

11. BASIC ECOLOGICAL CONSIDERATIONS Grasslands are complex biotic communities. Although an effort is made to stress the complicated interactions of various physical and biotic factors, and between various organisms and species, it is impossible to discuss inter-relationships at all levels in this review. Stress is laid mainly on the interactions of mammals, although it is realized that other vertebrates, invertebrates and plants also play an important, and sometimes a dominant role in these inter-relationships. Grasslands are typical of continental climates throughout the world, of the rank of biome, having throughout a common physiognomy, a constant growth form on the part of their dominants, a similar ecological structure, essentially similar climographic patterns, and a homogeneity of the larger predominant forms in most areas (Carpenter, 1940). Ungulates, rodents and lagomorphs are major consumers of the vegetation. They in turn are consumed by the predators. Ecological niches of several species may overlap to various degrees, hence active competition may occur. I n certain instances, a niche may remain unoccupied or partly occupied through the non-availability of suitable forms. The amount of energy that is produced and consumed is, of course, an important consideration. The degree to which energy is utilized in any biotic community

Composition of vegetation

T p to seven metrcs by giraffes and elephants BROWSISG

Up to two nictres b y

ib-1

movements

t-p to onc metre by small antelopes

Termitaria or rodent mounds affect physiography, ecology and productivity of landscape Grassy or woody vegetation on deserted termitaria

and laeomorohs a t eround levcl

1A&-

-.

ISoil structure BUHROWIXO ACTIVITIES O F

i1

(Soil structure

Soil aeration

BODENTS A S D TERMITES I AFFECT Soil

AFFECT

fertility

Surface erosion (Soil fertility

I

(Organic matter content

FIO.1. Biological and physical interactions in a grassland environment.

.

A , - .

140

A. DE VOS

affects the food web. These webs may be highly involved on range where game animals compete for a more or less common food supply (Costello, 1957). The biological and physical interactions in a grassland environment are schematically represented in Fig. 1. Rodent mounds and termitaria affect both the physiography and the ecology of the landscape and are themselves affected by these factors (Fig. 2 ) . Fires affect the composition

FIQ.2. A Topi (Damaliacus korrigum) on a termitarium on a long grass plain in the Serengeti National Park. Topis use termitaria as look-out posts. Photo by A. de Vos.

of the vegetation, the food available to herbivores and animal movements above ground, and soil conditions below ground level. While ungulates, rodents and lagomorphs affect the vegetation a t and above ground level by their grazing activities, browsing and barking is done a t various levels above ground by various groups of mammals. The burrowing activities of rodents and termites affect the soil structure, soil aeration, soil fertility and organic matter content. It can be readily visualized that the interaction of these various factors is complicated.

I1I. D E F I N I T I o N s Since a number of different terms are employed for the same concept, whilst the same term is used by different authors to mean different things, it is essential that the vnrious terms used in this paper be understood as meant by the author. These terms will be defined briefly. Production, as used in this paper, is defined as the amount, in kg,

PRODUCTION O F WILD HERBIVOROUS MAMMALS

141

of organic matter (i.e. animals) produced per unit area per unit

time. Standing crop (Biomass)is expressed as the weight of living individuals (including skeletons, horns etc.) forming a population or of populations forming a community per unit area present a t a given time. It is usually expressed in kg/ha or in g/m2. Weight may be expressed as dry or liveweight. Carrying capacity is the ability of a given area of land to support a certain population of animals on a continued basis. Range condition is the status of the range at a given time. Ecological eficiency is the ratio of assimilated energy to ingested energy within one species or a group of species belonging to the same trophic level.

Iv. DESCRIPTIONS O F GRASSLANDS AND

SAVANNAS

Since grasslands cover very large areas and provide pastures for grazing animals, they are important to man’s economy. The prairies of North America, the pampas of South America, the savannas and other grassland communities of the high plateau of South Africa and parts of Central and East Africa, the Mulga-Spinafex desert of Australia and portions of the steppes of Russia are all “grasslands’’. The term “grassland”, as used in this paper, includes any herbdominated vegetation. Little purpose seems to be served by not classifying savannas as grasslands. A more useful classification may be into natural grasslands, secondary grasslands (including derived grasslands) and wooded grasslands. The ecology of grasslands has been reviewed in detail by Hanson (1938, 1950). Many theories have been advanced about what environmental factors cause the existence or development of grasslands. The following factors have been suggested: 1. Climatic, based on moisture deficiency and alternating wet and dry seasons. 2. Biotic, based mostly on man’s activity. Herbivorous animals have affected the evolution of plant species and also the availability and distribution of grassland vegetation has affected the evolution of these animals. 3. Pedological, based on chemical deficiency in the soil. No single factor may be responsible for grassland formation, but rather this may be the result of the combined action of several adverse factors, although one of them may play a dominant role. 4. Fire. There is still much controversy about the extent of grasslands before man became an ecological dominant through the use of fire. Most botanists agree, however, that man has extended

142

A. D E VOS

grasslands by a considerable amount, and that the area of grassland would be much reduced if he discontinued the use of fire. Grasslande are generally characterized by distinct wet and dry seasons. For instance, in the temperate zone of the northern hemisphere grasses mature in the summer and fall. There is a drought period in the summer and a cold rest period in the winter. On most of these areas fire has been a natural factor, set by lightning. Fire is often used by the nomadic primitive peoples to aid in hunting or to improve the accessibility of green grass in spring (Shantz, 1940). The various formations that are, unsatisfactorily, named “savannas” result from the relative abundance of diverse life forms which compose them, from the structure in which these life forms are arranged and their relationships with animals all in a way that constitutes a biome. In addition to the grasses and other herbs, trees and woody plants are normally present; it is grassland with mostly xerophilous vegetation and scattered shrubs and trees. Savannas are often derived from pre-existent forest. However, scrub savanna can also arise from the deterioration of grassland and bush encroachment. Savanna vegetation is generally in two layers. The lower, grass layer is often a complex structure of many species of grasses and forbs with a variety of growth forms and seasonal growth patterns, making highly efficient use of the ground surface, light, and limited water. When present, the upper, woody layer may be composed of a variety of woody shrubs or trees. Secondary grasslands may arise as a result of climatic changes, but they are mostly man induced and maintained by fire. They never offer an equally satisfactory environment to large herds of herbivorous animals as the natural grasslands. There are apparently several reasons for this. First, the indigenous fauna may not be adapted to the changed vegetation, and a suitable immigrant fauna may not be available. Second, seasonal movements may be restricted and as a result the varying needs of the animals are not satisfied and the resulting overgrazing damages the herbage. Finally, the grazing spectrum is not likely to be balanced, and therefore full and efficient use cannot be made of the secondary grasslands (Vesey-Fitzgerald, 1963). Some African savannas support the world’s most abundant and varied wild animal populations. These are extraordinary examples of complex ecological responses and adaptation. I n general, rainfall is relatively low in these plant communities, with very irregular distribution and occurrence, and, therefore, there may be times of food scarcity when temperature and evaporation are very high. Although an often rich vegetation has developed under this climatic regime, this vegetation is in sensitive balance with the limited water supply and is particularly

PRODUCTION O F WILD HERBIVOROUS MAMMALS

143

vulnerable to desiccation caused by factors such as overgrazing (Talbot, 1963).

A.

THE NORTH AMERICAN GRASSLAND B I O M E

The North American grassland biome has been well described by Carpenter (1940). Three climax grassland types or associations are usually recognized, namely the Tall-Grass Prairie Association; the Mixed-Grass Prairie-Plains Association, and the Short-Grass-Plains Association. The grasses become progressively shorter westward as mainly determined by decreasing precipitation. The nearctic grasslands cover an area which shows many East-West and North-South variations. The Short-Grass-Plains Association is the most xeric of the communities of the biome. A good description of the North American prairie is given by Weaver and Fitzpatrick (1934): “The prairie is a community of great complexity. Variations in its structure result from differences in regional precipitation, local differences in habitat factors, and from changes brought about by the advance of the seasons. All of the dominant and nearly all of the subdominant species are perennials. Climax prairie is a closed community; the water content and light are so fully utilized that few seedlings of native species exist and invaders are excluded. Reproduction is largely vegetative. “Competition for light has resulted in layering. Certain forbs always remain near the surface of the soil; some with long, erect stems are leafy only above the grasses; others produce much foliage from soil surface to leafy top; often reaching a greater height than grasses.” The composition of the grassland community, including floristics and structure, as well as the resulting physiognomy, has been reviewed by Hanson (1950). Stratification of North American grasslands, particularly of aboveground parts, has been described in many papers. Two or more layers frequently occur. The uppermost layer sometimes suppresses the other layers. Sagebrush, e.g. when it covers substantial areas of the ground, has a suppressing influence on the other plants. The following are among the dominant genera: 1. Tall-Grass Prairie Association-Andropogon, Panicum, and Spartina. 2. Mixed-Grass Prairie Plains Association-Andropogon, Stipa, Sporo-

bolus, and Agropyron. 3. Short-Grass Plains Association-Buchloe,

Boutelow, and Poa.

Forbs generally are present., but do not produce much biomass in climax grasslands.

144

A . DE VOS

Some of the more prominent mammals which once ranged throughout the biome, and hence bound it into an ecologic unit, include the Bison (Bison bison), Pronghorn Antelope (Antilocapra arnericana), Wolf (Canis lupus), Badger (Taxidea taxus) Prairie Dogs (Cynomys)and the two Jack Rabbits (Lepus spp.). Plant composition has been greatly modified since the introduction of domestic stock. I n the desert plain grassland in the American South-West, desert and semi-desert shrubs, though always present, have undoubtedly greatly increased their range and abundance as a result of lessened grass competition, the grasses having suffered more from heavy grazing than shrubs (Whitfield and Beutner, 1938).

B.

THE AFRICAN GRASSLAND BIOME

The grassland pattern of Africa includes: (a) the climatically controlled, grazing modified grass plains of East Africa, (b) the valley grasslands of Central Africa and (c) the secondary fire-controlled grasslands (Vesey-Fitzgerald, 1963). Rattray (1960) has described the grass cover of Africa. The major grass associations often contain a number of communities, some of which may be edaphic variations or have resulted from differences in aspect, while others may represent various stages in the succession as a result of biotic influences. Many of these communities are very mixed and consist of a varying number of genera and species, one or more of which may be locally dominant. The result is a type of grass cover which a t first sight may appear to be merely a mosaic of small communities or colonies, but in which one or more grames may usually be found which are distributed in such a way as to characterize the whole association. The Hyparrhenia type, for example, which covers a considerable portion of Africa, is made up of a large number of different grasses, but species of Hyparrhenia itself are usually so much in evidence that it would be difficult to find another more suitable genus with which to characterize this type (Rattray, 1960).

Anderson and Talbot (1965) show that wind erosion and soil depth, texture and salt concentration, all of which affect moisture availability, largely determine the grassland patterns. I n East Africa there are seasonal changes in the weather, hence green flushes of herbage are also seasonal. Nevertheless, the dry grass is often nutritious, but its utilization necessitates access to surface water for many species of animals. These considerations necessitate periodic migrations from one grassland area to another. The major classification of grasslands in East Africa is illustrated in Table I.

PRODUCTION O F WILD HERBIVOROUS MAMMALS

145

TABLEI Grassland types in East Africa (from Heady, 1960) Grassland types

Location

Themeda-Hyparrhenia Wide range of plant (scattered-tree groupings, between grassland) 1200 and 2333 m Chrysopogon-Chloris- Elevations below Aristida (desert 1333 m grass- bush) Aristida Below 833 m

Highland grass and forests

Betweon 2166 and 3166 m

Pennisetum purpureum (elephant grass)

Between 1000 and 1666 m

Hyparrhenia types Wide variety of eleva(seven divisions are tion and rainfall recognized) I n Tanzania; subject to Mbuga grassland seasonal flooding Panicum-Digitaria

Coastal strip of Kenya

Panicum

Coastal strip of Kenya

Rainfall

Most important grasses

5 6 8 6 . 5 cm

Themeda triandra, Hyparrhenia fillipenduh 62-5 cm Chrysopogon aucheri, Long, irregular Chlwis myriostachya, drought periods Aristida papposa. 25-37.5 cm Aristida papposa, T etrapogon spatheus, Enneupogon cenchroides, Cenchrus Dactyloctenium. 87.5-225 cm Themeda triandra, Penniaetum schimperi, E l e k n e jaegeri. 112-5 cm Loudetia kagerenaia, Hyparrhenia spp., Cymbopogon, Brachiaria, Imperata, Melinis, Setaria, Sorghum. Many associated grass species. Many species, including waterloving ones. Many species with affinities both to wetter and drier areas. Composition varied both to dominance and species.

In Central Africa the climate is also seasonal and the quality of the pasture, and the availability of water, vary accordingly. The fauna of the edaphic valley grasslands is adapted to these contingencies. Floods exclude the main herds of herbivorous mammals from much of the area for about half the year. For much of the other half of the year, the flood plains are covered by rank unpalatable grasses. The valley grasses are perennial, and fresh green shoots grow from ground level during the dry season. Seasonal movements by herds of herbivores are affected by

146

A. DE VOS

these changes and this culminates in both a wet season and a dry season concentration of game. Grasses belonging to the genera Panicum, Pennisetum, Adropogon, Therneda and Hyparrhenia provide the dominant cover in both East and Central Africa.

V. T H E ECOLOGY OF DROUGHT CYCLES Existence on grasslands has for both plants and animals been one of adjustment to wet and dry cycles in the weather. During wet periods vegetation thrives and develops to a maximum, but after drought conditions, the more mesic plants have disappeared except in favoured places. Because of these adjustments, density of vegetation is greatly reduced (Albertson et al., 1957). Decrease in density continues until drought is broken and the soil is again sufficiently moist to support vigorous growth of vegetation. Then, if enough live growth remains, the cover of living plants is quickly restored. However, if cover is mostly gone, the process of secondary succession is greatly lengthened. It is obvious that grasslands, weakened by overgrazing during wet cycles, are extremely sensitive to deficient soil moisture when drought strikes. Loss of vegetative cover on heavily grazed ranges in the Central Great Plains of the United States often was nearly double that on those moderately grazed and frequently more than double the amount on the nongrazed grasslands. The reason why overgrazing is so destructive to rangeland seems to lie largely in the degree to which the plant production is affected. Growth of tops and roots cannot occur unless there is a food reserve which can be used in the growing process (Albertson et al., 1957). Drought, like overgrazing and, under certain conditions, burning, reduces the vigour of grasses and therefore causes similar vegetational changes. One major factor affecting the influence of drought is the degree of root development of the component species. Those with weakly or moderately developed root systems are usually the most sensitive to drought and grazing pressure. Drought may precipitate animal movements. Bronson and Tiemeier (1959) showed that when drought and overgrazing depleted the food supply in a sand-hill region in Kansas, jack rabbits migrated to the edge of the region in search of food. I n Africa droughts induce the movements of many plains inhabiting ungulates. Death of grasses by droughts varies with soil depth. Prairies on the deep loess soil of south-western Iowa as well as some north-eastward on the glacial soils were not harmed by the severe drought of 1934. Death

PRODUCTION O F WILD HERBIVOROUS MAMMALS

147

by drought increased south-eastward, ranging from 20 to 60% on thinner soils of exposed ridges to 80-96% losses on nearly level areas farther west (Weaver and Albertson, 1936). Erosion cycles are tied in closely with drought cycles. After prolonged periods of drought and especially under conditions of overgrazing erosion increases. On the other hand, a series of wet years results in increased vegetative cover and a reduction of erosion.

VI. THE ECOLOQY O F FIRE The effects of fire on the vegetation and soils in tropical and subtropical areas have been reviewed by West (1965) and Bartlett (1965). Daubenmire (1968) has reviewed the ecology of fire in grasslands comprehensively. The fire-setting activities of man perforce brought about deep and lasting modifications in what we might call “natural vegetation”, a term that may conceal long and steady pressure by human action on plant assemblages (Sauer, 1950). A surprisingly large portion of natural vegetation owes much of its character to the frequency of man-induced fires (Daubenmire, 1968). Fires have always been a part of ecosystems, but in the past two thousand years the development of human communities and more recently the invention of safety matches have accelerated the effect of fire upon the African landscape. Fire and shifting cultivation are unquestionably the major factors responsible for the formation and maintenance of most grassland country. Because fires have exerted such a profound influence on the vegetation of Africa for so long, they have become an important environmental factor almost equal in effect to topography and climate. Infrequent and therefore hot fires, because of accumulated vegetation and litter, maintain grasslands because shrubs are suppressed by the hot fire. Frequent fires are not hot enough to kill shrubs and young trees because there is an inadequate accumulation of fuel. Riney (1964) gives evidence that frequent fires can eliminate perennial grassland, encouraging scrub invasion and annual grasses. A.

ENVIRONMENTAL ALTERATION

Fires injure plant communities to a greater or lesser degree. However, fires are not always detrimental. Under the right circumstancesdesirable effects can be maximized, with undesirable influences prevented or at least kept to an innocuous level (Daubenmire, 1968). The effectiveness of fire in producing and maintaining grassland is

148

A. DE VOS

dependent on the season of the burn, on its intensity, and on the degree of tolerance towards fire exhibited by the woody elements of the vegetation (West, 1965). The intensity of a f i e depends to a large extent on the sum of combustible products either standing or accumulated in the form of litter. The relative effects of fires will vary with the inherent vigour of the grasses and hence with soil fertility, climate, etc. In nearly every influence of burning, the time of the year, or even the time of day when the fire occurs is almost as important as the occurrence of the fire itself (Daubenmire, 1968). Drastic changes in microclimate a t the soil-atmosphere interface are brought about by burning a stand of grass. Post-burn microclimate may favour frost damage to seedlings, especially since it often hastens spring germination (Daubenmire, 1968). In some geographic areas burning at certain seasons increases humus whereas under other circumstances it is reduced. After a fire, and before a new herbaceous cover develops, the blackened and unshaded soil is appreciably warmer, at least during daytime, in comparison with unburned areas. Presumably in consequence of this the foliage usually appears earlier in the first post-burn season, and sometimes the onset of flowering is advanced. Whether humus increases or decreases in consequence of repeated grass fires, or whether erosion is accelerated or not varies from place to place, but these seem constant for a given region and vegetation type (Daubenmire, 1968). Burning can result in greatly increased run-off and erosion, the magnitude of the effect depending on the extent to which the protective vegetative cover has been removed. Reduced shade allows the soil surface to dry readily, and this keeps microbial activity to a minimum (Dix, 1960). Some of the changes induced by burning grassland tend to reduce soil moisture, whereas others favour an increase.

B.

E F F E C T S ON T H E VEGETATION

The degree of modification of the vegetation that might be expected should be a function of the frequency of fires multiplied by the time period involved, i.e. the more often fires have occurred in a specific area and the longer the vegetation has been subjected to frequent fires, the greater the degree of modification (Humphrey, 1962). Because fire is such a dominant environmental factor in grassland environments, many plants have become fire resistant. Fire does not occur at the same frequency in all vegetational types and this has led to differences in types and degrees of fire tolerance among various species of plants.

PRODUCTION OF WILD HERBIVOROUS MAMMALS

149

Fire commonly favours forbs over grasses in both annual and perennial grassland. I n annual grassland the effect of fire is usually to reduce density in consequence of destroying a portion of the current seed crop. The composition of plant communities can be materially altered. If perennial plants have already started growth at the time of the fire, or if the perennating buds are at or near the soil surface, the plants may be injured or killed by burning. Whereas some perennials are killed and others are essentially unaffected by fire, a great many are conspicuously stimulated, such as initiating flowering activity. Fire has varied effects on the subsequent size of the vegetative organs (Daubenmire, 1968). Recurrent fires can be devastating to grasslands. Perennial grassland has been destroyed experimentally at Matapos in Rhodesia by recurrent fires (Child, personal communication).

c. E F F E C T S

ON A N I MALS

Fires can affect animals by killing them or by removing essential cover, or by affecting the available food supply. Fire can be devastating to ground-nesting birds. It not only destroys existing nests but removes the protective cover necessary for constructing new ones, and eliminates insect food resources. The loss by fire of essential food and cover is catastrophic for populations of mice and other small rodents. However, most of these animals rear their young in burrows which give them a measure of immunity from fire. I n western Minnesota optimal habitat for grasshoppers (Orthoptera) is provided by vegetation recovering from a burn, rather than by freshly burned or by long-unburned vegetation (Tester and Marshall, 1961).

Burning has an immediate effect upon the food supplies and the breeding season of birds and mammals. The attractiveness of new grass on recent burns for hooved grazing animals is well known. This is likely for two reasons: ( 1 ) the higher nutritious value of the new herbage, and (2) the absence of less nutritious and less palatable old leaves. D.

CHANQES I N PRODUCTIVITY OF THE VEGETATION

The effect of fire on production shows a remarkable consistency within a geographic region, with wide differences between regions. I n Africa, burning increases production in relatively moist regions, but is generally detrimental in more arid regions. The production of herbaceous

160

A. DE VOS

vegetation may be increased or reduced in consequence of burning, the latter result often being associated with an inopportune timing of the fire in relation to phenology, or with a very dry climate (Daubenmire, 1968).

I n new grass appearing after a fire, indigestible material is usually reduced, with food and minerals increased. Protein and mineral contents of post-burn grass shoots are higher, so the herbage is much more nutritious for animals (Daubenmire, 1968). Where animals have unrestricted access to the new growth on a burn they tend to keep it eaten down to the ground surface, which severely taxes the root reserves and jeopardizes the possibility of recovery. Fire that otherwise might stimulate increased productivity can in this way be indirectly devastating to grass.

V I I . ANIMALINFLUENCES O N T H E GRASSLAND ENVIRONMENT Grasslands are the basic grazing resource for herbivorous animals. Some plants are palatable and eaten, while others are not. Some plants replace others when changes occur in the complex of climate, soil, grazing and fire under use by man. The replacement may be toward or away from a vegetation that sustains the highest animal population (Heady, 1960). Grazing is one of the most important modifying forces in a grassland environment. The amount of grazing affects the subsequent yield of range by affecting the physiological systems of plants and their local environment. Grazing reduces photosynthetic processes by removing green leaves and it may damage growing stems and thereby prevent flowering, seeding and, therefore, regeneration of some species. Grazing, by removing the taller growing species, gives opportunity for plants in ower strata to increase in abundance. The relations of range animals and plants are complex and poorly understood. The reciprocal relations between the effects of animals upon the range, and of range condition on the abundance of these animals, vary greatly with circumstances. Animals do play an important part in the transformation of the environment and their activity contributes to changes in the vegetation. The composition of a plant community is affected by the kinds of animals grazing it, because Werent species have different preferences. Generally, herbivorous ungulates, lagomorphs and rodents form the more active element of the grassland biocenosis. The evolution of grassland associations has proceeded under the continuous influence of

PRODUCTION OF WILD HERBIVOROUS MAMMALS

161

these animals. Their primary influences on their surroundings are frequently much farther reaching than the mere devouring of the vegetation which characterizes their habitats. Trampling, if the animals are large, and then cutting of the sod with their hoofs, can modify the habitat considerably. Grazing animals accidentally plant seeds of many species by trampling them into the ground. The physiography of grassland areas can also be profoundly affected by animals. Not only grazing mammals affect the vegetation but ants, crickets, grasshoppers and termites also have a significant effect when they become so abundant as to consume large amounts of food. Then there are also indirect effects by animals.

A.

THE EFFECTS OF WILD UNGULATES ON GRASSLANDS

Grazing animals affect each other and range vegetation almost continuously. The effects of wild ungulates on grasslands are many and complicated. Elton (1966, p. 378) stated the following about the effects of herbivores on their biotic environment: “A whole series of secondary patterns have been forming, this time through the activities of the animals themselves, which may in turn create new secondary patterns in the vegetation. Thus when a powerful polyphagous herbivore like the cow feeding fairly randomly on a newly occupied pasture deposits its large parcels of dung, a new pattern is set up that has two main effects on the pasture system: the numerous scattered cow-pats attract a rich special community of animals, and they also alter the pattern of grass subsequently growing on the patches so that cattle tend to avoid feeding on them.” Herbivores graze particular plants or prefer some plant communities to others. They generally select leaves in preference to stems, and green matter in preference to dry material. The effect of selective grazing is commonly to reduce the proportion of palatable species. Successional trends of the vegetation are roughly proportional to grazing intensity; they are pronounced under severe grazing, and in some instancep difficult to distinguish at light or moderate levels (Ellison, 1960). Removal of fuel by grazing must be reckoned a factor in reducing the incidence of fires. When excessive numbers or concentrations occur, trampling or overgrazing may destroy the vegetation. Trampling into the earth of the seeds of different plants may be beneficial for the maintenance of an equilibrium between the different species constituting the plant covering. Localized heavy trampling may cause enough denudation of the vegetation that erosion sets in, creating a small hollow. Such a hollow

152

A. DE VOS

may be enlarged by pawing and wallowing activities of ungulates. Ultimately large enough hollows may be created in grasslands in East Africa to contain sufficient water after the rainy season to aid substantially in the water supply for herbivores. The elephant is the most dominant among terrestrial mammals. I t changes the environment by such activities as digging waterholes and pushing down trees, making areas more habitable for other animals. Many species of animals concentrate in large herds on favoured range and this habit appears to be beneficial for the production of herbage. The trampling and cropping by these animals not only tends to keep it in a state of active growth, and so incidentally retards maturity, but also arrests the normal course of succession. Trampling, followed by continued use, especially by close-grazing species, eventually reduces the long grass stands and causes the range to resemble a vast green lawn (Vesey-Fitzgerald, 1965). This is not true in all cases, especially on sandy soils where rainfall is limited and erratic. When extensive range areas are reduced to a short grass sward, it is probable that full utilization has been achieved. It is dangerous to generalize too much about this, since full utilization could represent overgrazing, leading to a shift in species composition favouring stoloniferous grasses. Large numbers of grazing animals may under certain circumstances cause grassland to spread by preventing woody regrowth so that when the mature woody component of the vegetation dies, there is no replacement. The primary productivity of grassland will depend on the grazing pressure, since the activities of the grazing animals will normally add fertilizer, reduce light interception by foliage, stimulate leaf regeneration, and reduce the growth of roots. There is presumably an optimum grazing pressure that will extract the highest yield from any particular pasture (Crisp, 1964). Fire incidence and/or grazing pressure have the effect of reducing the vegetation as a whole to an earlier stage in succession, but the growth of plants themselves is stimulated meanwhile. Grazing and trampling in long grass stands increases the short grass areas. Thus wild animals may modify their pastures to their own advantage (VeseyFitzgerald, 1963). This is, e.g., the case for wildebeest. Wild ungulates in an undisturbed savanna ecosystem have preferred diets which are complementary to one another.These diets involve both different plant species and different growth stages of the same plants. Therefore, all parts of the available vegetation contribute efficiently to support the biomass of mixed wild ungulates (Talbot, 1963). For instance, in a grassland environment jointly used by various species,

PRODUCTION OF WILD HERBIVOROUS MAMMALS

153

zebra select mainly the stems of grasses at the top level of the herb layer, wildebeest prefer mainly to eat leaves in the middle of the herb layer, and Thornson’s gazelles eat the low grasses and leaves of dicotyledons. Different species of animals eat different classes of food. Giraffes, for example, feed lkrgely on trees; rhinoceros feed largely on brush; while wildebeest almost exclusively eat grass. Removal of accumulated dry litter by grazing makes new grass growth more available to grazing animals. However, frequently much plant material remains free from herbivore use altogether, which becomes important with respect to the intensity of fire. Brief mention should be made of a physical effect of ungulates on their environment, that may in turn affect their movements. Weir (1962) has described that the origin of water holes in Rhodesia is attributable in many cases to the direct action of herds of large mammals. These animals, in turn, are inclined to remain around these pans, rather than move off, when the range dries up.

1. The eflects of overgrazing When herbivores are allowed to increase with little or no control they may seriously overgraze a range. Overgrazing has been described succinctly by Weaver and Clements (1938) as follows: “The more palatable species are eaten down, thus rendering the uneaten ones more conspicuous. This quickly throws the advantage in competition to the side of the latter. Because of more water and light, their growth is greatly increased. They are enabled to store more food in their propagative organs as well as to produce more seed. The grazed species are correspondingly handicapped in all these respects by the increase of the less palatable species, and the grasses are further weakened by trampling as stock wanders about in search of food. Soon bare spots appear that are colonized by weeds or weedlike species.”

Grazing pressure affects the availability of cover, which is essential for many species of herbivorous animals. The heavier the grazing pressure, the more severe the loss of cover. Heavy grazing should not be confused with overgrazing. Heavy grazing may actually be advantageous because the fullest use will be made of the growing vegetation. The term “overgrazing” implies harm caused by animals to both the range and individual plants, as well as to the soil. Erosion may result and dust may settle on the vegetation, reducing photosynthesis. Chronic overgrazing inevitably modifies the original cover (often irreversibly) and allows a replacement by plants whose requirements

154

A. DE VOS

are lower, or which otherwise evade the effects of overgrazing. This results in a smaller turnover of organic matter, reduced rainfall infltration (with a corresponding increase in run-off and erosion), increasing flood hazards, and other possible modifications of the environment. Animal responses under these circumstances may be characterized-to an extent depending upon the degree of stress-by slow growth, low birthrate and above average mortality. During drought, or any other period of additional stress, losses may be severe, so that in arid and semi-arid regions animal populations fluctuate excessively (Peterson, 1967). Some species may respond favourably to these changes, however, at least temporarily. Smith (1940) showed that early and continuous overgrazing depletes the reserves of perennial grasses, thus eventually killing them. As a result, the area formerly occupied by the taller perennial plants may be occupied (a) by perennials or annuals less edible or palatable, or (b) ones which cannot be so carefully grazed off such as the short grasses, or (c) if these are lacking, then erosion may remove the rich topsoil, thus preventing the original vegetation from returning before certain changes have been wrought by subclimax species. Plant composition has been greatly modified since the introduction of domestic stock, partly resulting from over-use of the range. In the desert plain grassland in the American southwest, desert and semi-desert shrub, though always present, have undoubtedly greatly increased their range and abundance as a result of lessened grass competition, the grasses having suffered more from heavy grazing than shrubs (Whitfield and Beutner, 1938). Observations in Utah by Pickford (1932) on areas subjected to heavy grazing showed in every case a serious depletion of perennial grasses, a decided increase in density of sagebrush, in some instances a sharp increase in the density of poor perennial weeds and annual grasses, and a decrease in the total plant density. These vegetational changes have resulted in reductions of 40-75% in the grazing capacity of the areas studied. Similar changes are widespread in southern Africa where overgrazing by sheep (also possibly Hyrax; Procavia capensis) seems to be the main factor. Owing to its likelihood of becoming overgrazed and eroded, the range is probably more subject to imbalance than any other natural community. Much more emphasis is needed on this concept, and particularly its application to maintenance and improvement of the range resource (Costello, 1957). Differential use of plant species affects the competitive abilities of practically all plants on the range. As a general rule, the less desirable species are favoured by continued heavy grazing. Successful competition

PRODUCTION OF WILD HERBIVOROUS MAMMALS

155

by undesirable species causes retrogression in range condition (Costello, 1957).

Noxious plants and high populations of certain rodents are frequently manifestations of overgrazing. Where serious competition between large rodents, lagomorphs and cattle grazing exists, it is usually for a very inferior type of forage. Pocket gophers appear to be favoured by a degree of overgrazing that permits extensive replacement of perennial grasses by perennial and annual forbs (Buechner, 1942). Pellet counts of various common rodents and lagomorphs by Phillips (1936) in Oklahoma indicated that jack rabbits were most abundant in moderately overgrazed areas. Trapping showed that Deer Mice (Peromyscus maniculatus) were most numerous in moderately overgrazed grassland while Cotton Rats (Sigmodon hispidus texianus) were almost entirely restricted to heavily grassed areas (Phillips, 1936). Areas overgrazed by hippopotamus in the Queen Elizabeth National Park, Uganda, are inhabited by larger numbers of wart hogs than areas where grazing pressure is low (G. Clough, personal communication). Overgrazing enables grasshoppers to increase enormously in abundance. However, when the cover is reduced so greatly that erosion becomes marked, numbers of grasshoppers decline (Smith, 1940). Overgrazing also appears to cause the number of termite mounds to decrease (Murray, 1938).

B.

T H E ROLE O F R O D E N T S A N D LAQOMORPHS I N ALTERING THE GRASSLAND ECOSYSTEM

I will summarize pertinent literature on the effects of rodents and lagomorphs on grassland areas in North America and the ecological importance of their activities to various other animals, in the hope that this will stimulate comparable studies in Africa. Bond (1945), Humphrey (1962) and Kalmbach (1948) have reviewed the information for North America. Very little is known about the pristine populations of the various grassland-inhabiting rodents of North America. Koford (1960, p. 327) contends that the prairie dog was the most characteristic animal of the Great Plains physiographic province. Burpee (1908, p. 104) referred to numerous “marmot” burrows, which according to the location of sighting, were more likely produced by ground squirrels. Although many papers have been written about various rodents frequenting the grasslands, relatively little has been published on the effects of these mammals on their environment. A number of authors

156

A. DE VOS

attribute certain environmental changes to these animals, but most of them provide little evidence to substantiate their claim.

1. Effects on soil and soil conditions Burrowing rodents have constructive as well as destructive influences on the soil. The most conspicuous activity of rodents is their burrowing, through which they bring loose soil material to the surface and, in varying degrees, honeycomb the subsurface with a network of passages. The Pocket Gopher (Thomomys talpoides) may bring five tons of earth per acre to the surface in one year (Ellison, 1946). A number of authors have maintained that the various burrowing rodents contribute significantly to the aeration of the soil (Grinnell, 1923, pp. 144-145; Taylor, 1930, p. 539; Koford, 1960, p. 339). Aeration is important in aiding microbiological processes, such as the rapid decomposition of organic matter, the promotion of good growth of higher plants, and so on (Buckman and Brady, 1962, pp. 148-152). Some authors have also asserted that the burrowing activities of rodents contribute to a loosening of the soil (Grinnell, 1923, pp.144-145; Taylor, 1930, p. 539; Ellison, 1946, p. 113; Koford, 1960, p. 332). Others tend to comminute the soil, thus producing a larger percentage of finer soil particles (Greene and Murphy, 1932, as cited by Reynolds, 1958, p. 123). Whatever happens also depends on the soil itself. Some authors consider the loosening of the soil as significant in increasing porosity and thus the percolation or infiltration of water and local drainage (Grinnell, 1923, pp. 144-145; Taylor, 1930, p. 539; Ellison, 1946, p. 113; Evans, 1951, p. 448; Koford, 1960, p. 332). Reynolds (1958, p. 123) points out however, that some rodents such as the Merriam Kangaroo Rat (Dipodomys merriami Mearns) affect such a small area by their burrowing, that the effect of increased infiltration would be negligible. With regard to the loosening of the soil, increasing water-holding capacity, Koford (1960, p. 332) asserts that this is the case with prairie dog mounds, which tend to preserve moisture in the underlying soil. Rodents may accelerate weathering of the soil by allowing greater air and water penetration of the subsoil (Grinnell, 1923, pp. 144-145; Koford, 1960, p. 332), or by bringing subsoil to the surface and thus exposing it directly to the elements (Grinnell, 1923, pp. 144-145; Ellison, 1946, p. 113). The bringing of loose material to the surface by burrowing rodents has been cited as a means of accelerating erosion. However, most writers hasten to point out that the burrowing activity of rodents is probably not a primary cause of erosion but rather an aggravation of

PRODUCTION O F WILD HERBIVOROUS MAMMALS

157

an existing process induced by man’s abuse of the land (Ellison, 1946, p. 113; Koford, 1960, p. 333), and directly related to degree of range depletion from overgrazing. The burrowing activities of rodents can aid in incorporating humus into the soil and their faeces, urine and dead bodies also tend to enrich the soil. The weight of Jack Rabbit (Lepus califmnicus) pellets in Arizona was found to average over 6.6 kg/ha (Vorhiesand Taylor, 1933). Some rodents take great quantities of plants into their holes for nesting material and food. The movement of parent material to the surface by rodents and the subsequent weathering of this material can also increase the availability of various nutrients and thus enhance soil fertility. The soil thrown out upon the surface is, as a rule, less alkaline, richer in mineral salts and poorer in humus.

2. Effects on the vegetation Rodents and lagomorphs may affect the vegetation in a number of ways, ‘thus competing with other forms of wildlife. Under certain circumstances they build up high population densities which consume and destroy considerable quantities of food otherwise available to ungulates. These mammals may, therefore, be in direct competition with ungulates. The forage lost through kangaroo rats much exceeds the quantity actually eaten by them. I n an enclosure stocked at the rate of 13 kangaroo rats per ha, the decreased yield was such that a destruction of five kg (dry weight) for each animal was indicated during the seven-month growing season, with some further loss during the dry season. It is also possible that quantities were carried underground. Rodents may alter the composition of the vegetation of an area by selective foraging. Koford (1960, p. 385) asserts that t,he foraging activities of Prairie Dogs (Cynomys ludovicianus) tend to make the composition of the vegetation more heterogeneous. Annuals may be destroyed because these animals consume seeds before they have a chance to mature. He also noted in some prairie dog towns that forbs such as sage are kept grazed to a few inches in height. I n his study of the Merriam Kangaroo Rat (Dipodomys merriami Mearm), Reynolds (1958, p. 124) found that “large seeded perennial grasses and tall shrubby plants increased markedly on plots where these rodents were most abundant”. He attributed this alteration in vegetational composition to this rodent’s habit of caching seeds in excess of its needs. Pocket gophers can apparently subsist on any of an extremely wide variety of plant species, although they have a strong preference for forbs (Miller, 1964). They cut many roots, thus affecting many plants that may not actually be eaten.

158

A. DE VOS

Rodents and lagomorphs may disseminate and even plant the seed of undesirable species. Bird (1930) and Moss (1932) have discussed the role of rodents in facilitating the spread of poplar vegetation into Canadian grasslands. Shrub communities became established in the grassland as a consequence of the activities of certain animals. I n some cases these communities were succeeded by aspen consociation. Pocket Gophers, Richardson’s Ground Squirrels (Citellus richardsoni), and Badgers, threw up mounds of earth that choked out the grass, thus enabling Elaeagnus and Symphoricarpos to gain a foothold, seeds of the latter shrub being distributed in large numbers by the Pine Grosbeak (Pinicola enucleator). I n the comparatively loose earth and sheltered conditions of Symphoricarpos and Symphoricarpos-Elaeagnusstands, aspen seedlings could establish themselves. Rodents may also accelerate the spread of shrubs. For instance, the majority of individuals of Sand Pocket Mice (Perognathus penicilatus pricei) near Tucson, Arizona, were found carrying products and seeds of mesquite (Prosopis juli,flora), an invader of overgrazed short grass (Arnold, L. W., 1942). Similarly, Reynolds (1964) showed that the Merriam Kangaroo Rat precipitated the spread and increase of mesquite. The vegetation upon the mounds thrown up by the numerous animals in the midst of the steppe has usually a more desert like, xerophytic character; at f i s t it contains many “weeds” (Formosov, 1928). Rodents tend to change the relative area of ground covered by each plant species. Rodent effects differ with the site and its vegetation. Not only do rodents affect the forage crop directly, by removing part of it each year, but also indirectly, through exerting long-term influences on the abundance of various plants. Range rodents and lagomorphs may delay or advance plant succession depending on environmental conditions and animal species concerned. On a range that has deteriorated to the point of having more weeds than grasses, the effects of jack rabbits will be towards further deterioration (Arnold, J. F., 1942). Rodents may postpone the natural succession of plant associations, and thereby assist in maintaining for long periods the kind of vegetation to which they have become adapted (Formosov, 1928). This conclusion was also arrived at by Koford (1958) who states that the activities of prairie dogs maintain and extend the short-grass association. If man does not alter the grassland, it seems impossible for rodents or lagomorphs to eliminate the grass climax or subclimax. This was found to be the case with jack rabbits in Arizona (Taylor et al., 1935) and with prairie dogs in the short grass prairies (Koford, 1958). Under some conditions range rodents and lagomorphs may assist in

PRODUCTION OF WILD HERBIVOROUS MAMMALS

159

the recovery of deteriorated ranges by differential pressure on plant species typical of early successional stages (Bond, 1945). For example: 1. I n an area in Oklahoma, Prairie Dogs seemed to be able to keep the woody components of the community well under control and, with the aid of domestic stock, to maintain indefinitely a condition resembling short-grass or mixed-grass prairies (Osborn, 1942). 2. I n an enclosure on the San Joaquin Experimental Range in California, a species of Ground Squirrel (Citellus beecheyi) in a five-year period had the effect of substantially decreasing the abundance of Erodium botrys and Lupinus bicolor, while increasing Bromw nzollis, a grass definitely higher on the scale of succession than the two forbs (Horn and Fitch, 1942). 3. A large proportion of the food of the White-throated Wood Rat (Neotoma albigula) consists of woody plants or weedy herbs. On ranges not being overgrazed, they may, to some extent, assist the climax perennial grasses in re-establishing themselves (Vorhies and Taylor, 1940).

3. Changes in populations and species of l a g m o r p h and rodents related to plant succession Rodent populations vary as a response to the degree of forage utilization by ungulates and some lagomorphs are likely to be more numerous on a rather depleted and weedy range than on one in climax or near-climax condition. Most studies have indicated a trend toward more jack rabbits on heavily used ranges. than on lightly or unused ranges. On the other hand, some species may decrease in numbers. For example, Vorhies and Taylor (1940) state “As the grazing range deteriorates in various parts of the American southwest, the superior perennial grasses tend to be replaced by annuals, and numerous weeds become abundant . . . cottontails, cotton rats, meadow mice, Harvest Mice (Reithrodontomys humulis) and other species characteristic of thick grass tend to decrease, and jack rabbits, kangaroo rats, prairie dogs, ground squirrels, and wood rats . . . tend to increase”. This type of range relationship seems to have at least two independent causes: 1. In the case of the California and antelope jack rabbits, ground squirrels, and prairie dogs, heavy stands of tall grasses appear to discourage the animals, in part at least, because their view is shut off, and they cannot keep adequate watch for dangers. 2. I n the case of the Pocket Gopher, the greater proportion of taprooted and bulbous-rooted plants in deteriorated range is more probably the deciding factor.

160

A. D E VOS

The larger and more numerous seeds usually afforded by the annual components of deteriorated range probably tend to increase the populations of certain spermophilous rodents, such as certain kangaroo rats, pocket mice, and probakly ground squirrels; some rodents may be benefited both by more open vegetation and a better food supply. Overgrazing favours prairie dogs (Koford, 1958). Range deterioration and consequent reduction in food supplies can ultimately be carried so far that the rodent and rabbit populations will be greatly reduced or disappear. Although there is relatively little published information on this subject for Africa, it seems that comparable conditions prevail to those observed in North America. I n Southern, Central and East Africa the incidence of Spring Hares (Pedetes capensis) and Hares (Lepus capensis cmwshayi and L e p w c. capensis) is often noticeably higher in heavily grazed areas.

c. T H E R O L E

OF RODENT MOUNDS A N D TERMITARIA

The most obvious modifications by animals on the physiography of grasslands include rodent mounds and termitaria. Although reference has been made to the effects of rodents on the soil and soil conditions, more should be said about rodent mounds. Rodent mounds produce somewhat comparable changes in the grasslands of North America and Eurasia to the termitaria of Africa, namely by breaking up flat surfaces with diggings, bringing up subsoil, aerating the soil through tunnels and loosening it up, and affecting the vegetation on and around the mounds. These various types of mounds affect the microclimate and also wind erosion patterns. Rodents producing mounds or hillocks include mainly pocket gophers, ground squirrels and prairie dogs. The latter two groups of rodents may leave changes on the surface of the landscape through their burrowing activities which may be noticeable several decades or more after mounds have been deserted. For instance, Mushketov (1885, i n Formosov, 1928) refers to mounds thrown up at the entrance to the burrows of a Ground Squirrel (Citellus pygrnaeus phnicola Satun), covering hundreds of square kilometres of the surface of the Kalmouk steppe, giving it a peculiar, hillocky, mottled aspect. Although the mechanics of the origin of the mounds on plains and prairies is still a subject of conjecture and controversy, it seems probable that burrowing mammals, including prairie dogs, are to a large extent responsible for the regular, rounded mounds on the Great Plains of North America (Koford, 1958). Ross et al. (1968) also express the view

PRODUCTION OF WILD HERBIVOROUS MAMMALS

161

that these mounds are formed primarily by animals disturbing and mixing the soil in a particular spot. I n parts of the Great Plains prairie dog mounds in current use are seven metres in diameter and one-half metre thick. Similar low mounds, fairly regularly spaced about 22 m apart, pimple many areas where now there are no prairie dogs. These mounds may have been formed by the work of many generations. The work of badgers may well be important in building up huge mounds, for when a badger digs out a burrow the amount of earth piled at the mouth increases markedly overnight (Koford, 1958). I n Africa, relatively few mounds produced by rodents are known, although spring hares throw up small mounds in front of their burrows and African mole rats (belonging to three genera) locally produce fairly sizeable mounds. Termitaria largely take the place of rodent mounds and have a somewhat comparable influence on the physiography of grasslands to rodent mounds. The variability in shape, size and colour of termite mounds is not normally due to different species of termites (Termitidae), but rather to different kinds of soil and climatic conditions. There are, however, certain fundamental differences in the mounds of different genera of termites. Termites take their building materials from the subsoil to a depth of approximately one-half to two metres; the topsoil is not usually touched (Hesse, 1955). Murray (1938) demonstrated that termitaria in the Transvaal had a higher percentage of humus, nitrogen (about twice as much) than the surrounding soils. They also had a high water-retaining capacity. Bushmen make use of the fact that termites bring minerals to the surface by setting snares and traps around termite holes on pans in order to trap springbok (Antidorcasmarsupialis) which come and “lick” the soil brought to the surface (Child, personal communication). Termites can have a profound effect on vegetation by their foraging activities. Termite attacks often cause death of plants (Murray, 1938). Living termitaria are rarely covered by vegetation. Glover et al. (1964) suggest that it is not the chemical composition, but the hardness and imperviousness of the soil which discourages plant growth on living termitaria, and that vegetation patterns around the mounds are influenced by the amount of clay and salts derived from the termitaria themselves. The reason why vegetation tends to increase on mounds which are deserted by termites is that the physical condition of the soil is better than that of the surrounding land because of better drainage and/ or aeration. When a mound has been built on or near land of poor drainage it has greater evaporating powers than the surrounding soils.

162

A. DE VOS

Consequently, a concentration of mineral salts occurs underneath it, including chloride sand nitrates. Chalk is sometimes deposited because when water drawn to a mound evaporates, calcium is precipitated as an insoluble carbonate (Hesse, 1955). The dense clumps of woody vegetation on old termite mounds in poorly drained soil are very distinctive; in some areas this vegetation is almost entirely confined to the mounds. On open savannas, shrub and tree growth is often almost entirely restricted to termite mounds. Glover et al. (1964) state that one termitarium can support a whole series of plant communities, ranging from the most primitive to the most highly organized, each mound supporting a micro-association within a larger vegetation type. These communities are often different from those of the immediate surroundings. Not only do rodent mounds and termitaria have a pronounced influence on the vegetation, but also on the food and other habits of animals. The concentration of mineral salts explains why termitaria are commonly used as salt licks by cattle and game (Hesse, 1955). Aard-varks (Orycteropus afer) dig numerous holes in low termite mounds. These animals not only bring up sizeable quantities of subsoil, but also scatter soils modified by termites, which has ecological consequences (Murray, 1938). Some of the other animals that also dig holes in the mounds or occupy old aard-vark holes are several species of Mongoose (Mungos mungo), Bat-eared Fox (Octocyon megalotis), jackal (Cunis mesomelas), Hyena (Crocuta crocuta), Porcupine (Hystriz spp.), and often Wart Hog (Phacochoerus aethiopicus). I n North America, badgers, Kit Fox (Vulpes mucrotis) and Swift Fox (Vulpes velox) dig into prairie dog and ground squirrel mounds and burrows. Termitaria are often more intensively grazed and/or browsed than the surrounding vegetation, because of the richer plant growth and often also because of the different type of vegetation found on these mounds. This more concentrated presence of herbivores in turn increases local faecal deposits. Termitaria mounds provide resting islands for Lechwe (Onotragw leche smithemuni) on flooded land, as well as for predators that prey on Lechwe. Mention should also be made of the effect of the foraging by termites on the vegetation in a circular area around their mounds, which is likely selective in nature. This may result in bare patches on the ground around the mound, enough to protect any vegetation growing on the mounds from fire. This, in turn, enables woody vegetation to survive. Gwynne (personal communication) estimates that termites can leave up to 10% of the land surface on which they forage devoid of vegetation. Not only rodents and termites affect the physiography of the landscape. Some ant species do this to a lesser extent. For example, the

PRODUCTION O F WILD HERBIVOROUS MAMMALS

163

Western Harvester Ant (Pogonomyrmex spp.) of the western part of the United States has this effect. Ants also affect the vegetation around their hills by their foraging activities.

V I I I . BIOMASSA N D E N E R G Y PRODUCTION OF HERBIVOROUS MAMMALS A.

BASIC CONSIDERATIONS

So far I have considered the environmental factors affecting production. I will now review the available literature on the production of herbivorous mammals, with emphasis on wild species. Biomass of herbivorous mammals is produced by converting plant material into animal tissue. Biomass is used for comparisons of production between different communities. It has often been argued that this is only a rough measure in view of the variable quantities of inorganic substances present in different types of organisms. A better guide to the total biological effect of animals on their environment is their expenditure of metabolic energy. I n measuring any community of animals containing species of different sizes, particularly where it is wished to compare the biological production of one community with that of another, the total energy “turnover” in calories is a convenient and useful criterion. The relative importance of different species can be compared more simply on the basis of their contribution to the energy flow of the community than in terms of biomass. “The study of energy flow in ecosystems where grazing plays a part must begin with the primary production of organic matter from solar energy by the plant. It has been increasingly recognized of late that it is not the obvious quantities of plant material present as standing crop that determines primary productivity but the unseen turnover of energy and organic matter.” (Crisp, 1964). Much of the energy available in the form of plant matter is not, of course, grazed by economically favoured species, because it may be used by rival herbivores ranging in size from insects to large grazing animals. Of the calorific value in food ingested a considerable proportion, varying usually from about 40% to more than 90% is rejected as faeces; only a reduced amount is actually assimilated. A proportion of this assimilated food is stored in the tissues of the animal or is used in the formation of eggs or young and thus contributes to the growth of the stock of the population. The rest of the food is broken down to produce excreted matter of reduced energy content and, at the same Q

164

A. DE

VOS

time, energy is liberated in the form of heat or mechanical work. The stock in turn is exploited by predators which, therefore, stand to benefit from a high secondary net production rate (Macfadyen, 1964). As has been pointed out by Talbot (1964), great variations exist between the basis of calculations of biomass by different authors, particularly with regard to the determination of the numbers of animals, their age, their weight, the land area involved, the period of time to which the calculations refer, the season and the stage or trend of population fluctuations at the time the calculations were made. Some authors consider only the principal herbivores in their calculations. Some include juveniles as well as adults, while others only adults. Ideally species weight should be based on a detailed knowledge of the population structure of each species. Biomass figures can be valid and useful, but they must be very carefully defined and applied, particularly when comparing results of different studies. I n terms of production and carrying capacity, the most useful data on biomass will be those determined over a period long enough to include fluctuations in climate and animal populations. Biomass figures only tell us what is there in a comparative sense, but nothing about potential. Comparing different areas by biomass/km2 only compares their standing crops, not their secondary production. Provided, however, that biomass of different species is not lumped together and each biomass is multiplied by its appropriate value of instantaneous turn-over rate, it can be used to estimate the secondary production of a management unit. Some counts have been made in arbitrarily defined areas, parts of which are not used significantly, or at all, by the animals to be counted. The inclusion of these parts in the calculation of weight per unit area result in an underestimation of the carrying capacity of the remainder of the area. The number and weight of animals a given rangeland can support on a long-term basis varies with the condition and type of vegetation and with the species of animal. This may also change from year to year as a result of climatic conditions and the degree of grazing to which a range has been submitted in previous years. Other factors include the animals presently grazing the area as well as the short and long-term effects of burning and the trends in the vegetation resulting from past land use history. Although weight records are now available for most species, the criteria for biomass determination remain somewhat arbitrary. Biomass figures should be carefully related to range condition and population structures to be truly indicative. A large amount of literature has accumulated concerning the many and varied techniques for sampling populations. The techniques vary

PRODUCTION O F WILD HERBIVOROUS MAMMALS

165

with the type of terrain and the kind of animals being sampled. The entire field estimate depends ultimately upon the estimate of the number of individuals in the area. Each investigator has his own modification of some existing technique made necessary by the kinds of animals and the terrain encountered, as well as by the time, materials, and money available to him. Since several estimates (e.g. biomaas, standing crop, age and/or size classifications) are derived directly from the number of individuals counted, it is important that these counts be as accurate as possible (Engelmann, 1966). Aerial censuses are used widely to determine the populations of ungulates. Many parameters influence the results obtained. These include human error, weather factors, seasonal influences (presence or absence of leaves), mechanical influences (type and air speed of aircraft, etc.), habitat influences (variability and amount of cover), animal influences (activity patterns and reaction to aircraft), population structure of species, time of day and profile of the ground. Some of these parameters are extremely difficult to evaluate. Aerial censuses are not always effective. Savory (1965) stated that during 40 minutes flying over an area in which a ground survey had indicated a population of one impala to four acres, not one was seen from the air. One method of estimating production is based on utilizing information on the age distribution of the population, the growth curve for the species, and the calorific equivalent of animal tissue. If an appropriate growth curve is available, and the age of the individuals in the population is known, the biomass produced in a given number of days can be estimated from the curve for each age. The gain in weight is then converted into energy with the proper calorific constant (Davis and Golley, 1963). Production, both primary (by green plants) and secondary (by consumers) in an ecosystem, is apparently increased by species variety because this permits the occupancy of more niches in the habitat. Talbot and Talbot (1963) have presented data to show that a variety of ungulates can make more efficient use of a range and sustain a higher biomass than a lesser number of species. I n East African rangelands it is not unusual to find over 20 species of wild herbivores living and feeding in the same area, varying in size from the Dik-dik (Madoqua kirki),weighing 5 kg, to the 3000-5000 kg African Elephant (Loxodrmta africana, Talbot et al., 1962). Direct competition is avoided or minimized because of niche separations of the species and their different preferences for food species and plant parts. Virtually all the vegetative growth provides nutrition for the animal mass feeding on it. It, therefore, seems reasonable that a range offering a greater variety of plant species and types could also maintain a larger number of ungulates. Recent work

166

A. DE VOS

however suggests that this is not such a simple picture as Talbot and Talbot (1963) suggest and that several species may compete for the same vegetation and may overlap in their food habits. A study by Ovington (1964) in Minnesota revealed that a savanna type, supporting trees, shrubs, forbs and grasses, produced annually more than five times as much plant material above ground per unit area as did nearby grassland areas. This vast difference seems explainable by the more efficient use which a variety of plants at different levels must be able to make of the above and below ground level than can herbaceous species alone. The complete removal of Hippopotamus (Hippopotamus amphibius) in study areas has resulted in a gradual increase in other species (Laws, 1964), so that at a certain stage a higher biomass of large mammals is supported in these areas than when a preponderance of hippopotamus was permitted to exist. I n the Queen Elizabeth National Park the very high biomasses are composed of relatively few species, and of these the elephant, hippopotamus and buffalo are the most important ones (Field, 1968). There are species differences in the proportion of food that is assimilated to the food ingested; the ruminants assimilate a greater proportion of their ingested food than, e.g., the elephant. Especially in dealing with a spectrum of grazing species on rangelands, production estimates may need to be based on the calorific values of forage production as compared with the energy requirements of animal consumers.

B. A V A I L A B L E

EVIDENCE O N PRODUCTIVITY

Numerous papers have been published on the biomass production of wild herbivorous mammals in grassland environments during the last decade, but most of them are based on inadequate field data collected during too short a period. However, to determine the standing crop accurately is often extremely difficult and must remain the objective of special research efforts. Some of the better papers on the subject will be discussed in some detail, particularly with reference to sources of error and/or bias. Stewart and Zaphiro (1963) compared the biomass production of different vegetation types in Kenya. Whenever more than one census was made per area, they presented maximum and minimum biomass estimates. Seasonal variations in biomass data as indicated by the maximum and minimum figures were small in areas which are virtually ecological entities and subject only to small-scale movements into and out of the areas. Much larger seasonal variations occurred in those

PRODUCTION OF WILD HERBIVOROUS MAMMALS

167

areas which are not ecological entities and subject to fairly regular large-scale migrations. They found that Acacia-Themeda grassland is the most productive vegetation type in Kenya and that other forms of tree-grassland came second. Highland grassland has only a third, and desert grass-bush a tenth of the carrying capacity of Acacia-Themeda grassland. They computed an average biomass of 1945 kg/km2 on the Athi-Kapiti Plains before 1961, and after the severe drought of 1961 of 1089 kg/km2, showing the depressing effect of drought conditions. Lamprey (1964) made an estimate of large mammal densities, biomass and energy exchange in a study area in Tanzania during the period 1958-61. He mainly used a transect system of game counting on the ground, but direct aerial counting and total counting on the ground were also employed to provide checks on the transect results. The transect lines were followed daily through vegetation of varying density. In order to define the width of the strip censused on each transect, a “visibility profile” was plotted by measuring the distance from the base line to the point where a khaki-dressed man ceased to be visible as he walked away from the line. The use of this profile in combination with the transect lines had the object of providing monthly absolute density figures. Individuals of different species of mammals were watched to determine whether they also ceased to be visible at the distances measured. With only three exceptions all species conformed to the general, visibility distance estimate. Elephant and Giraffe (Giraffa camelopardalis) could be seen approximately 5% further away under certain circumstances. Dik-dik became invisible at about two-thirds of the normal visibility distance from the transect line. One disadvantage of this method lies in the fact that a disproportionately large amount of open ground is included in the census. Lines were sufficiently far apart to make recounts of animals unlikely. The different methods of obtaining density values showed general agreement, suggesting a reasonable accuracy of the transect results. Statistical analysis of data, using a run test showed that the fluctuations of impala, warthog, waterbuck, dik-dik, and rhinoceros are significant, while those of hartebeest are marginally significant. With four other species the fluctuations could not be shown to be non-random in their distribution. One weakness of this study is that adjusted weights were obtained by subtracting from the average adult weights a percentage determined by the observed frequency of young animals in the population. I n view of the small size of the samples from which average weights are taken and the somewhat arbitrary adjustment for t,he young animals in the population, the adjusted averages can only be regarded as approximation.

A. DE VOS

168

TABLEI1 Year long standing crop ( b i o w s ) of wild ungulates and domestic liveatock (modified from RoM, 1966)

Types of range and location

Standing crop kg liveweight per sq. km

Stock

A. SAVANNA LANDS OR PRAIRIE, Partly overgrazed, over- Wild ungulates overstocked (1 1 species) (Albert National Park) Savanna (East Africa) Wild ungulates (numerous species) Wooded savanna (rainy Wild ungulates season) (22 species) Tarangire Game Reserve (Tanzania) Wooded savanna (dry Wild ungulates season) Tarangire (22 species) Game Reserve Prairie (Western U.S.A.) Bison and other wild ungulates

Reference

UNGRAZED B Y DOMESTIC STOCK

Bourlibre and Verschuren (1960).

7,574 20,469 Two areas* 12,260t

Talbot and Talbot (1963).

17,510t

Lamprey (1964).

1,050 (yearlong)* 12,300 (average of 4 years)*

Lamprey (1964).

2,4563,500*

Petrides (1956).

B. SAVANNA LANDS EXTENSIVELY USED FOR LIVESTOCK GRAZING Acacia-Commiphora-bush- Wild ungulates 1,960-2,800* Talbot and Talbot savanna (East Africa) livestock (only (1963). goats and sheep) 5,25612,600* Foster and Coe (1968). Mostly open plains Wild ungulates + (Nairobi National Park) cattle over 6 years (carrying cap. f6,300) Mostly open plains Wild ungulates 8,225 (one Petrides (1956). (Nairobi National Park) cattle census)*

+

+

c. SAVANNA Acacia-Commiphora savanna ColophospernumCombretum Commiphora-bushsavanna (Rhodesia)

* t

LANDS DETERIORATED THROUGH LIVESTOCK GRAZING

Wild ungulates (15 species) Wild ungulates 17 species)

From Foster and Coe (1968). From Roth (1966).

4,692t

Grzimek (1960).

4,418

Dasmann (1962).

PRODUCTION OF WILD HERBIVOROUS MAMMALS

169

Where a community of game animals includes a high proportion of individuals weighing between 50 and 500 kg, fluctuations in numbers can be expected to be accompanied by approximately proportional changes in biomass and total metabolic energy. Another detailed study of the biomass of game animals in the Nairobi National Park, 1960-66 was reported on by Foster and Coe (1968). The data were obtained by counts carried out on the last Sunday of each month in specific census areas. It was assumed that over the period of a year the times an animal is counted twice is cancelled out by the times it is not counted at all. Census results were considered to be reasonably accurate for eleven species of ungulates and the Olive baboon, Papio anubis Fisher. Species which were more difficult to count include the lion, the cheetah, the reedbuck (Redunca redunca and R. fulvorofula chanleu) and the bushbuck (Tragelaphus scriptus). Smaller species of mammals that are almost impossible to census accurately were not censused. The minimum adult weight was used to compute biomass figures. I n this way immature animals might be approximately compensated for by the underestimation of older animals. The biomass for each important species was computed. The biomass of large predators was only 1.4% of the total biomass of wild ungulates. Other papers referring to biological productivity include those of Talbot (1963), dealing with the productivity of savannas, and Roth (1966), dealing with Rhodesia. Petrides and Swank (1965) estimated the productivity and energy relations of an African elephant population. Examples of biomass production of wild ungulates and domestic stock are shown in Table 11. Only the more reliable estimates are included. This table shows that the biomass production varies considerably with environmental conditions. It tends to drop with deterioration of range condition quality and under joint use of wild and domestic stock under poor range management conditions.

c. A

C O M P A R I S O N B E T W E E N A F R I C A A N D N O R T H AMERICA I N TERMS OF BIOMASS P R ODUCTIO N

The relatively small number of species of large ungulates on the North American range may be a reason for their rather low biomass production as compared with parts of Africa. Not all portions of the vegetation seem to be utilized as efficiently as in Africa because of this small number and therefore a more restricted use of available food. Petrides (1956) has contrasted the biomass production of wild ungulates in East Africa with some American data. He found that the East African grasslands have a greater productivity of species and biomass than the American plains (Table 11).It should be remembered, however,

170

A . DE VOS

that in North America the best sections of the prairie have been converted to cattle range or crop production, while in East Africa there still remains a large amount of an improved range. This comparison is therefore not entirely valid. It seems, based on available evidence, that the influence of rodents and lagomorphs on the grassland environment in Africa is not as pronounced as in North America. Although in Africa rodent populations are generally high in forested environments, they appear to be lower in most open grasslands. While Misonne and Verschuren (1966) found 25 species of rodents in Serengeti National Park, only about half of these normally occurred in grassland ecosystems. On the whole, the population density of these species was very low, particularly in the dry grasslands and bush country. They concluded that it was possible that one species of rodent, Arvicanthis abyssinicus, could locally be considered a competitor to the large herbivores in the utilization of plant biomass. I n Botswana rodent numbers fluctuate widely on rangeland. I n some years (e.g. 1967) the ground is covered with rodent holes for acres at a time, while in other years (e.g. 1964) numbers are very low (Child, personal communication). However, Foster (personal communication) found a very high biomass (386 kg/km2)produced by six genera of rodents and one insectivore in the Ngorongoro Crater. The high spring hare and hare populations on overgrazed and deteriorating rangeland in Central and East Africa are comparable to jack rabbits populations on deteriorated land in North America (personal observations). There are few ground squirrel populations on the open grasslands of Africa. One species (Xerus anurus) occurs on open grassland on the Makarikari in Botswana (Child, personal communication). However, they do occur in substantial numbers in dry savanna country. Soil characteristics are probably important to their distribution. Somewhere on the North American prairies and on the African grasslands conditions can be found where the greatest complexity of biotic communities prevails. It would appear useful to compare the number of herbivorous species of mammals in these most complex communities in North America and Africa, to determine on which of these two continents are the interactions of these species most intricate.

D.

T H E E F F E C T S O F D E G R A D A T I O N OF T H E E N V I R O N M E N T O N T H E P R O D U C T I V I T Y OF W I L D H E R B I V O R O U S MAMMALS

Many grasslands are biotic communities which have been “deflected” from their normal course of ecological succession by the influences of cultivation, fire and grazing. When these factors become over-

PRODUCTION O F WILD HERBIVOROUS MAMMALS

171

accentuated deterioration sets in, resulting in lower and more primitive types of biotic communities and, eventually, in complete destruction of the habitat (Glover, 1966). On a deteriorating range the carrying capacity has been exceeded by the standing crop of animals for some time. This is unfortunately true for much rangeland. Indicators of the serious extent of land decline are ever decreasing wildlife populations over an extended period of time, and an increasing incidence of droughts and/or floods. While this overall decrease in wildlife is taking place, some species may temporarily increase. These include, e.g., impalas and oribis. Apart from the main function of energy trapping, range vegetation also plays a role in maintaining soil cover, content of organic matter, aeration and porosity, and in providing vital litter for soil cover. If climax perennial grass and, in particular, litter cover is destroyed too frequently by fire or by prolonged grazing, soil structure begins to alter and water runs off instead of soaking in: “floods” and/or “droughts” occur; perennial waters dry up; vegetation volume generally declines; the effective dry season lengthens as the remaining predominantly annual grasses green up later and dry off earlier; the survival of desirable mesophytic perennial grass seedlings becomes more and more difficult due to an arid micro-environment; xerophytic grasses predominate and soil losses proceed steadily. Observations on areas in Utah which have been subjected both to promiscuous burning and to heavy grazing show that a combination of these factors has seriously reduced the botanical density of the plant cover, and has depleted the stand of perennial grasses nearly 85%. Annual grasses and poor perennial and annual weeds are predominant. Changes in the plant cover due to fire and grazing caused a reduction of over 50% in the grazing capacity (Pickford, 1932). Range deterioration is widespread in many extensively used and scarcely-populated ranges in Africa, which are also used by wildlife. This may also be the case in unpopulated areas due to fire and possibly due to changes in settled neighbouring areas leading to a build up in mobile species which may then over-use the unsettled areas. This is a serious phenomenon which should be combated by better management.

I X . M A N A G E M E N TC O N S I D E R A T I O N S A.

GAME RANCHING AND UTILIZATION

In view of increasing protein scarcity throughout the world, there is no doubt about the need for new sources of food production, including

172

A. DE VOS

the harvest of wild herbivorous mammals, and for better range management, to insure that widespread range deterioration is halted. Darling (1960) was the first to describe the biological separation of various species of African ungulates in some detail and to propose that this be put to productive use. He argued that while wild species can use almost every aspect of the existing vegetation, cattle only use a small proportion, implying that if we start with what is there and manipulate it, a higher degree of productivity can be attained. Gwynne (personal communication) has obtained substantial evidence that some of the wild herbivores normally described as “browsers” prefer to eat grasses when available and that, in fact, not as wide use is made of the available spectrum ofvegetation by wild ungulates as had been surmized by Darling. There are several ways in which productivity may be measured. Reproduction, growth rates, live weight gains, and the meat yield per carcass are key factors. Advantages of utilizing wild herbivores in Africa in this regard include: 1. Rapid gain of weight. Wild animals reach marketable or economically harvestable size at an earlier age than domestic stock. Gain of weight varies from a rate of 0.06 kg per day for Thomson’s gazelle to 0.24 kg per day for eland. This compares with a gain of poorly managed African cattle on unimproved East African rangeland of 0.14 kg per day (Talbot et al., 1962). However, cow-eland growth comparisons in Rhodesia have shown that under similar range management cows gained weight more rapidly (Skinner, 1967). 2. Relatively high reproductive potential. First breeding varies from just under one year for smaller antelopes and gazelles, to between one and two years of age for large antelopes and between two and three years for eland and buffalo. The average African-owned cow in East Africa will breed when about three and a half years old (Talbot et al., 1962). The females of most wild ungulates up to the size of eland normally produce at least one young per year. 3. High dressing-out percentage, between 50 and 62 %. Domestic cattle can achieve such killing-out percentages, but at this level cattle carry up to 40% fat content on their dressed carcass, whereas the wild ungulates at this level carry only 2.5% fat (Ledger et al., 1967). Consequently, in terms of meat production the wild animals with virtually no fat make far more effective use of the available vegetation than do domestic animals. 4. A number of wild ungulates have specialized physiological water conservation systems, requiring considerably less water than cattle. Because they are less dependent upon free water for their survival in arid environments, they can utilize arid range more effectively than

PRODUCTION OF WILD HERBIVOROUS MAMMALS

173

domestic stock (Ledger et al., 1967). Some species living in areas with a rainfall of 12-25 cm have no access to free water for six to nine months. These include Gemsbok (Oryx gaxella), Impala (Aepyceros mebmpus), Hartebeest (Alcelaphzcssp.), Springbok, Eland and several other wild ungulates. Other species of wild ungulates are able to go waterless for several days. 5. Wild ungulates are more resistant to endemic diseases than domestic stock. This is an important consideration in Africa because of the widespread incidence of diseases. Game harvesting on an organized commercial basis is a relatively new industry, but its use is increasing rapidly. It is not restricted to game ranches, but it includes harvesting completely wild animals on a large scale, including hippopotamus, elephant, buffalo and several species of antelope. An important obstacle to the expansion of wildlife harvesting is veterinary restrictions based on the dangers of disease to both human beings and wildlife. Although disease may be controlled in domestic livestock, the same measures often cannot be applied to free-ranging wild animals. Although much has been written about the advantages of using a. wide spectrum of wild herbivores for meat production, relatively few authors have been able to demonstrate the practicability or the economic advantages of game ranching and utilization schemes. These include Dasmann (1962, 1964), Savory (1965) and Roth (1966). Riney and Kettlitz (1964) found that on a farm in Transvaal stocked with one beast per 8.5 ha over six months only, the standing crop of blesbuck and springbok together represented twice as much liveweight per km2 as cattle which was estimated at 3090 kg/km2. Roth (1966) evaluated statistical data of 1964 to give a critical account of the status of game as a source of food in Rhodesia, and to assess the overall economic value of the wildlife resource in this respect. The overall contribution of game animals to the nutrition of people equalled in significance the pig industry or the production from sheep and goats together. The particular importance of game is, however, that it produces protein in those areas which are either completely unsuitable or marginal to beef production. His analysis showed that in semi-arid savanna areas, where the maximum beef production is about 0.6 kg/ha, managed multi-species game populations have produced the same or even higher yields over successive years, in addition to the production from cattle. Among wild herbivores, eland appear most suitable for meat production. This antelope can be husbanded readily, comparable to domestic stock. Two main biological advantages of the eland over domestic animals include a higher reproductive rate and better physiological and

174

A. DE VOS

behavioural adaptation to a hot, semi-arid environment. Further, eland will feed on a wider spectrum of plants than domestic cattle. Certain problems will have to be considered in their management. For example, they are capable of jumping effortlessly over fences 2-2.5 m in height. Davison (1966) reports aggressive behaviour, even goring, by eland when penned up and, therefore, dehorning would be a necessity. A disadvantage of the eland is that its productivity as a domestic animal appears to be inferior to cattle. Its high metabolic rate and narrow thermal neutral zone necessitate a higher food consumption for each pound of meat produced (Taylor and Lyman, 1967). It is essential that studies be carried out to determine to what extent eland would compete with domestic livestock for the available vegetation in different areas, and particularly under ranching conditions. Further research into the susceptibility and resistance to disease, reproduction and growth rate of this antelope is required; in particular, the influence of dehorning and castration on growth rate should be investigated (Skinner, 1967). It is quite essential that the fauna should have access to all the component plant associations which are needed to satisfy the needs of each species through the seasons. Management should take into consideration such details as the availability of suitable pastures throughout the season, the establishment of grazing succession between the species of animals, and the development of a grazing mosaic, while allowing for periods of rest for the different grass associations (VeseyFitzgerald, 1963). In general, maximum variety and yield from the vegetation is maintained by a delicate balance between burning and grazing. Altering this balance usually decreases the number of plant species and their yield.

B. R A N G E

MANAGEMENT FOR WILD AND DOMESTIC

HERBIVORES

Since most rangeland which is now occupied solely by wildlife but which has a potential for livestock will no doubt be used for production of the latter in the foreseeable future, the problems of management for both wild and domestic herbivores will be discussed briefly. The objective of range management is maximum production of meat and animal products without damage to the land. Major management phases include: 1. deciding proper grazing use, 2. improving forage production,

PRODUCTION O F WILD HERBIVOROUS MAMMALS

176

3. increasing usability of the range, and 4. managing animal units (Stoddart, 1967).

Assuming that range management for a combination of wild and domestic herbivores is practical and economically feasible in Africa, what are some of the problems, and how can they be solved? The type of rangeland to be managed is carrying natural or seminatural vegetation which provides a habitat suitable for herds of wild or domestic ungulates. The ecosystem of such rangeland should be carefully studied, using the holistic approach. I n contrast to a stable and undisturbed “natural” ecosystem, in which a dynamic equilibrium between energy input and output is maintained, in managed range ecosystems part of the net production is converted into marketable animal products. These are removed and thereby lost from the cycle. For the efficient maintenance of energy flow and productivity in such modified ecosystems, two questions must be answered: (a) how much of the primary production can be removed by the consumer without endangering further storage of energy and further animal production, and (b) what is the most profitable and ecologically satisfactory way of channelling primary productivity into animal protein? (Naveh, 1966).

I n addition, we need to know more about the physical relationships between animals, plants and soils to estimate future production at different levels of use under different management systems. The range condition can be determined by long-term and systematic observations of the changes in vegetation and soil in different range types and under different grazing regimes. Carrying capacities for wildlife are extremely difficult, if not impossible, to determine accurately. Perhaps the most reasonable approach to the problem of determining carrying capacity is one of using the vegetational changes to indicate needed adjustments. Emphasis must be placed on range improvement and maintenance rather than carrying capacity. Beginning with a deteriorated range, the potential carrying capacity is not nearly so important as improvement to reach that potential (Heady, 1960). Where a range is jointly occupied by domestic stock and wildlife there is competition and the stocking rate should be adjusted accordingly. For instance, in North America elk (Cervw canadensis) compete directly and extensively with cattle for range forage. Pronghorn antelope and sheep feed extensively on many of the same plants. Competition for food between sheep and deer is greater than between cattle and deer. I n Africa there is considerable competition between

176

A. DE VOS

domestic stock and many more species of wildlife, including several species of antelopes, zebras, etc. Insufficient data are available dealing with a comparison of economic returns from wild and domestic herbivores. Ramsey (1965) showed that the potential economic return from deer was greater than that from livestock under conditions of average prevailing prices and adequate deer harvest in Texas. The best yearly return of $28.82 per animal unit of livestock was not as great as the 1958-63 average return of $38.60 from the deer herd. The deer herds are grossly under-harvested, with a resulting loss in potential income to the rancher. Deer products in the form of hunting have a demand in the study area which is increasing above that of the demand for any domestic livestock produced. One serious problem to be faced in range management in Africa is how to return damaged lands to a satisfactory level without tremendous capital expense. Maloiy and Heady (1965) have suggested some guidelines to meet this situation in Masailand for livestock. 1. Several areas of not less than 4090 ha, and preferably up to 20,240 ha, should be selected for development. 2. Range improvements including fenced pasture boundaries, new water sources, bush control, dip tanks and spray pumps for ectoparasites and tsetse fly control should be developed. 3. I n order to ensure even growth of animals, and to prevent drastic loss of condition during the dry season, attempts should be made to produce and conserve fodder. 4. Control of livestock numbers and intensity of forage use are absolutely essential. 6. Livestock production should evolve towards a commercial enterprise based on year-long, wet and dry season, balance of feed needs and SUPPIY. Obviously several of the more mobile species of wild herbivores would not be able to thrive under these conditions. But some, such as the antelopes, might. Some research is now in progress in East Africa to demonstrate the feasibility of joint management of wild and domestic herbivores under the suggested conditions. If wildlife populations are heavily utilized by harvesting on domestic stock ranches, their health condition is generally improved, thereby minimizing the disease transmission hazard. Vegetative measurements in Texas, showed that more efficient use of the range may be obtained by running one or several classes of livestock with deer in order to harvest the forage that deer do not utilize. Deer alone made inefficient use of the grass cover in their pastures (McMahon and Ramsey, 1965). According to livestock specialists the view that native grasslands a~

PRODUCTION O F WILD HERBIVOROUS MAMMALS

177

more productive and therefore more economic than improved grasslands cannot be maintained, except for such arid areas where it does not pay to make improvements. This statement does not imply that native grasses should be eliminated in favour of introduced species. Certain native grass species can be favoured, however, resulting in en increased carrying capacity of the range for both domestic and wild herbivores. One example might serve as an illustration: at the Muko Range Experiment Station in Uganda Cymbopogon afronardus, a highly unpalatable grass, was eliminated as a co-dominant with Themeda t r i a d r a and the effects of this removal on one and one-half to threeyear-old Ankole bullocks was studied. It was found in controlled experiments that the additional liveweight gain of the bullocks in areas where C. afronardws had been removed was 5 kg/ha/annum (Harrington, 1968).

X. R E C O M M E N D A T I OFN OR S RESEARCH Relatively little quantitative information is available on vegetational changes in Africa. How much has bush increased? What is the best stage in grass succession for grazing? How can it be attained and maintained by a particular or a number of species of grazer? More research effort should be devoted to obtaining better information about the optimum production potentials of different sites. Equally, little is known about the population densities at which different species of ungulates under a given set of environmental conditions, give maximum production. More attention should be given to the production, utilization, and accumulation of energy on range used by grazing animals. Other questions that require answers deal with the effects of overgrazing by livestock on the long-term productivity of wiid ungulates and the effects of fire on the productivity of grasslands and the physiology of plants. The reciprocal effects of wild and domestic herbivores on range vegetation and habitat should be carefully investigated. It also seems essential that further information be accumulated on the effect of harvesting pressure on the population structure and productivity of ungulates. These, and many other questions, need to be answered for a better understanding of the ecological basis of grassland productivity. S U M M A RAYN D CONCLUSIONS Based on a review of the literature, the author has made an effort to show that the interaction of various physical and biological factors

178

A. DE VOS

affecting the production of wild herbivorous mammals in grasslands is very complicated. A better understanding of the influence and interaction of these various factors, and specifically how they affect the production of herbivorous mammals, will be essential before intensive management of these mammals can be initiated. There is a need for more experimental work in which interactions of various factors are studied by a team of scientists in a designated study area over a long period of time. Life in the grasslands has been one of adjustment of both plants and animals to wet and dry cycles in weather. Drought is a severe limiting factor to the environment, but many mammals have developed adaptive mechanisms to it. Fire is generally a significant component of grassland environments. The importance of burning in determining the distribution and form of many plants as well as the composition of vegetation is stressed. The effect of burning on wildlife and range production is discussed. The effects of wild ungulates on the vegetation are discussed and particularly the effects of overgrazing. These effects are many and complicated. Wild herbivorous mammals are generally well adapted to natural range conditions. An imbalance, such as is caused by overgrazing, may result in much wastage of both animals and rangeland although some levels of deterioration may temporarily favour some species. A balanced stocking by a variety of species of animals is essential for optimum long-term production. Examples are cited of the effects of overgrazing on biotic communities and the physical environment. Rodents and lagomorphs can play a significant role in modifying grassland environments. While they can significantly compete with ungulates for forage in North America, this does not seem to be generally the case in Africa. Rodents, through their burrowing activities, aerate and loosen the soil and increase the percolation and infiltration of water. They may accelerate weathering of the soil and aid in incorporating humus into the soil. Various rodent activities, including their foraging and burrowing habits, have a significant effect upon the vegetation. Rodents can modify and influence the rate of plant succession. Rodent mounds and termitaria affect the physiography and biotic aspects of the environment. Changes may occur in the percentage of humus, minerals, drainage and aeration of the soil. Deserted termitaria may support a whole series of plant communities and may attract a number of burrowing mammals. They are often more intensively grazed and/or browsed by mammals than the surrounding vegetation. The limitations of biomass figures and better methods of assessing energy production are discussed.

PRODUCTION OF WILD HERBIVOROUS MAMMALS

179

The effects of degradation of the environment on the production of herbivorous mammals are demonstrated. The problems of game ranching and utilization and of range management for wild and domestic herbivores are discussed.

REFERENCES Albertson, F. W., Tomanek, G. W. and Riegel, A. (1957). Ecol. Monogr. 27 ( l ) , 27-44. Ecology of drought cycles and grazing intensity on grasslands of central Great Plains. Anderson, G. D. and Talbot, L. M. (1965). J. Ecol. 53,33-56. Soil factors affecting the distribution of the grassland types and their utilization by wild animals on the Serengeti Plains, Tanganyika. Arnold, J. F. (1942). Univ.Ariz. Coll. Tech. Bull. 98, 50-86. Forage consumption and preferences of experimentally fed Arizona and antelope jack rabbits. Arnold, L. W. (1942).J. Mammal. 23 (3),339-341. Notes on the life history of the sand pocket mouse. Bartlett, H. H. (1955, 1957). “Fire in Relation to Primitive Agriculture and Grazing in the Tropics”: annotated bibliography. 2 Vols. Univ. of Michigan, Ann Arbor. Bird, R. D. (1930). Ecology 11, 35-42. Biotic communities of the Aspen Parkland of Central Canada. Bond, R. M. (1945). Trans. N. Am. Wildl. C m f . 10, 229-234. Range rodents and plant succession. BourliBre, F. end Verschuren, J. (1960). Explor. Parc. natn. Albert. Introduction h 1’6cologie des ongul6s du Parc National Albert. Bruxelles. Bronson, F. H. and Tiemeier, 0. W. (1959).Ecology 40 (2), 194-198. The relationship of precipitation and black-tailed jack rabbit populations in Kansas. Buckman, H. 0. end Brady, N. C. (1962). “The Nature and Properties of Soils”, Sixth ed. The Macmillan Company, New York. Buechner, H. K. (1942). J . Mammal. 23, 346-348. Interrelationships between the pocket gopher and land use. Burpee, A. J. (ed.) (1908). Proc. Trans. R. SOC.Can. Series 3, Vol. 11,Section 11, No. 11,pp. 89-122. A n Adventurer from Hudson Bay. Carpenter, J. R. (1940). Ecol. Monogr. 10 (3), 618-684. The grassland biome. Child, G. Personal communication, dated 7.5.68. Clough, G. Personal communication. Costello, D. F. (1957). Ecology 38 ( l ) , 49-53. Application of ecology to range management. Crisp, D. J. (ed.) (1964). “Grazing in Terrestrial and Marine Environments.” Blackwell, Oxford. Darling, F. (1960). “Wildlife in an African Territory.” Oxford Univ. Press, Oxford. Dasmann R. F. (1962). Bull. epizoot. Dis. Afr. 10, 13-17. Game ranching in African land-use planning. Dasmann, R. F. (1964). “African Game Ranching.” Pergamon Press, Oxford. D a u b e k e , R. (1968). I n “Advances in Ecological Research” Ecology of fire in grasslands. (J.B. Cragg, ed.), Vol. V, pp. 209-266. Academic Press, London. Davis, D. E. and Golley, F. B. (1963). “Principles in Mammalogy.” Reinhold, New York.

180

A. DE VOS

Davison, E. (1966). New8 Bull. 2001. SOC.8th. Afr. 7 (2), 1-5. Capture and translocation of game animals. Dix, R. L. (1960).Ecology 41,49-56. The effects of burning on the mulch structure and species composition of grasslands in western North Dakota. Ellison, L. (1946). Ecology 27, 101-114. The pocket gopher in relation to soil erosion on mountain range. Ellison, L. (1960). Bot. Rev. 26 ( l ) ,2-66. Influence of grazing in plant succession of rangelands. Elton, C. S. (1966). “The Pattern of Animal Communities.” Methuen, London. Engelmann, M. D. (1966). I n “Advances in Ecological Research” (J.B. Cragg, ed.), Vol. 3, pp. 72-1 13. Academic Press, London. Energetics, terrestrial field studies, and animal productivity. Evans, F. C. (1951). J . Mammal. 32, 437-449. Notes on a population of the Striped Ground Squirrel (Citellw tridecemlineatua) in an abandoned field in Southern Michigan. Field, C. R. (1968). Proc. Wildl. Mngt. Land Use Symp. Nairobi, July 1967. Government Printer, Nairobi. The food habits of some wild ungulates in relation to land use and management. Formosov, A. N. (1928). Ecology 9 (a),4 4 9 4 6 0 . Mammalia in the steppe biocenose. Foster, J. B. Personal communication. Foster, J. B. and Coe, M. J. (1968). J . 2001.Res. 155, 4 1 3 4 2 5 . The biomass of game animals in Nairobi National Park, 1960-66. Glover, P. E. (1966). “The Role of Fire and other Human influences on the Savannah Habitat with some suggestions for further Research.” Paper presented a t F.A.O. Meeting in Khartoum, October 1966. Glover, P. E., Trump, E. C. and Wateridge, L. E. D. (1964). J . Ecol. 52, 367-377. Termitaria and vegetation patterns on the Loita Plains of Kenya. &innell, J. (1923). J . Mammal. 4, 137-149. The burrowing rodents of California as agents in soil formation. Grzimek, B. (1960). I n Roth, H. H. (1966). Gwynne, M. D. Personal communication, dated 16.5.68. Hanson, H. C. (1938). Bot. Sew. 4 (2), 51-82. Ecology of the grassland. I. Hanson, H. C. (1950). Bot. Rev. 16 (6), 283-361. Ecology of the grassland. 11. Hanington, G. M. (1968). Muko Expt. Station, Uganda. Progress Rep., May. Heady, H. F. (1960). “Range Management in East Africa.” Government Printer, Nairobi. Hesse, P. R. (1955). Tanganyika Notes and Records, No. 39, pp. 16-25. Some facts and fallacies about termite mounds. Horn, E. E. and Fitch, H. C. (1942). In “The San Joaquin Experimental Range” (C. B. Hutchinson and K. Otok, eds), pp. 96-129. Univ. Calif. Coll. Agr. Bull. 663, 1-145. Inter-relations of rodents and other wildlife of the range, pp. 96-129. Humphrey, R. T. (1962). “Range Ecology”, p. 234. Ronald Press, New York. Kalmbach, E. R. (1948). U.S.D.A. Yearbook 1948. Rodents, rabbits and gresslands. pp. 248-256. Koford, C. B. (1958). Wildl. Monogr. 3, 1-78. Prairie dogs, whitefaces and blue f.3T-a

Koford, C. B. (1960). In “Ecology and Management of Wild Grazing Animals in Temperate Zones” (F.Bourlidre, ed.), Symp. of IUCN, 8th Tech. Meeting, Warszawa, July 15-24, Morges, Switzerland. The prairie dog of the North American plains and its relations with plants, soil and land use.

PRODUCTION O F WILD HERBIVOROUS MAMMALS

181

Lamprey, H. P. (1964). E. Ajr. WiMl. J . 2, 1-47. Estimation of the large mammal densities, biomass and energy exchange in the Tarangire Game Reserve and the Masai Steppe in Tanganyika. Laws, R. M. (1964). In “Report Uganda Net. Parks, 1963”, pp. 23-30. The Nuffield Unit of Tropical Animal Ecology. Progress Report 1962-63. Ledger, H. P., Sachs, R. and Smith, N. S. (1967). Wld Rev. Anim. Production, Vol. I11 ( l l ) , 13-38. Wildlife and food production, with special reference to the semi-arid areas of tropics and sub-tropics. Macfadyen, A. (1964). I n “Grazing in Terrestrial and Marine Environments” (D. J. Crisp, ed.), pp. 3-25. Blackwell, Oxford. Energy flow in ecosystems and its exploitation by grazing. Maloiy, G. M. 0. and Heady, H. F. (1965). J . Range Mg~nt18 ( 5 ) , 269-272. Grazing conditions in Kenya Masailand. McMahon, C. A. and Ramsey, C. W. (1966). J. Range Mgmt 18 ( l ) , 1-7. Response of deer and livestock to controlled grazing in central Texas. Miller, R. S. (1964). Ecology 45 (2), 256-272. Ecology and distribution of pocket gophers (Geomyidae)in Colorado. Misonne, X. and Verschuren, J. (1966). MammalicC 30 (4), 517-537. Les Rongeurs et Lagomorphes de la region du Parc National du Serengeti (Tanzanie). Moss, E. H. (1932). J. Ecol. 20, 3 8 0 4 1 5 . The vegetation of Alberta, IV. The poplar association and related vegetation of Central Alberta. Murray, J. M. (1938). S. Ajr. J . Sci. 35, 288-297. An investigation of the interrelationships of the vegetation, soils and termites. Naveh, Z. (1966). Trop. Agric., Trin. 43 (2), 91-98. The need for integrated range research in East Africa. Osborn, B. (1942). Ecology 23 (2), 110-116. Prairie dogs in shinnery (oak scrub) savannah. Ovington, J. D. (1964). I n “Grazing in Terrestrial and Marine Environments” (D. J. Crisp, ed.), pp. 43-63. Blackwell, Oxford. Prairie, savanna and oakwood ecosystems at Cedar Creek. Peterson, R. A. (1967). Proc. Second Int. Sem. Integrated Surveys of Natural Grazing A r m 17-22 April 1967. Delft, Netherlands. Grassland surveys and grasslands production problems. Petrides, G. A. (1966). Trans. N.A. Wildl. Conj. 21 625-537. Big game densities and range carrying capacities in East Africa. Petrides, G. A. and Swank, W. G. (1965). Proc. 9th. Int. & a d d Congr. SBo Paulo, Brazil. pp. 831-841. Estimating the productivity and energy relations of an African elephant population. Pickford, G. D. (1932). Ecology 13 (2), 159-171. The influence of continued heavy grazing and of promiscuous burning on spring-fall ranges in Utah. Phillips, P. (1936). Ecology 17 (4), 673-679. The distribution of rodents in overgrazed and normal grasslands in Central Oklahoma. Ramsey, C. W. (1966). J. Range Mngt 18 ( 5 ) , 247-260. Potential economicreturns from deer as compared with livestock in the Edwards Plateau Region of Texas. Rattray, J. M. (1960). F.A.O. agric. stud. 49, 168. The grass cover of Africa. Reynolds, H. G. (1958). Ecol. Monogr. 28 (2), 111-127. The ecology of the Merriam Kangaroo rat (Dipodonzys memianti Mearns) on the grazing land of southern Arizona. Reynolds, H. G. (1964). J. Range Mngt 7 (a), 176-180. Some interrelations of the Merriam Kangaroo Rat to Velvet Mesquite.

182

A. DE VOS

Riney, Th. (1964).A rapid field technique and its application for describing conservation, status and trends in semi-arid pastoral lands. African soils 8 (2),159-258. Riney, Th. and Kettlitz, W. L. (1964).Marnmlia; 28, 188-248. Management of large mammals in the Transvaal. ROSS,B. A., Tester, J. R. and Breckenridge, W. J. (1968).Ecology 49 (l),172-177. Ecology of mima-type mounds in N. western Minnesota. Roth, H. H. (1966).Marnmlia; 30 (3), 397423. Game utilization in Rhodesia in 1967. Sauer, C. 0. (1950).J . Range Mngt 3, 16-21. Grassland climax, fire and man. Savory, C. R. (1905).Zoologica Afr. 1 (2),321-337. Game utilization in Rhodesia. Shantz, H. L. (1940).EcoZ. Mongr. 10,311-342. The relation of plant ecology to human welfare. Skinner, J. D. (1967). Anirn. Breed. A&. 35 (2), 177-186. An appraisal of the eland as a farm animal in Africa. Smith, C. C. (1940).Ecology 21 (3),381-397. The effect of overgrazing and erosion upon the biota of the mixed grass prairie of Oklahoma. Stewart, D. R. M. and Zaphiro, D. R. P. (1963). Marnmlia; 27 (a), 483-496. Biomass and density of wild herbivores in different East African habitats. Stoddart, L.A. (1967).J. Range Mngt 20 (2),304-307. What israngemanagement? Talbot, L. M. (1963).I n “The Ecology of Man in the Tropical Environment”. IUCN, Morges, New Ser. Publ. No. 4, p. 336. The biological productivity of the tropical savanna ecosystem. Talbot, L. M. (1964). Marnrnalia 28 (4), 613-619. The concept of biomass in African Wildlife research. Talbot, L. M. and Talbot, M. H. (1963).Tram. N.A. Wildl. Conf. 28, 466476. The high biomass of wild ungulates on East African savanna. Talbot, L. M.,Ledger, H. P. and Payne, W. J. A. (1962).Proc. 8th Int. Anim. Prod., pp. 206-210. Hamburg. The possibility of using wild animals for animal production in the semi-arid tropics of E. Africa. Taylor, C. R. and Lyman, C. P. (1967).Physiol. Zool.40 (3),280-296. A comparative study of the environmental physiology of an E. African antelope, the eland, and the Hereford steer. Taylor, W. P. (1930).Ecology 11 (3), 623-542. Methods of determining rodent preesures. Taylor, W. P. (1936).Ecology 16, 127-130. Some animal relations to soils. Taylor, W. P., Vorhies, C. T. and Lister, P. B. (1936).J. For. 33, 490-498. The relations of jack rabbits to grazing in southern Arizona. Tester, J. R. and Marshall, W. H. (1961).Univ. Minn. Mm. Nat. Hist. Occas. Papers 8.61. A study of certain plant and animal inter-relations on a native prairie in north-western Minnesota. Vesey-Fitzgerald, L. D. E. F. (1963). Proc. Ninth Technical Meeting, IUCN., Nairobi, 17-20 Sept. 1963 (not published). Grasslands. Vesey-Fitzgerald,L. D. E. F. (1966).E . Afr. Wildl. J . 3, 3848. The utilization of natural pastures by wild animals in the Rukwa Valley, Tanganyika. Yorhies, C. T. and Taylor, W. P. (1933). Univ. Arizona: Coll. Agr. and Exp. Stn. Tech. BuU. 49. The life histories and ecology of jack rabbits, l e p s alleni a d l e p s mlifornicua in relation to grazing in Arizona. Vorhies, C. T. and Taylor, W. P. (1940).Bull. A r k . agr. Exp. Stn. 86, 463-629. Life history and ecology of the white-throated woodrat, Neotoma albigub albigub Hartley, in relation to grazing in Arizona.

PRODUCTION OF WILD HERBIVOROUS MAMMALS

183

Weaver, J. E. and Albertson, F. W. (1936). Ecology 17 (a),567-639. Effects of the great drought on the prairies of Iowa, Nebraska, and Kansas. Weaver, J. E. and Fihzpatrick, F. J. (1934). Ecol. Monogr. 4 (2), 113-293. The prairie. Weaver, J. E. and Clements, F. E. (1938). “Plant Ecology”, p. 601. Weir, J. S. (1962). Proc. Fir& Fedn. Sci. Congr. (Salisbury), 301-305. A possible course of evolution of animal drinking holes (pans) and reflected changes in their biology. West, 0. (1965). Commonw. Bur. Pastures and Field Crops, Hurley, Berkshire, Eng., p. 53. Fire in vegetation and its use in pasture management, with special reference to tropical and subtropical Africa. Whitfield, C. J. and Beutner, E. L. (1938). Ecology 9 ( l ) ,26-37. Natural vegetation in the desert plain grassland.

This Page Intentionally Left Blank

A Simulation Model of Animal Movement Patterns D. B. SINIFF AND C. R. JESSEN

Department of Ecology and Behavioral Biology University of Minnesota, Minneapolis, Minnesota, U.S.A.

.

I. Introduction 11. Baais for a Simulation Model A. AnimalMovements B. Home Range . 111. T h e Simulation Model A. Empirice1 Requirements for a Successful Model B. Theoretical or Desirable Distributions which Appear Useful C. The Evolution of our Model D. Our Current Model . E. Comparison of Telemetry Data and Simulated Data . IV. Discussion and Future Developments . Acknowledgements . References

. .

.

.

.

.

186 187 187 197 199 199 200 203 210 210 213 217 218

I. INTRODUCTION Many biologists have indicated that non-migratory animals spend most of their lives in a particular area, and much study and some controversy has accompanied the development of this notion. The animals most commonly investigated in this regard have been mammals, particularly the small rodents. This chapter will not be unusual in this regard, and since the basic work is based on telemetry data, the bulk of the discussion will be directed toward mammals which have been monitored via telemetry, such as the red fox (Vulpes fulva) and the snowshoe hare ( L e p w americana) or the raccoon (Procyon lotor). However, the discussions of this paper would seem to have much wider application and may be useful in studies of other animal groups. I n general, we have studied movement patterns obtained from telemetry data in terms of the probability distributions which are involved as the animal travels in its normal daily activities. I n effect, the decisions made by the animal were reduced to functions of these probability distributions. We initially started with the assumption that each movement to a new location was independent of all previous 186

186

D. B. SINIFF AND C. R. JESSEN

movements. However, as our studies progressed, we found this assumption not realistic and further manipulation of the movement patterns was carried out. These studies were done by constructing a computer simulation model of animal movements and then applying the appropriate modifications as the obvious deviations from actual data presented themselves. Simulation modeling has been utilized in many sciences to imitate activities so that the probable outcome of procedures may be explored in advance of their application. This technique forces one to define all assumptions; thus, the effects of alternative assumptions about a particular process can be observed. This process of defining and then testing assumptions was particularly useful in the current endeavor, because it allowed us to modify our simulation procedure until a realistic movement pattern was observed. I n the past, this method has been applied to many biological problems. Gould and O’Regan (1965) used simulation to study the probable outcome of various forest management strategies. Watt (1966) gives a good discussion of the importance of simulation in resource management, and Paulik and Greenough (1966) discuss research involved with a simulation of a commercial fishery. Studies such as these indicate the importance of simulation modeling in studies of complex ecological systems, and have given impetus to our effort. Burt (1943), for mammals, gave some historical background and is generally recognized as the first to give a specific definition to the home range concept when he called the home range “that area traversed by the individual in its normal activities of food gathering, mating, and caring for young”. Hayne (1949) reviewed the concept with special reference to small mammals. Past studies of home range have been concerned primarily with small mammals and have used trap-markrecapture methods to determine the home range dimensions. Various methods have been proposed to quantify the home range characteristics derived from recapture data. Hayne (1949) considered the patterns of home range use by meadow mice (Microtus sp.) in terms of the distribution of recaptures from the geometric center; he called this location the center of activity. Dice and Clark (1953) examined the concept further by computing the recapture radii from the center of activity for the Deer Mouse (Peromyscus maniculatus bairdii). They were interested in the probability distribution which would fit the distribution of recapture radii and tested for conformity to a Pearson Type 3 probability function. However, significant differences were found between the Pearson Type 3 distribution and the observed data. Calhoun and Casby (1958), using data on Harvest Mice (Rheithrodontomys sp.), also studied the distribution of radii from the center of

ANIMAL MOVEMENT PATTERNS

187

activity. They found that a bivariate normal distribution (expressed in terms of polar coordinates) was a satisfactory approximation to their data. Brown (1962) and Sanderson (1966) have reviewed in detail the concept of home range and indicated the numerous problems involved. Jorgensen (1968) expanded the circular concept of home range even further, and considered the probability of contact for animals with overlapping home ranges. This author adopted the model proposed by Calhoun and Casby (1958) and assumed a circular normal distribution was a satisfactory representation of home range patterns. He estimated the probability of interaction by solving for the probability that two animals were located in the same area of overlap given that each possessed a circular normal home range with a certain amount of overlap. The home range patterns we have observed with telemetry data are in general not adequately described by the circular normal distribution (Tester and Siniff, 1965). Within a home range there are often several centers of activity which may shift, depending on season or other environmental factors. Therefore, the utilization of the circular normal distribution model of a home range in the analysis of telemetry data has not proved satisfactory. The exact nature of a satisfactory mathematical model to describe home ranges based on the telemetry data is not clear at this time. This problem has been a primary reason for looking to computer simulation for an adequate model. I n this paper we describe some of the progress we have made in this area. The endproduct of our effort is certainly not realized within this paper, and it is hoped that the simulation model presented here will stimulate both theoretical and applied research in the areas of home range determination, distribution of animal movement patterns, studies of social interaction and other related fields.

11. B A S I S F O R

A

SIMULATION MODEL

Attempts to simulate animal movement without some knowledge of actual home range use would be folly. Many man-hours of effort have been directed towards a better understanding and a better measurement of animal movement. The following summarizes the results of some of those efforts which were necessary before a reasonable simulation process could be initiated.

A.

ANIMAL MOVEMENTS

Figure 1 illustrates a few basic characteristics of animal movement paths as viewed by telemetry. This pattern gives the impression that

188

D. B. SINIFF AND C. R. JESSEN

the animal moves between point locations which have been established by telemetry. Each point location established by telemetry is usually referred to as a “fix”. The telemetry data which provides the basis for these studies was obtained from the University of Minnesota’s Cedar Creek automatic tracking system (Cochran et al., 1965). The Cedar Creek system continually monitors movement of animals carrying miniature radio transmitters. The radio signals are received by rotating

FIG 1. An example of red fox movement a8 obtained from telemetry data.

antennas supported on two towers spaced one-half mile apart. After amplification and conversion, the signals are fed to a 52-channel receiving and recording system located in a laboratory between the towers. Time and bearing data for up to 52 animals are continually recorded on 16-mm film. An operator using a microfilm reader takes bearings from the film as desired. These bearing data are converted, by the computer, into location data by triangulation methods. The mechanical accuracy of the system is 0.5’. A full description of the system is found in Cochran et al. (1964).

ANIMAL MOVEMENT PATTERNS

189

The mammals studied with the Cedar Creek system generally occupy some rather specific area. There are certain locations within their home ranges which are intensively used; others are rarely entered (see for example Turkowski and Mech, 1968). The edge of the home range is fairly well defined, although shifts in utilization pattern both within and on the periphery of the home range occur. These characteristics vary among species, with season, and among different age and sex categories of each species. For the movement pattern as viewed via telemetry, two measures are involved: (1) the relative angle (in this case measured in a clockwise direction) between three successive locations and (2) the distance from an initial location to the point where the next location is recorded. The observation of many successive fixes made it possible to pool data to form the distribution of angles between fixes and the distribution of distances between successive locations. The general form of these distributions can be observed from the Cedar Creek tracking system. The biological counterpart of the way relative angles are used in this report are as follows. A relative angle of 180” is the direction “straight ahead” while angles of 0” or 360” are “directly behind”. There are systematic errors in the observed distributions because the positions are obtained by triangulation from two receiving towers. A discussion of these telemetry problems was presented by Heezen and Tester (1967). Even though the observed distributions contain the errors from triangulation, we feel the general form of the observed distributions are proper and representative of the actual distributions. Data from snowshoe hares and red fox gave some insight into the form of these distributions. This examination is not intended to be an exhaustive study but rather is intended to furnish evidence of the general form of the distributions involved. All data for red fox were recorded as described by Sargeant et al. (1967a), and show more consistency in sampling than the data for the other species. Data for the snowshoe hare represent the efforts of two investigators and were originally used for rather diverse purposes. Although they show some variation in sampling interval between successive fixes, they are useful for the purposes proposed here. Several observed rate of travel distributions for red fox are shown in Fig. 2. These animals comprised part of a family group; male (108) and female (103) which shared the same home range, and a juvenile (132) which was one of their pups. All of these distributions were made by observing the distances moved in 8,9,10,11, and 12 minute sampling intervals within the time of the year shown. Values are given in feet per minute and all instances where no movement occurred were eliminated from the distributions. The data were obtained from the

D. B. SINIFF AND C. R. JESSEN

190

Red fox 103 -Adult

0.15

female

0.15 6 May to 3 June, 1964

8 April to 6 May, 1964 N = 277 0.10

0.10

0.05

0.05

0

0

5

105

205

Red fox 108 - Adult male 0.15 10 April to 6 May, 1964

0.15-

-e

6 May to 3 June, 1964

v)

2 0.10-

0.10

0 C

0.05-

0 05

a 0

2

n

0-

0

105

i

5

205

105

205

Red fox 132 - Juvenile

-

0.25 0.20 16 July to 13 Aug, 1965

4 June to 16 July, 1965 0.15

0.10 0.05

5

105

0 205 5 Rate of speed in feet per rnin

105

205

FIG. 2. Some observed distributions of distance traveled per minute for red fox. These were obtained by using distance traveled in 8 , 9 , 10 and 11minutes and dividing distance by time t o obtain rate in feet per minute.

time period shown; however, within this interval, periods may have occurred where data were not obtained because of interference with the transmitted signal. These observed distributions show that distance moved per minute is represented by a unimodal curve. The curve rises rather sharply

191

ANIMAL MOVEMENT PATTERNS 9

- I I Min sampling interval between fixes

Smwshoe hore 225 Adult female

5

5

105

105

5

105

01 In

z

.c

6

4

E

0.6

- 6 Min sompling interval between fixes 0.6

0.5

0.5

0.4

Snowshoe hare 201 Adult female 0.4 I6 Jan to 29Jan,

0.3

0.3

0.2

0.2

0.1

0.1

C

Snowshoe hare 201

Snowshoe hare 201 Adult female IIFeb to I6 Feb,

I

105

105

5

105

Rate of speed in feet per min

Fio. 3. Some observed distributionsof distance traveled per minute for snowshoe hare. These were obtained by using the sampling interval &own above and dividing distance moved by the time interval in minutes to obtain feet per minute.

from the origin and has a long right-hand tail. The only obvious difference among the distributions for these individuals or periods of time is the general slower movement of the juvenile during the period 4 June to 16 July 1965. At that time this animal was still dependent on parental care and had not expanded its movements to cover the

192

D. B. SINIFF AND C. R. JESSEN

full parental home range. The rather uniform appearance of these distributions is what one might expect because normal travel speed may be rather constant for adult red fox (Sargeant et al., 1967b). Red fox 103 8 April to 6 May, 1964

0.10

- Adult femole 0.10

0.05

6 May to 3,June, 1964

0.05

I

180

I

360

I

0

I

180

360

Red fox 108 - Adult male

Red fox 132 - Juvenile

16 July to 13 Aug, 1965

4 June to 16 July, 1965 0.q

0.101

005

0

I80

360 Angle between successive positions

FIG. 4. Some observed distributions of relative angles turned (clockwise) between successive fixes for red fox.

Samples of observed rate of travel distributions for snowshoe hares are shown in Fig. 3. Hares 225 and 201 were adult females and hare 212 was an adult male. Again we observe a unimodal curve, exhibiting& general slower rate of travel than for the red fox. These data also show

ANIMAL MOVEMENT PATTERNS

193

that as the sampling interval lengthened the curve is shifted to the left as the average speed of movement becomes less. Instances of “notmoving” were eliminated from these distributions. The same data groups which were examined for rate of travel per unit time were used to derive the observed relative angle of movement distributions. Observed data for the adult female and adult male red fox (Fig. 4) are similar with a general unimodal appearance with the peak at about 180 degrees. Sargeant et al. (1965) compared red fox tracks in the snow to the telemetry data, and gave data which indicated that red fox traveled in a general linear fashion with occasional stops for concentrated movement in one location. The juvenile red fox demonstrated a rather different pattern for the Grst period shown in Fig. 4. Prom 4 June to 16 July the animal was dependent on parental care and inhabited a small area. During the second period (16 July to 13 August) it showed a trend toward the characteristic distributions of the adult animals indicating the transition to adult traveling habits. Observed angle of movement distributions for the snowshoe hares are shown in Fig. 5. These distributions are rather different from those of the adult red fox and manifest both a bimodal and uniform appearance. The distribution for hare 212 differed from the others in that it shows a much greater proportion of the relative angles around 0’ and 360”. This animal had a home range which was long and linear, but located in an area of poorer telemetry resolution than the home ranges of 201 and 225. It is probable that the shape of the home range of 212 was the most important factor contributing to the form of the observed distributions; however, the telemetry system bias may have also affected the results. The differences in the general pattern between these two species gives insight into how each uses its home range. Rongstad (personal communication) indicated that tracks in the snow and telemetry data showed that snowshoe hares utilized certain areas very intensively and spent a high proportion of their time (75%) apparently milling about, probably feeding. I n addition to the distributions of relative angle between successive fixes and distance moved per unit time, in the simulation model, there is the additional consideration of the duration of the rest and movement periods. I n general, telemetry data have indicated that red foxes, raccoons, snowshoe hares, and cottontail rabbits (Sylvilagus firidanus) move during the night and remain relatively stationary during the day (Mech et al., 1966a, b). On the other hand, the white-tailed deer (Odocoileus virginianus) at Cedar Creek gave day and night movement patterns which were similar in form (Moulton, 1966). Nocturnal species start moving about sunset and, apart from a few rest periods

194

D. B. SINIFF AND C. R. JESSEN Snowshoe hare 201 16 Jon to 29 Jan.1964

Snowshoe hare 201 IIFeb to 16 Feb, 1964

0.10

0.10

0.05

0.05

0

0

Snowshoe hare 201 7 A p r i l to 5 Moy,1964

180

360

Snowshoe hare 212 1 Sept to 16 Sept, 1966

0.10

0.05

0

I80

360

m Snowshoe hare 212 16 Sept to I Oct, 1966

Snowshoe hare 225 1 Sept to 1 Oct, 1966

0-10

0’1°1

0.05

0

I do

360

b

Id0

3hO

Angle between successive positions

FIG.6. Some observed distributions of relative angles turned (clockwise) between successive fixes for snowshoe hare.

scattered throughout the night, stop about sunrise. Thus, for the purposes proposed here, a t any one moment an animal can be classified as either “moving” or “not moving”. If the lengths of movement and rest periods are observed over a period of time, the results form distributions which give the probability of the duration of movement or rest for some chosen time interval. Many factors influence the form of these distributions and, thus, differences in form provide criteria for biological interpretation. Tables I and I1 give examples of frequencies of duration of rest and

195

ANIMAL MOVEMENT PATTERNS

TABLEI Duration of night re& for red fox

Time interval (min) 0-30 31-60 61-90 91-120 121-150 151-180 181-210 211-240 241-270 over 270

Totals

Juvenile (132) Frequency (yo) 34 23 17 9 4 2

36.6 24.6 18.3 9.7 4.3 2-2

0

0.0

1 3 -

1.1 3.2

-

93

100.0

Adults (103 and 108) Frequency (yo) 37 38 23 15 8 2 4 1

28.9 29.7 18.0 11.7 6.3 1*6 3.1 0.7

128

100.0

TABLEI1 Duration of night moves for three individuals of red fox

Time interval (min) &30 31-60 61-90 91-120 121-150 151-180 181-2 10 2 11-240 241-270 27 1-300 301-330 331-360 361-390 391-420 421-450 451-480 48 1-5 10 511-540 541-570 671-600

over 600

Totals H

Juvenile (132) Frequency (yo) 24 19 16 20 12 8 4 5 3 3 2 2

1

-

0-8 -

1

0.8

6

12-3 6.8 10.2 8.3 6-8 4.8 6.8 9.5 5.4 6.1 2-0 3.4 2.0 1*4 2.0 0.7 2.0 3.4 0.7 2.0 3-4

120

100.0

147

100.0

-

20.0 15.8 13.3 16.7 10.0 6.7 3.3 4.2 2.5 2.5 1.7 1.7

Adults (103 and 108) Frequency ( % )

-

-

18 10 15 12 10 7 10 14 8 9 3 5 3 2 3 1 3 5 1 3

196

D. B. S I N I F F AND C . R. JESSEN

movement periods for the juvenile and adult red fox considered in Figs. 2 and 4. Sargeant et al. (1967b) discuss differences in these distributions for red fox relative to season, time of day, and age. Extraction of data of this type by radio telemetry requires the interpretation of RELRTIONSHIP BETWEEN OISTANCE TRRVELEtl RND RNGLE BETWEEN FIXES RNIMRL 103 FROM 91 W 5'42 TO 5 / 6 ' 56 1969

+ Z400 -

'+

+ + +

++

1600

-

+

+

+

++

+ +

*+

+

+

+ +++

+ +

+

$++

+ + .

qELqTIONSHIP BETWEEN OISTRNCE TRRVELED RND RNGLE BETWEEN FIXES RNIMRL 201 FROM I / I&' 1725 TO I / 29' 655 1969

I+ 0

+ +

t

I600

+

+

+ +

* +++

+

+

180

360

ANGLE

FIG.6. Some examples of the relationship between angle turned (clockwise) and the corresponding distance moved for a set of data for red fox and showshoe hare.

changes in signal quality caused by movement of the animal (Moulton, 1966). Duration of movement and rest periods for snowshoe hares have not been obtained. It could be assumed that fast rates of travel would be closely associated with linear movements and would therefore exhibit relative

197

ANIMAL MOVEMENT PATTERNS

angles between successive fixes of around 180'. Because the simulation model assumes that there is no relationship between distance moved per unit time and angle between successive fixes, these data were investigated, to determine the validity of this assumption, by plotting angle and the corresponding distance moved. Figure 6 is a representative example of these plots and indicates that no apparent relationship exists. B.

HOME

RANGE

I n the analysis of telemetry data there is a general problem of quantifying the differences in movement patterns that are observed between species or even within the same species. For example, one can construct a map of movements which may show that the general appearance of movements of snowshoe hare differ from those of red fox. To measure the difference quantitatively is not an easy task. I n general, we can observe that the overall distributional pattern of fixes on the home range is not random but is a contagious distribution. This occurs because there is a high probability that an animal will enter a desirable area and a low probability that an animal will enter an undesirable area. To measure the differences in spatial patterns, one needs a method for studying the clustering or contagion of the fixes. For movement data, preliminary studies have suggested that the square sampling unit may be useful (Tester and Siniff, 1965). A square sampling unit is often used for studies in plant ecology where the interest is the degree of clumping of certain plant species (Greig-Smith, 1965). The area of measurement of contagion in biological populations has generated considerable discussion in the literature (Seal, 1966; Ghent, 1066).

The contagion of fixes was measured by comparison of observed data to that predicted by the negative binomial distribution. The home range was partitioned into square sub-units and the number of fixes per square was tallied. Robinson (1954) has suggested this method for measurement of contagion of plant populations. Bliss and Fisher (1953) give a good discussion of the negative binomial and examples of its utility in biological studies. The negative binomial density function may have the form:

x=o, 1, 2,

. ..

where m is the arithmetic mean and k is a positive exponent. This is an extension of the well-known Poisson series in which the population mean is equal to the variance. For the negative binomial the variance

198

D. B. SINIFF AND C . R. JESSEN

is larger than the mean, and as clustering decreases and the variance approaches the mean, the parameter k becomes larger. I n this study the agreement of the observed data to the negative binomial and the relative changes in the dispersion parameter (k) were evaluated. Because areas occur within the home range where no fixes fall and also because the edge of the home range lacks definition to an observer, no observed value was possible for the number of squares not containing fixes. Thus, if one is to fit the negative binomial to such data, it must be truncated to allow for the zero frequency missing. Fitting of the truncated case was carried out according to Hartley (1958). For our data, the squares were 528 x 528 f t (16 x 16 m) on a side for the red fox data (with the exception of animal 132, 4 June to 16 July, where the squares were 268 x 268 f t (8 x 8 m) and squares of 132 x 132 ft (4 x 4 m) on a side were used for the snowshoe hare. The estimated values of the k parameters are shown in Table 111. These data were TABLEI11 Estimates of the dispersion parameter (k)from fitting of the negative binomial to distributions derived from telemetry data; Animal

k parameter

Chi-square value

Red Fox 103; 8 April to 6 May 1964 Red Fox 103; 6 May to 3 June 1964 Red Fox 108; 10 April to 6 May 1964 Red Fox 108; 6 May to 3 June 1964 Red Fox 132; 4 June to 16 July 1965 Red Fox 132; 16 July to 13 Aug. 1965 Snowshoe hare 225; 1 Sept. to 1 Oct. 1966 Snowshoe hare 212; 1 Sept to 16 Sept. 1966 Snowshoe hare 212; 16 Sept. to 1 Oct. 1966 Snowshoe hare 201; 16 Jan. to 29 Jan. 1964 Snowshoe hare 201; 11 Feb. to 16 Feb. 1964 Snowshoe hare 201; 7 April to 5 May 1964

0.421 0.413 0.190 0.132 0.627 0.296 0.828 0.112 0.193 0.310 0.189 0.381

8.245 3.376 10.450' 1.953 4.442 1.045 5*224* 12.350* 5.437 1.999 6.691 11.804

* Significantly different from the predicted negative binomial distribution at the 0.05 probability level. subjected to goodness of fit comparisons by the usual chi-square criteria (Bliss and Fisher, 1953)) and the resulting chi-square values are also shown in Table 111. Significant chi-square values are indicated (0.05 probability level). These findings show that the negative binomial makes a satisfactory approximation to data of this type and is useful in describing degrees of contagion. Some speculation as to why the negative binomial approximates the data of this type is given in the discussion of this paper.

ANIMAL MOVEMENT PATTERNS

199

As previously mentioned, the area in which an animal makes its residence has been termed home range and not all areas within the home range receive equal usage by the animal. We believe any probability distribution which can describe “usage of the home range” allows the biologist another measure with which to describe the utilization of the home range space, and we suggest the negative binomial as satisfactory for this purpose. Certain limitations must be considered in the relationship between home range, the sampling units, the number of “fixes”, and the species. The home range of the species must be divided into appropriate sized sub-units, if the negative binomial distribution is to be a satisfactory approximation and is to be useful in describing degrees of contagion. We, therefore, have confined the simulations reported herein to those sub-units which have been investigated using telemetry data and have been found to be satisfactory. 111. THE SIMULATION MODEL A.

E M P I R I C A L R E Q U I R E M E N T S FOR A S U C C E S S F U L M O D E L

Our initial attempts to simulate animal movements have been limited to some portion of an animal’s life span, where movements are not complicated by such factors as migration, breeding behaviour, the transition from juvenile to adult, or other major events which may occur during the lifetime of the individual. It is in our present opinion that each of these major events must be dealt with separately as a special case. Successful simulation a t this time is defined as the generation of animal movement and the simulated animal’s use of a defined home range in such a manner that the simulated data cannot be distinguished from the telemetry data. The most difficult “fit” to accomplish in the simulation is the use of home range. I n measuring home range use via the negative binomial it should be remembered that the parameters of the simulated movement are the results of the simulated movement and not the cause of the movements. A discussion of the parameters and explanations of their use follow. If the model is confined to some arbitrary finite time period and if migration is excluded, then by such restriction the home range will also be finite in that time period. During the simulation, methods were developed to set “in memory” the animal’s home range. I n doing this we were able to choose an appropriate home range size and shape and then to simulate movements within this chosen home range. The desired end point of this technique was home range use, typical of what we might have observed via telemetry within that area. Such home

200

D. B. SINIFF AND C. R. JESSEN

range confinement may be interpreted as the use of an established home range.

B.

T H E O R E T I C A L OR D E S I R A B L E D I S T R I B U T I O N S WHICH A P P EA R U S E F U L

The mathematical or theoretical distributions which are suggested as useful aids in simulation or description of biological movements are not meant to be an exhaustive list. The theoretical justification of these distributions will not be attempted here. For the distributions of “angle between successive fixes” some circular probability distribution will be appropriate. These distributions have their total probabilities spread about the circumference of a circle. If the animal has no preferred directions the points would be spread rather uniformly about the circle and would be considered to

FIG.7. Linear diagrams of the circular normal distribution for different values of c, with point of maximum probability at zero. (After Batschelet, 1966.)

follow a uniform circular distribution. I n this case, each of the 360’ would have an equal probability of occurring. A theoretical distribution, the circular normal, is often used in the study of such data. This type of distribution would occur, in the case of these data, when the preferred movement direction is concentrated symmetrically about a particular bearing. The circular normal which is a unimodal distribution was introduced by Von Mises in 1918, and is sometimes referred to as the Von Mises distribution. It is characterized by two parameters, herein referred to as m and c. The parameter m is the angle of maximum probability, i.e. the modal direction, and c is generally designated the parameter of concentration because as c increases the spread of the distribution becomes less. Figure 7 shows

201

ANIMAL MOVEMENT PATTERNS

diagrams of this distribution for different values of c. The density function is:

where I,(c) stands for the “Bessell function of purely imaginary argument of order zero” (Batschelet, 1965, p. 10). Its purpose is to force the entire cumulative distribution to take on a value of one, i.e. so that the area under the curve equals 1.0. The distribution becomes the uniform distribution case when c equals zero. A good discussion of the circular normal and other circular probability distributions can be found in Batschelet (1965). ANGLE

.u

DlSTRlSUTlONS

0

DEGREES

0

SCALE

Id0 DEGREES

360

2 MILES

FIG.8. Some examples of movement patterns obtained utilizing bimodal distribution in the simulation model to represent angle between successive fixes.

202

D. B. SINIFF AND C. R. JESSEN

Another theoretical distribution which may be useful in describing the angle distribution is one with bimodal form. Such a distribution DISTANCE TRAVELED

DISTRIBUTIONS

010

>

t

-

$

0.05

0 (L

GAMMA

a.2

SCALE 2 MILES

FIG. 9. Some examples of movement patterns obtained utilizing different distance travelled distributions in the simulation model. The mode of the distributions remains the aame and only the variance is changed.

has been described by Greenwood and Durand (1955) and has a central symmetry; which means that the circular distribution is determined within any 180' sector, and the complementary sector repeats the same

ANIMAL MOVEMENT PATTERNS

203

pattern. Again, two parameters describe this distribution, and examples of the form are shown in the graphs of Fig. 8. The density function is given by: 1

ec cos 2(2-m)

f(.)=&) and as shown is similar to the density function of the circular normal. A discussion of this distribution is also given in Batschelet (1965). These two theoretical distributions can be used to describe the angle between successive fixes. Actual data may deviate considerably from these but they remain useful for studying general patterns. The theoretical distributions which may approximate the observed data for duration of movement periods, duration of rest periods and distance traveled may be many. These data constitute, as in the case of the angles, continuous distributions which may take on any value greater than zero, with some practical upper limit. It has been observed that the distance traveled distributions were unimodal and generally rose quickly from zero to some peak and then had a long right-hand tail. This general form suggests a gamma distribution. This distribution is characterized by two parameters, and the density functions can be given by:

where a is greater than -1, ,3 greater than zero and x may assume any value o<x < co (Wadsworth and Bryan, 1960). This distribution is skewed to the right for all values of a and /3 but as a gets larger the skewness becomes less pronounced. The right side of Fig. 9 shows examples of this distribution where a and ,3 vary.

c.

T H E EVOLUTION O F OUR MODEL

We have moved through many levels of refinement in developing a satisfactory simulation model of animal movement. Initially, we tried using the four distributions (distance traveled, angle between successive fixes, duration of rest, and duration of movement) to provide a basis for the simulation model. Figure 10 presents these initial concepts and distributions in a related picture, giving the flow of logic of our first simulation attempt. I n this model, the movement at each point was independent of every other choice. For example, the angle chosen for movement to the next fix was not influenced by the distance chosen

204

D. B. SINIFF AND C. R. JESSEN

or by the location on the home range. Figure 11 shows an example of the type of movement pattern one can obtain using this simulation procedure. This plot (Fig. 11) was produced using the logic and distributions shown in Fig. 10 and allowed the simulation to run for 1000 fixes. The overall pattern can be changed by varying the form of the angle distribution and the distance traveled distribution. A further analysis is given below.

J

3'0

4

c

420

2io

30

2io

420

Duration of move (min)

Duration of rest (min)

Establish positions from the following distributions

I

Repeat the previous position

A sotisfied

Speed of movement 'eet moved per unit time)

2b

I60

7

360

~~~l~ between successive fixes

8

FIG.10. Block diagram of simulation procedure proposed for animal movement. The distributions used in this figure are hypothetical.

The effect of changing the form of the distance traveled distribution for three gamma distributions is illustrated in Fig. 9. The model remained constant and only the variance of distribution was changed in these comparisons. It is clear that a change in the mode without a

ANIMAL MOVEMENT PATTERNS

205

change in the variance causes only the scale of the pattern produced to be different. The angle distribution utilized in these comparisons was the observed distribution for red fox 108 6 May to 3 June 1964.

FIQ. 11. An example of a simulated movement pattern obtained from the distributions and process shown in Fig. 10.

The effect of changing the angle distribution from the uniform distribution to the circular normal distribution with a mode of 180" and the dispersion parameter (c) equal to 1 resulted in the movement patterns shown in Pig. 12 for 1000 locations each. The distance traveled distribution for the above comparisons was the observed data for red fox 108 6 May to 3 June 1964. The form of the angle distribution is shown in the insert of the simulation movement maps. The path of travel is erratic with a noticeable clumped pattern when we used a uniform angular distribution. Using the circular normal distribution with a mode of 180°, the simulated home range changes so that the travel path becomes more linear. The uniform case resembles a pattern of snowshoe hare movement while the circular normal case has much the appearance of fox travel. Figure 8 shows the pattern obtained using

206

D. B. SINIFF AND C. R. JESSEN

examples of bi-modal distributions. When the distribution is only slightly bi-modal (i.e. c=0.2) the pattern differs little from the uniform case. When the distribution is more sharply peaked (i.e. c=l.O) the pattern changes considerably. This change is due to many approximately 0" and 360' relative angles of direction. ANGLE

DISTRIBUTIONS

DEGREES

Fra. 12. Contrasts of the changes in pattern obtained by different angle distributions in the simulation model.

After the visual comparisons were considered, the observed distributions shown in Figs. 2, 3, 4 and 5 were used in the simulation model shown in Fig. 10, and 500 positions were generated for each simulation. The values of the k parameter derived from fitting the negative binomial are shown in Table IV. The corresponding chi-square values indicating goodness of fit are shown. Comparing these parameters to those for actual data (Table 111)i t is seen that, in general, lower values

207

ANIMAL MOVEMENT PATTERNS

TABLEIV Estimates of the dispersion parameter (k)from fitting of the negative binomial to distributions derived from the simulation model shown in Fig. 10. Animal

Red Fox 103 Red Fox 103 Red Fox 108 Red Fox 108 Red Fox 132 Red Fox 132 Snowshoe hare Snowshoe hare Snowshoe hare Snowshoe hare Snowshoe hare Snowshoe hare

* Significantly

225 212 212 201 201 201

k parameters 1.997 0.810 1.287 1.532 2.622 0.682 2.340 1.088 0.802 1.241 1.275 0.866

1.474 1.868 2.482 0.662 2.723 4.802 0.876 0.953 0.904 1.022 0.890 0.736

Chi-square values 1 *564 1.572 2.368 5.055 0.387 9.547* 2.388 11.900* 3.485 5.777 3.872 4.714

3.020 9*128* 3.154 3.507 4.127 0.929 2.928 2.655 4.275 1.289 3.205 4.844

different from the predicted negative binomial distribution at the

0.06 probability level.

exist for the actual data than for the simulated data. This suggests that the former presented more of a clumped pattern than the latter. The reason for this is probably the re-use of specific areas. Also simulations based on this particular model revealed that, given enough simulated positions, the movement would usually include a much larger area than would be expected from an actual home range. The tendency to “wander off” was more evident in the case of unimodal distributions with a mode a t 180°, than for bi-modal or uniform cases. The bimodal and uniform distribution cases displayed some tendency to “wander off” after a large number of positions had been simulated. These tendencies varied greatly depending on the random number sequence chosen. Simulations of the above type exemplified the need for more information concerning the establishment of the home range boundary and the re-use of preferred areas. The following is a discussion of how we solved this problem in the simulation model. It was obvious to us that an animal usually recognizes some boundary of its home range and separates desirable and undesirable areas within the home range. The conclusion is that an animal moving within a home range returns with high probability to areas which are desirable and rarely enters areas which are undesirable. The reasons why an animal may decide that an area is desirable or undesirable are not well understood. We only observed that this phenomenon occurred. The decision was made that we should work with weighted probabilities in the simulation. Therefore, we directed an animal to areas it

208

D. B. SINIFF AND C. R. JESSEN

previously occupied with a higher probability than to areas it had not previously occupied. We have developed several methods of implementing this manipulation. These methods may be partitioned into two general approaches. The fist was that of a simple presence-absence concept where the next modal direction was weighted in favor of areas which contained previous fixes. The second was more complex and takes on the more quantitative approach to the problem by arriving at a modal direction through formulas and functions. Further explanations will be given below. When we initially began working with weighted probabilities, we decided to let the simulation “run” for some finite number of fixes to establish a home range on which to work. We let the simulation “run” 100 locations and then initiated the restrictive movement phase. I n this restrictive movement phase we located previous fixes which were in close proximity to the present location of the “animal”. At this time the next movement was directed toward the area where previous fixes were found. This operation was encouraging as the pattern obtained after simulation of several hundred positions was a closer approximation to telemetry movement patterns than we had previously obtained. The simulated movement remained within a relatively small area, and the clumping pattern approached that observed with actual telemetry data. At this stage of development we realized, however, that the total simulation of animal movement, e.g. 400-800 positions, was dictated principally by the initial 100 positions. The results from the above type of simulation tended to reflect correct biotic use of the home range but generated a home range which was strongly reflective of the initial 100 positions and was a complicating factor in the perfection of good simulation distributions. Valid comparisons of the simulated animal movement (as measured by the k parameter estimate of the negative binomial distribution) were confounded by unequal home range size and shape. It should not be inferred that we consider the home range size and shape to be the major factor in the use of the home range by either simulation or actual animal use. It complicated the assessment of the technique and the problem of trying to decide whether distribution changes actually “improved” the animal simulation. The obvious correction for this complication was to use a constant initial home range to perfect the controlling distributions. This was accomplished by using an actual telemetry home range or by creating an artificial home range for the species. The results of succeeding simulations utilizing a constant initial area were, as expected, less variable between simulations and more critical assessments were allowed.

0

A. THE INITIATION OF: A PROGRAM START : A SIMULATION

0:

A HOVEHENT CYCLE

0.

8. THE DECISIONS OF MOVEMENT DIRECTION.

Choosr ,he modal

d i n t i t i (unction with the

I C. THE MOVEMENT FROU ONE LOCATION TO THE NEXT.

I D. THE DECISIONS CONCERNING ANALYSIS OF DATA AND CONTINUED SIMULATION.

pprmfed

10

E’

DEC1s’oNlNVDLWNG

AND

z point

where mrl~r8s01 d m

ch. duntlen d nll. approprim lor the

n1.rir. .Z.‘I. ~

Fro. 13. The flow chart for our current simulation model. Glossary of some terms used in the chart: Modal direction: the most probable direction of travel for the next move. It is measured in the X-Y coordinate system. Location: the “fix” given in the X-Y coordinate system. Special case: an environmental or biological circumstance which will govern the next move. Duration of movement: time laps before the next rest period. It may contain many moves or “fixes”.

210

D . B. SINIFF AND C. R. JESSEN

D.

OUR C U R R E N T MODEL

We hope it is obvious that we do not consider the current model either complete or perfected. It is continuously undergoing changes. Figure 13 gives our simulation flow chart in summary form. It is our desire to depict by this flow chart how our model has actually been implemented. A few of the terms used in the flow chart are explained at the bottom of the chart. Programs now in existence are generally of the form described in the flow diagram shown in Fig. 13. These may make use of circular normal distributions where the parameter c may be continuous between the value 0 and 25. The value of c may be solved anew after each move, or may be set equal to a constant for a whole simulation. The “home range” may be set to be any shape or may be of any size in our simulation. Home ranges with an initial regular shape; for example, circles and ellipses, may be generated, removed, regenerated, enlarged, made smaller or moved to other map coordinates, or may combine two or more of these overlapping regular shapes to form other irregular shapes. These options may be chosen and held constant for the entire simulation or they may be changed with any frequency desired. One or more avoidance areas of any shape or size can also be generated with any home range, thus creating lakes, cities, or other habitat avoidance areas. To date, home range use by these more restrictive criteria have reshlted in a better correspondence of the Simulation data with the telemetry data.

E.

COMPARISON O F T E L E M E T R Y

DATA A N D

SIMULATED DATA

Comparisons may take on several forms and it is therefore difficult to choose examples of simulation since the possibilities are many. At the present time with the flexibility of our current simulation models we feel it is possible to obtain close approximations to many different biological situations. Much of the graphic displays have already been covered in the preceding sections where the “movement” was not confined to an established home range. Figure 14 gives three examples of simulated movement with the home range defined and the movement directed with weighted probabilities. The classical random walk situation is included to provide a visual basis of comparison. The following is a discussion of the comparison of the (k)parameter of the negative binomial to red fox telemetry data. The complexities of these comparisons increase in an exponential manner with an increase

21 1

ANIMAL MOVEMENT PATTERNS

in the number of variables. For that reason all the following comparisons use the same distance traveled distribution and the same duration of rest and duration of movement distributions which have previously been given for red fox. The pooled estimate of the k parameter, from the negative binomial distribution, for red fox telemetry data is 0.225.

AN “ESlAIlISHED” HOME RANGE WAS USED. O N L Y TE1EMElRY DISlRIIUlKHS WfRE USED.

NO HOME RANGE CONflNEMENl WAS UPD. A UNlFOlM ANGLE DISIRIWlION WAS USED. A CONSlANl DISlANCE WAS USED. F W R HUNDRED FIXES WERE USD.

FOUR HUNMED FIXES WE=

A N “ESlANlSliED’ M E RANGE WAS USED. A CIRCULAR NORMU ANGLE DISfllIUTION W l l H C=5 WAS USED. THREE WNDRED FIXES WE*

USED.

A N ~ESlAILISHED”HOME RANGE WAS USED. ’ A CIRCULAR NORMAL A W L E D I P R I M I O N W l l H C = 1 WAS USED. THREE HUNDRED FIXES WERE USED.

USED.

I

ONE MILE

4

FIG. 14. Fox movement patterns generated with the current simulation model. The upper left movement pattern is the classical random walk.

Table V gives comparisons for various modes of operation of the current simulation model. The column labeled “movement circular normal c values” (column 3) relates to the value of this parameter used in the “angle between successive fixes” distribution for a particular siAulation. The symbol ‘y(z)” used in Table V means this parameter was a variable which changed value according to the current location of the simulated animal in the home range. For example, if at some point in time the “simulated animal” was located in an area with many

212

D. B. SINIFF AND C. R. JESSEN

TABLEV Simulated red f o x movement with the current simulation model using the circular nomnal angk distribution. Column 1 i s the estimate of the disperaion parameter k f o r a Simulation. Column 2 i s equivalent to the T y p e 1 error of a chi-square “goodnessof-fit” test. Column 3 i s termed “movement circular normal c value”. Column 4 is termed “confinement circular n o m l c value”. Columns 3 and 4 represent modes of operation for the simulation model (see text f o r more explanation). 1 0.68 1.66 1.27 0.78 3.33 1.66 2.74 1.822 3.60 1.97 2.83 1.03 1.19 1.23 0.63 0.88 1so9 0.33 0.68 2.52 0.85 0.22 0.26 0.35 0.22 0.30 0.22 0.31 0.19 0.44 0.12 0.12

2

3

4

0.79 0.87 0.99 0.91 0.53 0.87 0-95 0.85 0.81

0.77 0.57 0.43 0.37 0.79 0.94 0.83 0.26 0.62 0.73 0.26 0.92 0.57 0.72 0.92 0.24 0.91 0.88 0.06 0.18 0.01 0.00 0.54

f (2) 5

fixes the value of the c parameter was low (about 1.0) so that simulation could proceed with more or less no preferential direction. If, however, the immediate surrounding area was relatively void of fixes the c parameter would take a higher value (approximately 5.0) and the orientation of the peak of the angular distribution would be toward an area with many fixes. The column labeled “confinement circular

ANIMAL MOVEMENT PATTERNS

213

normal c values’’ (column 4) refers to the method of defining the mode of simulated movement when the home range boundary was encountered. The negative binomial contagion parameters (k)for the simulation data (column 1) were estimated by a computer program which utilized the least squares method after Hartley (1958). The chi-square “fit” (column 2) corresponds to the degree to which the negative binomial distribution approximates the simulated data. The value in the chi-square column is a proportion and is equivalent to the a-error of a chi-square test, e.g. if the chi-square fit is 0.25 for some negative binomial distribution then the probability that the negative binomial is a satisfactory approximation is estimated to be 25%. Table V illustrates that the simulations utilizing a variable-movement and variable-confinement mode approached the red fox telemetry data in terms of the dispersion parameter.

IV. DISCUSSIONA N D F U T U R D EE V E L O P M E N T S Watt (1966) suggests that beginning to think of a biological system in terms of simulation, even if that beginning be modest, is a step towards a more complete understanding of the components involved. This simulation procedure representing animal movement is to be taken in this light. Many questions remain to be answered, and these answers must be placed in their proper perspective in the simulation model. A bright prospect in this regard is that simulation does furnish a structure in which to incorporate new information. With the capabilities of large computer systems, we can build such a simulation procedure into as complex a system as our biological knowledge allows. When considering the general aspects of home range, the bivariate normal model proposed by Calhoun and Casby (1958) no longer appears appropriate for the mammals studied here, since it is clear that there is rarely one center of activity; instead we observe several areas of intensive utilization. Mohr and Stumpf (1966) have pointed out that the typical shape of the home range can hardly be classified as circular. The concepts of the simulation procedures presented here would seem to have application both in formulation of a better underlying theory of home range and in suggesting methods of analysis to better understand how animals utilize the area in which they live. The forms of the various distributions which comprise the simulation model help to present a clearer understanding of how an animal moves about. The sequence of choices give some information on how movement patterns may develop. These simulation methods provide a means whereby factors which influence movements can be studied, and they may provide a beginning base for both inter- and intra-specific comparisons.

214

D. B. SINIFF AND C. R. JESSEN

I n carrying out these studies it became evident that many additional biological questions remain which are concerned with the problem of defining a home range boundary. Each species seems to represent different problems and -the following is intended to provide further insight into these problems. Sargeant (personal communication) suggests that red fox generally traverse a major portion of their home range during every nightly excursion and often return to some rather specific daytime resting location. Thus, for this species, study of the sequence of choice leading to the daytime bedding site is needed. Tester and Siniff (1965) have demonstrated that an adult male raccoon covered its home range in about four days while Turkowski and Mech (1966) showed that a young male raccoon did not use the full extent of its home range until five months had elapsed. It has also been shown (Mech et al., 1966b) that raccoons in the fall usually use a different bedding site each day. Thus, it seems that for this species the home range boundary may be rather indefinite on a day-to-day basis and may take form only after an extended time period. No doubt other species have other characteristics in relation to the boundary of the home range and it is desirable that such biological differences are determined and methods of incorporating them into the simulation model are formulated. This approach is somewhat like the approach suggested by Holling (1965) in which he stresses the need to examine the whole system rather than isolated fragments, but emphasizes the importance of the interaction among fragments. The comparisons in the spatial patterns of the simulated and actual data indicate that the negative binomial is a relatively satisfactory model for movement data. Anscombe (1950) indicated the known ways that can give rise to a negative binomial distribution, and one of these would seem to be applicable to the present situation. He suggests that if colonies or groups of individuals (in this case locations) are distributed randomly over an area, then the number of groups observed in samples of fixed area have a Poisson distribution. The negative binomial arises for the total counts of positions per fixed area if the positions in the groups are distributed independently according to the logarithmic series. This may describe the situation represented here. We do not know if the assumption that the number of individual positions per group follows the logarithmic series is reasonable and this problem r e q u ~ e sdetailed investigation. The mathematical aspects of the relationship between the spatial patterns observed and the distributions utilized in the simulation model have not been explored in this project. In developing the simulation model of animal movement we have encountered failures and some small measure of success. We consider that the results approximate the movement patterns observed via

ANIMAL MOVEMENT PATTERNS

215

telemetry. Many areas of ecological interest can be investigated to some degree, utilizing these simulation procedures. The remainder of this discussion suggests a few of the possible areas where this simulation, may be utilized. The negative binomial distribution is a good approximation of contagion for telemetry data on home range use. For this reason, it offers a method for deriving estimates of home range size. Such a measure could be obtained by summing the expected frequencies (including the estimate of the zero class) and multiplying the sum by square size. However, this is not recommended a t this time, since study is needed on the relationships among square size, relative home range size and the k parameter of the negative binomial. If square size is small, relative to the home range, the expected frequency of the zero class becomes very large and the corresponding computed home range size may not be biologically realistic. It is possible, however, that some predictable relationship exists; but further work is needed to establish this point. Simulation work could be the mode of approach to examine this relationship. As noted in the results portion of this paper the distributions of distance moved per unit time and angle between successive fixes are biased to some extent. The reasons for these biases, discussed in this paper and also in Heezen and Tester (1967), have been shown to include errors in the resolution of triangulation and in reading errors made when abstracting the data. Utilizing the simulation procedure it would be possible to adjust for these biases and arrive at approximations of the actual distributions involved. With simulated telemetry data containing biases representing very closely the known biases, this simulated telemetry data would be compared to the observed telemetry data and a judgement made as to the extent of agreement. This process could be repeated until the simulated known distributions with their biases conform to the observed telemetry data. The form of the actual underlying distributions would, hopefully, be approximated by some probability function, perhaps the ones previously suggested, so that repeated trials as suggested above, would produce closer estimates of the distribution parameters involved. One of the problems that continues to plague wildlife workers is that of census methods. It is perhaps not the need of new census methods that is so important, as it is a better understanding of the underlying biases that occur in the current methods. Edwards and Eberhardt (1967) have recently provided a good evaluation of capture-recapture census methods by comparing estimates of numbers of cottontail rabbits (Sylvilagas floridanas) in a 40-acre pen with the actual numbers present. They suggest that the probability of capture vaned between animals and

216

D. B. SINIFF AND C. R. JESSEN

also for the same animal depending on how many times the individual had been captured. A census method first described by Eberhardt et al. (1963) appears to give the most reasonable census results. This method involves tallying the number of animals that are captured on 1, 2, 3, etc. occasions and then back-calculating to obtain an estimate of the animals not captured. The sum of these frequencies (including the estimate of the zero captures) give an estimate of the population. The number of animals in the zero frequency was calculated by regression analysis and also by fitting the truncated geometric distribution to the observed data and utilized the expected zero frequency as the estimate of the zero class. Edwards and Eberhardt (1967) give some hypotheses as to why such a distribution may fit data of this type. The simulation model proposed here offers an excellent method for the study of some of these problem areas. It would be possible to simulate both an animal population and the traps within an enclosed area and to control the many probabilities involved. For example, the traps could be placed in either random, systematic or clumped fashion and the probability of capture could be varied among animals and from one capture to the next. Utilizing such a method, it would be possible to observe the effects of these probabilities on the various methods of estimation. I n addition, simulation could provide a better understanding of why the geometric distribution happens to be a good census approximation for the frequency of recapture. It is clear that total distance traveled by an individual for some period of time is not necessarily a good measure of inter- and intraspecific differences. The form of the duration of movement, duration of rest, and distance moved per unit time distributions can be different for two sets of data, and yet the total distance traveled may be the same. Sargeant et al. (1967b), in a study on red fox, have utilized these distributions to show differences between summer and winter, adults and juveniles, and healthy and injured animals. The shifts in the form of these distributions indicate how these animals adapt to their changing environment and physical status. These distributions discussed in the preceding paragraph could also be used for biological interpretations of the relationship of an animal with vegetation types or other permanent or seasonal habitat features. It seems likely that movements involving food gathering will appear quite different from other types of activity. Thus, for example, by correlating distribution forms with vegetation type it would be feasible to obtain some notion of vegetation preferences and to observe shifts in the utilization of the home range which may occur throughout the year. Once such distributions become established, i t should be possible to simulate correctly a species use of a given area by reading into the

ANIMAL MOVEMENT PATTERNS

217

computer the habitat of that area. If this can be accomplished, it will increase the validity of all our remarks concerning ecology and simulation. The movements of individuals within any community may be influenced by the presence of other individuals of the same species and by other species. This relationship among individuals obviously affects the pattern of movements and the areas traversed. The amount of contact, in terms of distance between individuals at a given instance in time, can now be measured via telemetry. One of our many unsolved problems concerns the absence of information on the expected frequencies of distance between two animals which share the same area. After assuming that contact is random, the problem still remains unsolved. Once simulation procedures are perfected to the stage where the simulation data cannot be distinguished from telemetry data, then an empirical base line for two (or more) animals may be established for the condition “no interaction”. Repeated analysis of two simulated animal movements on the same home range a t the same time would provide such a base line. The comparison of two sets of telemetry data values, with this base line distribution, would allow a test for interactions between the telemetered animals. Ecology will be greatly advanced if the perfection of simulation will allow evaluation of interactions within species or among species. Interpreting whether avoidance or attraction is taking place requires some “yardstick” for comparison, and it is anticipated that the simulation procedure will eventually furnish this criterion.

ACKNOWLEDGEMENTS We wish to acknowledge the financial support of the U.S. Atomic Energy Commission, Contract At( 11-1) 1332, Document COO-1332-36. A portion of this investigation was supported by PHS Training grant number 5 TO1 GMO-1779 from the National Institutes of Health. Dr John R. Tester contributed many helpful suggestions, and provided guidance throughout this study. We appreciate the aid of the other personnel of the radio-tracking project, especially Mr Alan B. Sargeant, Dr Orrin J. Rongstad, and Mr V. B. Kuechle in terms of both stimulating discussions and in making tracking data available. Dr William H. Marshall and Mr Alvar Peterson cooperated generously in making the facilities of the Cedar Creek Natural History Area available. Dr L. D. Mech provided a portion of the snowshoe hare data which were used herein, and Dr L. L. Eberhardt, Hanford Laboratories, Richland, Washington, contributed many stimulating ideas. Dr Frank

218

D. B. SINIFF AND C. R. J E S S E N

McKinney and Mr G. G. Montgomery offered valuable criticisms of the manuscript. The Numerical Analysis Center of the University of Minnesota graciously provided additional CDC 6600 computer time as it was needed.

REFERENCES Anscombe, F. J. (1950). Biometrika 37, 358-382. Sampling theory of the negative binomial and logarithmic series distributions. Batschelet, E. (1965). Mono. of Am. Inst. of the Biol. Sci., Wash. D.C. Statistical methods for the analysis of problems in animal orientation and certain biological rhythms. Bliss, C. E. and Fisher, R. A. (1953). Biometrics 9, 17C196. Fitting the negative binomial distribution to biological data. Brown, L. E. (1962). I n “Survey of Biological Progress” (B. Glass, ed.), pp. 131-179. Academic Press, New York. Home range in small mammal communities. Burt, W. H. (1943). J . Mammal. 24, 246-352. Territoriality and home range concepts as applied to mammals. Calhoun, J. B. and Casby, J. U. (1958). Public Health Mono. #55. U.S. Dept. of Health, Educ. and Welfare. The calculation of home range and density of small mammals. Cochran, W. W., Warner, D. W. and Tester, J. R. (1964). Tech. Rep. #7. Mus. of Net. Hist., Univ. of Minn. The Cedar Creek automatic radio tracking system. Cochran, W. W., Warner, D. W., Tester, J. R. and Kuechle, V. B. (1965). Bioscience 15, 98-100. Automatic radio-tracking system for monitoring animal movements. Dice, L. R. and Clark, P. J. (1953). Contr. Lab. Vertbr. Biol. 62, 1-15. The statistical concept of home range as applied to the recapture radius of the deermouse (Peromyscus) Eberhardt, L., Peterle, T. J. and Schofield, R. (1963). Wildl. Mono. 10, 1-51. Estimating cottontail abundance from live trapping data. Edwards, W. R. and Eberhardt, L. (1967). J . Wildl.Mgt. 31, 87-96. Estimating cottontail abundance from live trapping data. Ghent, A. W. (1966). Trane. Am. Piah. SOC.95, 437-441. Binomial cornerassociation assessment of contagion: A response to certain criticisms of the method. Gould, E. M. and O’Regan, W. G (1965). Harvard Forest Papers 13, 1-86. Simulation, a step toward better forest planning. Greenwood, J. A. and Durand, D. (1955). Ann. Math. Stat. 26, 233-246. The distribution of a length and components of the s u m of n random unit vectors. Greig-Smith, P. (1965). “Quantitative Plant Ecology”, 2nd edn. Butterworths, Washington D.C. Hartley, H. 0. (1958). Biometrics 14, 174-194. Maximum likelihood estimation from incomplete data. Hayne, D. W. (1949). J . M a m d . 30, 1-18. Calculation of size of home range. Heezen, K. L. and Tester, J. R. (1967). J . Wildv. Mgt. 31, 124-141. Evaluation of radio-tracking by triangulation with special reference to deer movements. Holling, C. S. (196s). Memoirs Ent. SOC., Canada 45, 1-60. The functional response

.

ANIMAL MOVEMENT PATTERNS

219

of predators to prey density and its role in mimicry and population regulation. Jorgensen, C. D. (1968). J. M a m m l . 49, 104-112. Home range as a measure of probability interactions among populations of small mammals. Mech, L. D., Heezen, K. L. and Siniff,D. B. (1966a). Anim. B e h v . 14, 410-413. Onset and cessation of activity in cottontail rabbits and snowshoe hares in relation to sunset and sunrise. Mech, L. D., Tester, J. R. and Warner, D. W. (1966b). J. M a m m l . 47, 540-466. Fall daytime resting habits of raccoons as determined by telemetry. Mohr, C. 0. and Stumpf, W. A. (1966). J . Wildlf. Mgt. 30, 293-304. Comparison of methods for calculating areas of animal activity. Moulton, J. C. (1966). Master’s Thesis, Univ. of Minn. Movement and activity of three white-tailed deer during the winter of 1964-65 in east central Minnesota determined by telemetry. Paulik, G. J. and Greenough, J. W. Jr. (1966). I n “System Analysis in Ecology” (K. E. F. Watt, ed.), pp. 215-252. Management analysis for a salmon resource system. Robinson, R. (1954). Ann. Botany, N . S. 18, 35-45. The distribution of plant populations. Sanderson, G. C. (1966). J. Wildlf. Mgt. 30, 215-235. The study of mammal movements-a review. Sargeant, A. B., Forbes, J. E. and Warner, D. W. (1965). Tech. Rep. #lo, Mus. of Nat. Hist., Univ. of Minn. Accuracy of data obtained through the Cedar Creek automatic radio tracking system. Sargeant, A. B., Warner, D. W. and Siniff, D. B. (1967a). (Unpublished manuscript), Mus. of Nat. Hist., Univ. of Minn. Methods of analysis of radio telemetered data on red fox. Sargeant, A. B., Warner, D. W. and Siniff, D. B. (1967b). (Unpublished paper presented a t the 29th Proc. Midwe& Wildlf Conf., Dec. 1967.) Some regulatory parameters influencing fox actions. Seal, H. L. (1966). Trans. Am. FGh. Soc. 95, 436-437. Testing for contagion in animal populations. Tester, J. R. and Siniff, D. B. (1965). Trans. North Am. Wildlf. Conf. 30,380-392. Aspects of animal movement and home range data obtained by telemetry. Turkowski, F. and Mech, L. D. (1968). Tech. Rep. #13, Mus. of Nat. Hist., Univ. of Minn. An analysis of the movements of a young male raccoon. Wadsworth, G. P. and Bryan, J. G. (1960). “Introduction to Probability and Random Variables.” McGraw-Hill Book Co. Inc., New York. Watt, K. E. F. (1966). Ira “System Analysis in Ecology” (K. E. F. Watt, ed.). pp. 253-278. Academic Press, New York. Ecology in the future.

This Page Intentionally Left Blank

Author Index Numbers in italics refer to the pages on which references are listed in bibliographies at the end of each article. A Albertson, F. W., 146, 147, 179, 183 Allen, K. R., 19, 28, 71 Amren, H., 26, 71 Anderson, C. D., 144, 179 Anderson, R. O., 27, 71 Anscombe, F. J., 214, 218 Arnold, J. F., 158, 179 Arnold, L. W., 158, 179 Assman, A. V., 13, 71 Atkins, W. R. G., 7, 71

Brady, N. C., 156, 179 Braun, E. L., 87, 94, 110,131 Bray, J. R., 86, 97, 101, 102, 103, 131 Breckenridge, W. J., 160, 182 Bronson, F. H., 146, 179 Brown, L. E., 187, 218 Brown, R. T., 85, 96, 126, 131 Bryan, J. G., 203, 219 Buckman, H. O., 156,179 Buechner, H. K., 155, 179 Buell, M. F., 87, 90, 91, 96, 97, 107, 109,131 Burkholder, P. R., 33, 72 Burpee, A. J., 155, 179 Burt, W. J., 186, 218

B Backiel, T., 61, 62, 71 Baker, H. G., 107, 118,131 Baldina, E. P., 22, 23, 24, 74 C Ball, R. C., 28, 38, 71, 74 Cain, S. A., 96, 131 Bartlett, H. H., 147, 179 Calhoun, J. B., 186, 187, 213, 218 Batschelet, E., 200, 201, 203, 218 Cantlon, J. E., 98, 109,131 Baylor, E. R., 59, 72, 79 Carefoot, T. H., 46, 68, 72 Beamish, F. W. H., 47, 48, 72 Carpenter, J. R., 138, 143, 179 Beklemishev, C. W., 54, 72 Casby, J. U., 186, 187, 213, 218 Bell, J. O., 59, 72 Chancy, R. W., 117,131 Berezina, N. A., 46, 72 Chapman, S. W., 28, 72 Beutner, E. L., 144, 154, 183 Billings, W. D., 106, 114, 115, 116, 131 Chapman, G., 59, 72 Child, G., 149, 161, 170, 179 Bird, R. D., 158, 179 Clark, P. J., 186, 218 Birge, E. A., 31, 72 Clarke, G. L., 17, 32, 72 Blink.;, L. R., 13, 72 Clmo, R., 46, 79 J3liss, C. E., 197, 198, 218 Clausen, J., 116, 117, 118, 132 Bond, R. M., 155, 159,179 Clements, F. E., 84, 85, 91, 92, 93, 94, Boriey, A. D., 13, 72 104, 106, 109, 111, 114, 120, 135, IJonner, J., 95, 122, 124, 131, 133 153,183 l k m a n n , F. H., 125, 131 Cochran, W. W., 188, 218 Borner, H., 125, 131 Coe, M. J., 168, 169, 180 I
222

AUTHOR INDEX

Conover, R. J., 41, 54, 72 Cook, C. W., 114, 116, 130,132 Cook, M. T., 123,132 Cooper, L. H. N., 7, 8, 72 Cooper, W. E., 28, 73 Corner, E. D. S., 41, 54, 55, 72, 73 Corwin, N., 8, 75 Costello, D. F., 140, 154, 155, I79 Cowey, C. B., 54, 55, 73 Crisp, D. J., 152, 163, 179 Crow, J. F., 108,132 Cummins, K. W., 66, 73 Curl, H., 37, 73 Curtis, J. T., 85, 86, 87, 96, 97, 99, 101, 102, 103, 105, 112,131,132,133 Cushing, D. H., 6, 54, 64, 73

D Dagnelie, P., 101, 102, 132 Dale, M. B., 97, 99, 101, 102, 133 Darling, F., 172, 179 Darnell, R. M., 66, 73 Dasmann, R. F., 168, 173,179 Daubenmire, R., 100, 102, 132, 147, 148, 149, 150, 179 Davidson, D. W., 87, 90, 91, 96, 97, 107, 131 Davis, D. E., 165, 179 Davis, E. F., 122, 123, 124, 132 Davis, G. E., 47, 62, 73, 80 Davidson, E., 174, 180 De Candolle, A. P., 121, 132 Dice, L. R., 106, 110,132, 186, 218 Dickie, L. M., 47, 48, 50, 61, 67, 68, 72, 76, 77 Dickson, J. G., 99, 123, 133 Digby, P. S. B., 24, 73 Dix, R. L., 87, 109, 132, 148, 180 Dobzhansky, T., 108, 119,132, 134 Doudoroff, P., 62, 80 Dugdale, R. C., 5 , 27, 37, 64, 73, 76 Dunn, L. C., 108,134 Durand, D., 201, 218

E Eberhardt, L., 215, 216, 218 Edmondson, W. T., 25, 73 Edwards, R. R. C., 51, 73 Edwards, R. W., 12, 14, 15, 73, 76 Edwards, W. R., 215, 216, 218 Ehrlich, P. R., 107, 132

Ellison, L., 151, 156, 157, 180 Elton, C. S., 151, 180 Engelmann, M. D., 165,180 Evans, F. C., 156,180

F Felger, R. S., 116, 132 Field, C. R., 166, 180 Fisher, R. A., 197, 198, 218 Fitch, H. C., 159, 180 Fitzpatriok, F. J., 143, 183 Foerster, R. E., 20, 78 Fogg, G. E., 59, 73 Forbes, J. E., 193, 219 Forbes, R. D., 128, 133 Formosov, A. N., 158, 160, 180 Foster, J. B., 168, 169, 180 Fulton, J. D., 25, 37, 61, 77 G Gaarder, T., 4, 73 Garrett, S. D., 123, 124, 132 Gates, D. H., 114, 116, 130, 132 Gerking, S. D., 28, 37, 47, 53, 57, 58, 69, 73 Ghent, A. W., 197, 218 Gilmartin, M., 9, 11, 66, 73 Gittins, R., 103, 132 Gleason, H. A., 84, 91, 95, 96, 99, 105, 106, 107, 110, 118, 121, 132, 133 Gliwicz, Z., 26, 74 Glover, P. E., 161, 162, 171, 180 Goering, J. J., 5, 37, 73 Goldman, C. R., 4, 12, 74 Gotley, F. B., 165, 179 Goodall, D. W., 101, 106, 117, 133 Gould, E. M., 186, 218 Gran, H. H., 4, 73 Grant, C. M., 38, 77 Gray, R., 95, 133 Greenidge, K. N. H., 109,133 Greenough, J. W. Jr., 186, 219 Greenwood, J. A., 202, 218 Greig-Smith, P., 97, 103, 133, 197, 218 Greze, V. N., 22, 23, 24, 29, 30, 74 Grinnell, J., 156, 180 Grzimek, B., 168, 180 Gwynne, M. D., 162, 172,180

H Haines, B. L., 126, 134 Hall, D. J., 26, 74

AUTHOR INDEX

Hanson, H. C., 141, 143, 180 Harrington, G. M., 177, 180 Harris, E., 55, 74 Hartley, H. O., 198, 213, 218 Harvey, H. W., 32, 53, 74 Haler, A. D., 26, 79 Hauge, R., 122, 134 Hayes, F. R., 37, 38, 72, 74 Hayne, D. W., 28, 74, 186, 218 Heady, H. F., 145, 150, 175, 176, 180, 181 Heezen, K. L., 189, 193, 215, 218, 219 Heinle, D. R., 27, 74 Hellebust, J. A., 59, 74 Hepher, B., 12, 74 Herskowitz, I. H., 108, 133 Hesse, P. R., 161, 162, 180 Hiesey, W. M., 116, 117, 118, 132 Hillbricht-Ilkowska, A., 26, 74 Hodd, D. W., 14, 77 Holling, C. S., 214, 218 Holm, R. W., 107,132 Holway, J. G., 112, 134 Hong Shik Min, 55, 77 Hooper, F. F., 27, 38, 71 Horn, E. E., 159, 180 Horton, P. A., 28, 74 Hoskin, C. M., 14, 61, 74, 76 Hough, A. F., 128,133 Hult, R., 92, 133 Humphrey, R. T., 148, 155,180 Hutchinson, G. E., 37, 74, 113, 133

I Ivlev, V. S., 4, 16, 17, 39, 42, 45, 50, 57, 61, 74, 75, 76

J Jackson, D. F., 12, 75 Jaeger, E. C., 114, 133 Jodrey, L. H., 37, 72 Johannes, R. E., 56, 59, 75, 80 Johnson, J., 99, 123, 133 Jones, L. R., 99, 123,133 Jorgensen, C. B., 59, 75 Jorgensen, C. D., 187, 219 Juday, C., 17, 26, 30, 31, 59, 72, 75 K Kalmbach, E. R., 155,180 Kmwischer, J., 9, 10, 33, 80

223

Karzinkin, G. S., 57, 76 Keck, D. D., 116, 117, 118, 132 Kennedy, H. D., 13, 75 Ketchum, B. H., 8, 75, 78 Kettlitz, W. L., 173, 182 Klekowski, R. Z., 41, 43, 75 Koford, C. B., 155, 156, 157, 158, 160, 161,180 Korstian, C. F., 125, 133 Kowalczewski, A., 36, 76 Krogh, A., 41, 50, 75 Kuechle, V. B., 188, 218 Kuenzler, E. J., 33, 46, 55, 56, 69, 75 Kuznetsov, S. T., 59, 75

L Lambert, J. M., 97, 99, 101, 102, 103, 133,135 Lamprey, H. P., 167, 168, 180 Langford, A. N., 87,90,91,96,97,107, 131 Lasker, R., 54, 75 Laws, R. M., 166,181 LeBrasseur, R. J., 6, 25, 37, 61, 77 Le Cren, E. D., 61, 62, 71 Ledger, H. P., 165, 172, 173, 181, 182 Lindeman, R. L., 1, 31, 65, 69, 75 Lipin, A. N., 57, 76 Lister, P. B., 158, 182 Lowe, C. H., 116,132 Lyman, C. P., 174, 182 M McFadden, J., 12, 75 Macfadyen, A., 1, 17, 75, 164, 181 McIntire, C. D., 62, 75 McIntosh, R. P., 85,86,95,96,99,101, 132,133 Maciolek, J. A., 13, 75 McLaren, I. A., 42, 75 McMahon, C. A., 176, 181 McMillan, C., 116, 118, 133 Magnitzky, A. W., 59, 72 Maloiy, G. M. O., 176, 181 Malovitskaya, L. M., 60, 61, 68, 81 Mann, K. H., 1, 2, 20, 28, 34, 47, 50, 51, 53, 67, 71, 75 Margalef, D. R., 92, 133 Margalef, R., 4, 76 Marshall, S. M., 54, 55, 73, 76 Marshall, W. H., 149, 182

224

AUTHOR INDEX

Martin, H., 122, 133 Martin, N. V., 61, 76 Massey, A. B., 124, 125, 133 Mathews, C. P., 36, 76 Mathews, H . M., 55, 77 Maycock, P. F., 105, 133 Mech, L. D., 189, 193, 214, 219 Meien, V . A., 57, 76 Menzel, D. W . , 59, 76, 79 Mikola, P., 113, 133 Miller, R. S., 157, 181 Miller, R. W., 155, 133 Misonne, X . , 170, 181 Mitchell, J . E., 115, 133 Mohr, C. O., 213, 219 Moss, E . H., 158, 181 Moulton, J . C., 193, 196, 219 Muller, C. H., 109, 115, 122, 226, 127, 130, 134 Muller, W. H., 122, 126, 134 Murray, J . M., 155, 161, 162, 181 N Naveh, Z., 175, 181 Ness, J., 27, 76 Neess, J . C., 26, 79 Negus, C. L., 27, 34, 76 Nichols, G. E., 85, 105, 107, 134 Nicholson, H . F., 6, 7 3

0 Odum, E. P., 14, 33, 36, 53, 76, 111, 134 Oduni, H . T., 1, 14, 17, 32, 61, 76, 77 Ohmann, L. F., 87, 90. 91, 96, 97, 107, 131 Oosting, H. J., 125, 134 Ophel, I . L., 39, 76 O’Regan, W . G., 186, 218 Om, A. P., 54, 76 Osborn, B., 159, 181 Overland, L., 126, 134 Ovington, J . D., 166, 181 Owens, M., 12, 14, 15, 73, 76

P Paloheimo, J. E., 47, 50, 61, 67, 68, 76, 77 Park, K., 14, 77 Parsons, T . R., 6, 7, 24, 37, 61, 77, 78 Paulik, G. J., 186, 219

Pavlova, E. V., 41, 77 Payne, W . J . A., 165, 172, 182 Pease, A. K., 61, 77 Pechen, G. A., 24, 77 Penfound, W . T., 12, 77 Peterle, T . J., 216, 218 Peterson, R. A., 154, 181 Petipa, T . S., 42, 77 Petrides, G. A., 168, 169, 181 Petrusewicz, K., 71, 77 Philips, J., 92, 134 Phillips, J . E., 38, 74 Phillips, P., 155, 181 Phinney, H . K., 62, 75 Pickford, G. D., 154, 171, 181 Pieczynska, E., 13, 77 Pomeroy, L. R., 14, 33, 38, 55, 77 Ponyatovskaya, V . M., 101,134 Putter, A., 59, 77 R Ramsay, C. W., 176, 181 Rattray, J . M., 144, 181 Ray, S. M., 59, 72 Raymont, J . E . G., 4, 21, 54, 78 Redfield, A. C., 8, 32, 78 Reynolds, H . G., 156, 157, 158, 181 Rice, E . L., 1 2 7 , 1 3 4 Richards, P. W., 118, 119, 134 Richards, S. W., 27, 78 Richman, S., 40, 41, 42, 43, 78 Ricker, W . E., 3, 20, 39, 40, 78 Riegel, A., 146, 179 Rigler, F . H., 37, 54, 55, 78 Riley, G. A., 8, 27, 32, 53, 62, 63, 64, 78 Riney, Th., 147, 173, 181, 182 Robinson, R., 197, 219 Roe, F . G., 110, 134 Roff, P. A., 66, 73 Ross, B. A., 160, 182 Roth, H . H., 168, 169, 173, 182 Rowe, J . S., 110, 113, 120, 121, 134 Ruttner, F., 13, 78 Ryder, R. A., 61, 78 Ryther, J . H., 4, 5, 9, 78

S Sachs, R., 172, 173, 181 Salamun, P. J., 86, 135 Sanders, H . L., 26, 78

AUTHOR INDEX

Sanderson, G. C., 187, 210 Sanford, G. B., 123, 134 Sargeant,A. B., 189,192,193,196,216, 219 Sauer, C. O., 147, 182 Savory, C. R., 165, 173,182 Schofield, R., 216, 218 Scott, J. T., 112, 134 Seal, H. L., 197, 219 Shantz, H. L., 142,182 Sheina, M. P., 57, 76 Sheldon, R. W., 6, 7, 78 Shul’man, G. E., 57, 78 Shushkina, E. A., 24,41,43, 75, 77 Silliman, R. P., 69, 78 Siniff, D. B., 187, 189, 192, 193, 196 197, 214, 216, 219 Sinnott, E. W., 108, 134 Skinner, J. D., 172, 174, 182 Sladeckova, A, 13, 79 Slobodkin, L. B., 1, 31, 39, 43, 45, 69, 79 Smalley, A. E., 13, 33, 76, 79 Smith, C. C., 154, 155, 182 Smith, E. E., 38, 77 Smith, F. E., 65, 79 Smith, H. P., 8, 78 Smith, N. S., 172, 173, 181 Sorokin, J. I., 54, 79 Spodniewska, I., 26, 74 Stanczykowska, A., 27, 79 Steele, J. H., 8, 29, 79 Steemann Nielsen, E., 4, 5 , 79 Stephens, G. C., 59, 79 Stephens, H., 6, 25, 61, 77 Stewart, D. R. M., 166, 182 Stoddart, L. A., 114, 116, 130, 132, 175,182 Straskraba, M., 13, 79 Strickland, J. D. H., 4, 5 , 8, 79 Stross, R. O., 26, 79 Stumpf, W. A., 213, 219 Sushchenya, L. M., 41, 46, 47, 79 Sutcliffe, W. H. Jr., 59, 60, 72, 79 Swank, W. G., 169, 181 Szczepanska, W., 13, 77 T Talbot, L. M., 143, 144, 152, 164, 165, 166, 168, 169, 172, 179, 182 Talbot, M. H., 165, 166, 168, 182

225

Talling, J. F., 12, 80 Tansley, A. G., 93, 94, 104, 106, 110, 111, 121,134 Taylor, A. G., 59, 72 Taylor, C. R., 174, 182 Taylor, W. P., 156, 157, 158, 159, 182 Teal, J. M., 1, 9, 10, 17, 33, 35, 59, 80 Tester, J. R., 149, 160, 182, 187, 188, 189, 193, 197, 214, 215,218, 219 Tiemeier, 0. W., 146, 179 Tomanek, G. W., 146,179 TragArdh, I., 121, 134 Trama, F. B., 46, 80 Trump, E. C., 161, 162,180 Turkowski, F., 189, 214, 219 V Verschuren, J., 168, 170, 179, 181 Vesey-Fitzgerald, L. D. E. F., 142, 144, 152, 174,182 Vorhies, C. T., 157, 158, 159, 182 Vucetic, T., 54, 73 W Wadsworth, G. P., 203, 219 Wales, J. H., 62, 80 Walker, J. C., 123, 134 Warner, D. W., 188, 189, 192, 193, 106, 214, 216, 218, 219 Warren, C. E., 47, 62, 73, 80 Wateridge, L. E. D., 161, 162, 180 Waters, T. F., 27, 80 Watt, A. S., 120, 121, 134 Watt, K. E. F., 186, 213, 219 Weaver, J. E., 84,92, 93, 104, 106, 109, 114, 120,135, 143, 147, 153,183 Webb, K. L., 59, 80 Weir, J. S., 153, 183 Wont, F. W., 95, 135 West, N. E., 97, 99, 115, 133, 135 West, O., 147, 148, 183 Westlake, D. F., 12, 13, 80 Wetzel, R. G., 13, 80 Whireway, S. G., 37, 72 Whitfield, C. J., 144, 154, 183 Whitford, P. B., 86, 135 Whittaker, R. H., 85, 93, 95, 98, 100, 106, 111, 135 Wiegert, R. G., 71, 80 Wieser, W., 33, 80

226

AUTHOR INDEX

Williams, W. P., 34, 80 Williams, W. T., 102, 103, 135 Winberg, G. G., 14, 22, 46, 49, 67, SO, 81 Wolf, F. A., 123, 135 Wolf, F. T . , 123, 135 Wood, J. F., 59, 81

Y Yablonskaya, E. A., 21, 81 Yentsch, C. S., 5, 9, 78

2 Zaika, V. E., 60, 61, 68, 81 Zaphiro, D. R. P., 166, 182

Subject Index A

America, South-West, 154 Ampelieca, 27 Aard-varks, 162 Amphipods, 13, 28, 47, 66, 57 Abies balsameu, 120 Analysis (Plant Association), 101Acacia - Commiphora - busJ~- savanna, 103 168 Andropogon, 143, 146 Anglesey, 103 Acacia-Themeda grassland, 167 Acurtia ckzusi, 22-24, 60, 61 Animal movement patterns, 185-219 Acer rubrum, 90 Animal production, 16, 137, 183 Acer sacchurum, 86, 87, 91, 106, 109, Ankole bullocks, 177 120, 128 Annelids, 34 Achillea, 116-1 1 7 Anodonta, 27, 36 Acorns, 36 Antelopes, 139, 144, 172, 173, 176, Adenostoma fasciculatum, 127 176 Aepyceros melampus, 173 Antidorcaa mrsupialis, 161 Aeshna grandis, 46 Antilocapru americana, 144 Africa, 138, 146, 147, 149, 155, 160, Ants, 151, 162, 163 161, 169, 171-173, 175-178 Aphids, 65 Central, 141, 144, 145, 146, 160, Aplysia pumctuta, 46, 68 170 Aquatic ecosystems, 1-81 East, 141, 144, 146, 152, 160, 165, Arctic, 102, 119 168-170, 172, 176 Arctostuphylos uva-ursi, 121 South, 141, 154, 160 Aristida, 145 African elephant, 165, 169 Aristida oliguntha, 127 African mole rats, 161 Aristida papposa, 145 Agropyron, 143 Arizona, 157, 158 Albert National Park, 168 Artemia, 44, 59 Alberta, 120, 121 Artemia salina, 41 Alburnua alburnus, 34, 50 Artemisia tridentuta, 114, 115 Alcekzphus, 173 Arvicanthis abyssinicus, 170 Algae, 4, 5, 13, 14, 17, 32-36, 46, 69, Aspen, 158 64, 68 Assimilation, 3, 54, 69 planktonic production, 4-12 Association, plant, 83-136, 150 Algonquin Park, 61 Mixed-Grass Prairie-Plains, 143 Allen Curve, 19, 21, 27 Short-Grass-Plains, 143 Allelopathy (Plant association), 122Tall-Grass Prairie, 143 Atheriz, 38 129 Amelanchier, 90 Athi-Kapiti Plains, 167 America, North, 84, 93, 94, 104, 105, Atomic Energy Commission, U.S.A., 109, 110, 116, 130, 138, 141, 217 143, 155, 160, 162, 169, 170, 176, Atriplez confertijolia, 114, 116 178 Australia, 141 I

227

228

SUBJECT INDEX

Auto-intoxication (Plant association), 122-128 Autotrophic organisms, 3 Azov Sea, 29, 30, 60

B Baboon, 169 Bacteria, 16, 17, 34, 35, 37, 39, 55, 57, 59, 62, 123 Badgers, 144, 158, 161, 162 Baffin Island, 102 Balsam poplar, 120 Barley, 126 Barnes Ice Cap, 102 Basalt, 90 Bat-eared fox, 162 Bean, 127 Benthic epifauna, 27 fauna, 17, 31, 46, 67 plants, 12, 31, 36 production, 12-16 Benthos, 8, 17, 31, 34, 36, 37, 40, 45-47, 55-57 measurement of, 26-28 Bessell function, 201 Betula lenta, 90 Betula lutea, 90, 109 Bioenergenetics, 47 Biomass, 3, 12, 16, 17, 20, 21, 26-28, 60, 66, 67, 163-171 definition of, 141 Birds, 149 Bison, 144, 168 Bison bison, 144 Black Sea, 22, 24, 41, 61 Black Walnut, 123, 124 Bleak, 34, 36, 50, 53 Blekinge, Sweden, 92 Bluegills, 28, 58 Bluegill sunfish, 53, 57 Botswana, 170 Bouteloua, 143 Bouteloua gracilis, 106 Brachiaria, 145 Brachycentrus, 38 Britain, 94, 106 British Columbia, 7, 9, 11

Bromus mollis, 127, 159 Brook trout, 48 Brown trout, 28 Brunswick formation, 90 Bryazoa, 13, 36 Buchloe, 143 Buffalo, 166, 172, 173 Bushbuck, 169 Byram gneiss, 90

C Cactus, 116 Calanipeda aquae-dulcis, 60, 61 Calanus finmarchicus, 54, 55 Calanus heligolandicus, 42 Calanus plunachrus, 24 California, 13, 108, 122, 159 Calluna, 120 Canada, 7, 102, 110, 113, 115, 120, 158 Canis lupus, 144 Canis mesomelas, 162 Cape Breton Island, 109 Carbon, 4-6, 10, 17 Carp, 49 Carnivores, 2, 32, 34, 37, 44, 46, 59, 62, 66 Carolina, North, 125 Carpinus caroliniana, 87 Carrying capacity (grasslands), 141, 163, 171, 175 Carya cordiformis, 90 Carya ovalis-glabra, 90 Camja tomentosa, 90 Castanea dentata, 90 Caterpillars, 121 Cedar Creek Natural History Area, 217 Cedar Creek system, 188, 189, 193 Cenchrus, 145 Centropages crayeri, 60 C e m s canadensis, 175 Cheetah, 169 Chironomus plumosus, 27 Chlamydomonas, 41-43, 61 Chloris rnyriostachya, 145 Chlorophyll, 5, 6, 8, 10 Chrysopogon, 145 Chrysopogon, 145 Cirsiurn, 122

229

SUBJEUT INDEX

Citellua beecheyi, 159 Citellua p y g m u a planicola, 160 Citellua richurahoni, 158 Cladocera, 41, 61 Classification (Plant association), 84, 101, 103

Clementsian system (Plant association), 85, 93-96, 98, 104, 112, 115, 118, 128

Climatic factors (Plant association), 114-115

Climax association (Plant), 85, 87, 91, 94, 107, 109, 111, 118, 128

theory (Plant), 92-95, 104-105, 118 Coastal Plain, 87 Co~ophospernum-Combretum,168 Competition, 138, 143, 175 Conservation (grasslands), 138 Continuum concept (Plant association), 85-91, 96-101, 105, 107, 111-112, 128 Copepods, 21, 25, 42, 54

Coral reef community, production of, 14

Corn, 107 C m u s canadensis, 126 Cornuaflorida, 87, 90 Cotton rats, 155, 159 Cottontails, 159, 193, 215 COttUS, 38 Coulter particle counter, 6, 7 Cow, 151, 172 Crabs, 34, 35 Crickets, 151 Critical levels (Plant association), 112122

Crocuta crocuta, 162 Crustacea, 17 Cryptopleura, 46 Cucumis sativw, 127 CYClOpS, 50 Cymbopogon, 145, 177 Cynomya, 144, 157 Cyprinidae, 28

Dartmouth, 70 Decomposers, 2, 3, 12, 14, 16, 18, 20 Decomposition, 31, 58 processes, 58-60 Deer, 175, 176, 193 Deer-Mice, 155, 186 Degradation, effects of, 170-171, 179 Demersal fisheries, 29 Departure Bay, British Columbia, 7 Detritus, 6, 7, 34, 36, 38, 39 feeders, 2 Dextrose, 7 Diaptomua salinus, 21 Diatoms, 32, 55, 57 Digitaria, 145 Dik-dik, 165, 167 a p o d o m y s merrhrni Mearns, 156, 157

Dispersion parameter (Animal movements), 207, 213 Distribution angle, 202-203, 205, 212 mathematical, 200-203, 215 size-frequency, 28 Divisiveness, universality of (Plant association), 117-118 Dominants, influence of, 105-107 Drekqserul polymorpha, 27 Drosophila peraimilia, 108 Drosophib pseudoobscura, 108 Drosophilae, 112 Drought cycles (grasslands), 146-147, 171

Duke Forest, North Carolina, 125 Dynamics aquatic ecosystems, 1-81 vegetation, 84

E Echinoids, 13 Ecological adaptation, 142 Ecological efficiency, 44, 45, 53, 69, 141

D Dactyloctenium, 145 Damaliscua korrigum, 140 Daphnia, 26, 40-43, 46, 61, 69 I*

Ecological niches, 138, 165 Ecological responses, 142 Ecological structure, 138 Ecosystems aquatic, 1-81 energetics of, 30

230

SUBJECT INDEX

Ecosystems-continued trophic-dynamic model of, 1 trophic structure, 2 whole, study of, 3&39 Ecotones (Plant association), 111, 118 Ecotypes (Plant association), 115-117, 129

Edaphic factors, 114-115 Eelgrass, 32 Egestion, 4, 55 Elaeagnus, 158 Eland, 172, 173, 174 Elephant grass, 145 Elephants, 65, 139, 152, 165, 166, 167, 169, 173

Eleusine jaegeri, 145 Elk, 175 Energetics, 39-53 Energy, 4, 30, 47, 48, 50, 54, 62, 177, 178

balance, 33, 46, 48, 67 budget, 30, 31, 39, 42, 43, 46, 53 flow, 1, 3, 32, 35-39, 53, 66, 70, 163, 175 of metabolism, 3, 163, 169 primary accumulation of, 30

production (herbivorous mammals), 138, 163-171

of respiration, 2-3 of sun, 2, 59 transfer, 3 England, 28, 34, 110 English Channel, 7-9, 24, 32 Ennmpogon cenchroides, 145 Entosphenus cornuta, 38 Entosphenus needhami, 38 Environmental gradients, critical levels (Plant association), 112-122, 129 Ephemeroptera, 46 Ericads, 121, 126 Erigeron, 122 Erodium botrys, 159 Erodium cicutarium, 127 Erosion, 91, 104, 139, 144, 148,

Europe, 121 Eurotia lanatu, 115 Excretion, 3 , 5, 39, 40, 55

F Factor analysis (Plant association), 101 Fagus grandifolia, 56, 87, 90, 109 Fagus aylvatica, 106 lrestuca megalura, 127 Filter feeders, 38, 39, 59 Fire, on grasslands, 139-142, 144, 147-150, 151-153, 164, 174

Fish, 16, 17, 19, 20, 31, 32, 34, 36, 37, 39, 40, 46, 47-53, 57-58, 67

measurement of, 28-30 Fladen Ground, 9 Florida, 17, 32 Flow chart (simulation model), 209-210 Food biomass, 53 capture, 3 chains, 2, 36, 45, 61, 69 intake, 53-58 web, 140 Forests beech-maple, 87, 104, 118 boreal, 120, 121, 130 conifer-hardwood, 85-86, 105, 121 deciduous, 94, 104, 105, 110 hemlock-northern hardwood, 87, 95, 128

maple-basswood, 86, 112 oak-chestnut, 87, 104 prairie, 99, 114 spruce-fir, 112, 120 steppe, 100 tropical rain, 118-120, 129 upland, 86, 87, 96, 99 FOX, 188-190, 192, 193, 195-198, 207, 21&214, 216

Fraxinus americana, 90 Fungi, 59, 113, 114, 123

163-156, 160

cycles, 147 Estuaries, production of, 14 EuphauSia, 54 Euphrbia, 122 Euphotic zone, 11, 42 Eurasia, 160

G Game ranching (grasslands), 171-174 Gammrua, 38,48 Gastropods, 13 Gazelles, 172

231

SUBJECT INDBX

Gemsbok, 173 George’s Bank, 32, 63, 64 Georgia, 33, 35, 46, 55 a r a f f a camelopardalk, 167 Giraffes, 139, 153, 167 Goats, 173 Goldfish, 49 Gophers, 155-160 Grasshoppers, 33, 149, 151, 155 Grasslands animal influences on, 150-163 conservation, 138 descriptions of, 141-146 management, 138, 174-177 production of wild herbivorous mammals, 137-183 Grazing (grasslands), 15CL.153, 174, 177 effects of overgrazing, 153-155, 178 Great Basin Desert, U.S.A., 114, 130 Great Lakes, 105 Ground squirrels, 155, 158-160, 162, 170

Growth, 3, 27, 28, 39, 47, 48, 52, 53, 57, 61, 67

curves, 27, 165 form (grasslands), 138 rates, 28, 64, 67, 172, 174 Gulf of Maine, 8 Guyana, 119

Hordeum vulgare, 126 Hudson Bay, 120 Husan, 63 Hyalella azteca, 28 Hydra, 44, 69 Hydropsyche, 38 Hyena, 162 HyparrhniCt, 144-146 Hyrax, 154 Hyatrix, 162

I Ichneumons, 121 Impala, 167, 171, 173 Incubation, 4, 5, 13 techniques, 6, 9, 11 Indian Arm, British Columbia, 9 Indiana, 28 Individualistic concept, 95-101, 102 Ingestion, 3, 69 Insects, 35, 36, 163 Integration (Plant association), 107 International Biological Programme, 71

Invertebrates, 4, 17, 36, 39, 138 Iowa. 146

H

J

Hanford Laboratories, Richland, Washington, 217 Hares, 160, 161, 170, 185, 189-198, 207, 217

Hartebeest, 167, 173 Harvest Mice, 159, 186 Herbivores, 2, 3, 13, 31, 32, 37, 59, 61,

Jackal, 162 Jack pine, 126 Jack rabbits, 144, 146, 155, 157, 158, 159, 170

Juglans nigra, 122

63

mammals on grasslands, 137-183 Herring, 29 Heterotrophic organisms, 4, 66 Hexagenia, 36 Hippopotamus, 155, 166, 173 Hippopotamus amphibius, 165 Homeostasis, 106, 107-111 Home range concept (animal movement), 186, 187, 189, 197-199, 200, 205, 2 13-2 15

207,

208,

210,

211,

K Kalmouk steppe, 160 Kangaroo rats, 156-160 Kansas, 146 Keewatin District, Northwest Territories of Canada, 113 Kenya, 145, 166, 167 Kit Fox, 162 Kittatinny limestone, 90 Krogh’s curve, 23, 24, 41, 50, 61

232

SUBJECT INDEX

L Lagomorphs, 138-140, 150, 155, 170, 178

role of (grasslands), 155-160 Lake Beloie, 27 Lake Mendota, 17, 30, 31, 59 Lakes, 12, 27 LaGx, 120 Leaf hopper, 33 Lechwe, 162 Lembos intemedius, 56 Lepidoptera, 121 L e p w , 144 L e p s m r i c a n a , 185 L e p w calqornicus, 157 Lepus capensis crawshayi, 160 L e p w capensis capensis, 160 Lesttes, spowa, 46 Life cycles, 17, 27, 30, 47 Life history, 91, 92 Light, 5, 6 influence of, 138 intensity, 5 Limnology, 12 Lion, 169 Liriodendron tulipifera, 90 Littoral zone, 12, 13 Long Island Sound, 8, 55 Lophocereus schottii, 116 Loudetia kagerensis, 145 Loxodonta afGcana, 165 Lupinus bicolor, 159

M Macrocyc~opsalbidus, 41, 43, 44 Macrophytes, 12-14, 34, 36, 38, 39, 69 Madoqua kirkij, 165 Maine, Gulf of, 8 Makarikari, Botswana, 170 Malaria, 108 Mammals, 185, 186, 213 herbivorous, production of, 137-183 Management (grasslands), 138,17 1-177 Marine bays, production of, 14 Marine ecology, 5, 12 Marine Ecology Laboratory, Dartmouth, 70 Marmot, 155

Marshes, salt, 2, 33-35, 55 Masailand, 176 Matapos, Rhodesia, 149 Materials, turnover of, 53-58 Mayfly, 27 Mbuga grassland, 145 Meadow mice, 159, 186 Meal-worms, 57 Meiosis, 84 Melinis, 145 Menippe mrcenaria, 46 Merriam Kangaroo Rat, 156-158 Mesquite, 158 Metabolism, 3, 14, 30, 31, 33, 42, 46, 48-50, 54, 61, 67

Metamorphosis, 17 Mexico, 115 Mice, 149, 155, 158-160, 186 Michigan, 95 Microtus, 186 Microplankton, 6 Migration, 199 Milwaukee, Wisconsin, 86 Minnesota, 109, 149, 166, 188, 218 Minnows, 48 Mississippi kite, 103 Missouri University, 109 Models simulation (animal movement patterns), 185-219 theoretical, 62-65, 69, 70 trophic dynamic, 1, 31, 65 Modiolus dernism, 46, 65, 56, 58, 69 Moheve Desert, 110 Molluscs 27, 34, 36 Mongoose, 162 Moraballi Creek, Guyana, 119 Mortality, 16, 26-28, 52, 55, 63, 64 Muko Range Experiment Station, Uganda, 177 Mulga-Spinafex desert, 141 Munges mungo, 162 Mussels, 27, 34, 36, 46, 55, 56, 69 Myconhim, 113-1 14

N Nairobi National Park, 168, 169 Nanoplankton, 6 National Institutes of Health, U.S.A., 217

SUBJECT INDEX

National Park Service, 87 Natural Environment Research Council, 70 Nematodes, 13, 34 Neogobius melanostomus, 29, 30 Neotom albigula, 159 Nevada, 114 New England coast, 63 New Jersey, 87, 90, 96, 97, 107, 128 New York State, 112 New Zealand, 28 Ngorongoro Crater, 170 Nigronia, 38 North America, 84, 93, 94, 104, 105, 109, 110, 116, 130, 138, 141, 143, 165, 160, 162, 169, 170, 175, 178 North Sea, 9, 29, 32, 64 Nova Scotia, 109 Numerical Analysis Center, University of Minnesota, 218 Nun moth, 121 Nuphar, 36 Nutrients, 2-4, 7, 8, 65, 66 circulation, 37-39, 66 Nutrition, 54 Nyssa sylvatica, 90

0 Oceanography, chemical, 8 Octocyon megalotis, 162 Odocoileue virginknus, 193 Oklahoma, 12, 127, 155, 159 Oligochaetes, 17, 45 Olive baboon, 169 Omnivores, 38, 39 Onotragus leche mithemni, 162 Ontario, 102 Orcheatia bottae, 47 Ordination (Plant association), 95-103, 112 Oregon Cascades, 99 Organismic Concept, 92-93, 95 Oribis, 171 Orthoptera, 149 Orycteropus afer, 162 Oryx gazella, 173 Oatrya virginiana, 90 Ottawa, 102 Oxygen, 4, 5, 7, 8, 10, 11, 13, 14, 32, 46, 47, 66

233 P

Pampas, 141 Panicum, 143, 145, 146 Papio anubis, 169 Paramecium, 4 1, 44 Peach, 122 Pearson Type 3 probability function, 186 Pedetes capensis, 160 Pelagic organisms, 8 Penndeetum purpreum, 145 Pennisetum schimperi, 145 Pennsylvania, 128 Perch, 39 Periphyton organisms, 13, 14, 38, 39, 61 Perognathus penicilatus pricei, 158 Permyscus mankulatus, 165 Permyscus mniculatus bairdii, 186 Phacochaerus aethiopicue, 162 Phosphate concentration, 6-8 Phosphorus, 6, 8, 37-39, 56-57, 69, 69 Photic zone, 6, 9 Photosynthesis, 3-5,7,9,10, 14-16,32, 33, 35, 69, 63, 153 Phragmites cmmunis, 12 Phytoplankton, 6, 13, 31, 32, 36-38, 63 Picea g l a m , 120 Piedmont Plain, 87 Pigs, 173 Pimpla, 121 Pine Grosbeak, 158 Pinicola enucleator, 158 Pinus banksiana, 113, 126 Pinus resinosa, 126 Pinus strobus, 90, 113 Pinus sylveatris, 1I4 Plankton, 17, 37, 40-45, 61, 62, 67 Planktonic algae, 4, 13 Plant association, 83-135 Pleuronectes platessa, 51 Plocamium, 46 Plymouth, 24 Poa, 143 Pocket gophers, 165-160 Pocket mice, 160 Pogonomymex, 163 Poikilotherms, 49 Poisson distribution, 214

234

SUBJECT INDEX

Polychaetes, 27 Pond &h culture, 16 Population density, 17, 25, 67, 177 dynamics, 33 structure, 163 Populus, 93 Populus bulsamfera, 120 Populus grandidentata, 90 Porcupine, 162 Potato, 123 Prairie Dogs, 144, 155-162 Prairies, 142, 143, 146, 168 Predators, 3, 16, 18, 20, 26, 31, 38, 44, 138, 163, 169 Primary analysis, 102 Principal component analysis, 101 Procavia cupensis, 154 Procyon lotor, 185 Producers, primary, 2, 3, 6, 14, 31 Production, 3, 53-58 annual, 12, 13 definition of, 140 effect of fire, 149-150 fish, 49 gross, 5, 8, 9, 11 net, 5, 8-10, 12 plant, 4 primary, 3, P 1 6 , 59, 66, 175 rate, 5, 13, 60 secondary, 4, 16-30, 66, 68 understanding and measurement of, 4-30 wild herbivorous mammals on grasslands, 137-183 Pronghorn antelope, 144, 175 Prosopis jul$ora, 158 Protozoa, 13 Prunus avium, 90 Prunus serotina, 90 Pteridium aquilinum, 126 Pteronarcys, 38

Q Quebec, 95 Queen Elizabeth National Uganda, 155, 166 Quercus, 87, 90, 91, 109, 128 Quercus alba, 87, 90

Park,

Quercus coccinea, 90 Quercus macrocarpa, 86 Quercus prinus, 90 Quercus rubra, 90 Quercus velutina, 90

It Raccoon, 185, 193, 214 Radio-activity, 5, 13, 39, 55 Radio-isotopes, 37, 39, 51, 54, 69 Range condition (grasslands), 141 Range management, 174-177 Reading, 34 Red fox, 185, 188-190, 192, 193, 195-198, 205, 207, 210-214, 216 Redunca fulvorofual chanleu, 169 Redunca redunca, 169 Reedbuck, 169 Reeds, 84 Reedswamps, 12 Regeneration, 6 Reithrodontomys dontomys, 186 Reithrodontomys humulis, 159 Reproduction, 3, 16, 17, 25, 39, 55, 172, 174 Respiration, 4, 5, 7, 16, 31, 34, 35, 39, 48, 50, 53-58, 61, 63, 64 algal, 8 community, 9, 14, 15, 32 primary producers, 3 rate, 5, 11, 40, 50, 51-53 Rhinoceros, 153, 167 Rhizobium, 127 Rhodesia, 149, 153, 168, 169, 172, 173 Rice, 127 Richland, Washington, 217 River Ivel, 15 River Thames, 5, 6, 28, 34, 36, 50, 51, 53, 59, 70 Rivers, 12, 14 Roach, 34, 53 Rodents, 138-140, 149, 150, 155, 170, 178, 185 role of (grasslands), 155-160 Rotifers, 17 Round goby, 29 Rushes, 84 Russia, 141 Rutilus rutilus, 34

235

SUBJECT INDEX

S Sagebrush, 114, 116, 143, 154, 157 Sagitta, 63 Sagittaria, 32 Salix, 36 Salmo, 38 Salt marshes, 2, 33-35, 55 Salvelinua fontinalis, 48 Salvia leucophylla, 126, 127 San Joaquin Experimental Range, 159 Sand Pocket Mice, 158 Sapelo Island, 33 sassafras albidum, 90 Savannas, descriptions of, 141-146 Sea of Azov, 29-30, 60 Seaweeds, 13, 46, 47 Serengeti National Park, 140, 170 Setaria, 145 Sevastopol, 22 Shawangunk conglomerate, 90 Sheep, 154, 173, 176 Sierra Nevada, 116 Sigmodon hispidus texianus, 155 Silver Springs, Florida, 17, 32 Simulation models, 185-219 Simuliurn, 28 Sinergism (Plant association), 122-1 28, 129

Skeletonema costatum, 55 Snowshoe hare, 185, 189, 191-198,207, 217

Soils (grasslands), 138-1 39 Solen, 17 Solidago juncea, 126 sorghum, 145 South America, 141 Spartina, 33-35, 143 Sphagnum, 112, 121 Spiders, 35 Sponges, 36 Sporobolus, 143 Springbok, 161, 173 Spring Hares, 160, 161, 170 Springs, 2, 33 Squirrels, ground, 155, 158-160, 162,

Stipa, 143 S t i p comata, 106 stipa pukhra, 127 Streams, 37-38, 62 Succession (Plant association), 84, 91, 92, 107, 112, 128

Sugar maple, 109 Surinam, 119 Sweden, 92, 121 Swift Fox, 162 Sylvilugw, jloridanwr, 193, 215 Symphoricarpos, 158

T Tanzania, 145, 167, 168 Tarangire Game Reserve, 168 Taxidm taxus, 144 Telemetry, 185, 187-189, 193, 196-199, 208, 210-213, 215, 217

Temperature, influence of, 138 Tench, 49 Termitaria, 139, 140, 155, 160-163, 178 Termites, 139, 151, 161 Tetrapogon s p a t h e u s , 145 Texas, 108, 176 Themeda, 145, 146, 167, 177 Thomomys talpoides, 156 Thomson’s gazelle, 172 Tilia amricana, 86, 87, 90, 109 Tomato, 123-126 Topi, 140 Tragelaphys scriptus, 169 Transvaal, 161, 173 Tregaron, Wales, 120 Trophic ecology, 3 levels, 3, 5, 59, 65, 66 Trout, 28, 61, 62 Tsetse fly, 176 Tsuga canccdensie, 87, 90, 91 Tubifex tubifex, 45, 46 Tubificid worms 36 Tucson, Arizona, 158 Typha lutifolia, 12

170

Stabilization (Plant association), 91, 118-122, 130 Steppes, 100, 141, 158, 160 Stellaria media, 126

U Uganda, 165, 177 Ungulates, 138, 139, 140, 146, 160-165,

236

SUBJECT INDEX

Ungulates-continued 157, 159, 165, 169, 172, 173, 175, 177, 178 Unio, 27, 36 University of Minnesota, 188, 218 University of Missouri, School of Forestry, 109 U.S.A., 114, 130, 146, 163, 168, 217 Utah, 114, 154, 171

V Vegetation classification, 84, 101, 103 climax, 85 continuum concept, 85-91, 95-101, 105, 107, 111-113, 118, 128

critical levels, 112-122 dynamics, 84 integration, 107 ordination, 95-101, 102, 103, 112 stabilization, 91, 118-122, 130 succession, 84, 91, 92, 107, 112, 128 universality of divisiveness, 117-1 18 Vineyard Sound, 9, 10 Vulpes julva, 185 Vulpes macrotis, 162 Vulzles velox. 162

Water circulation, 10 Water replacement, 10 Waterbuck, 167 Weight, definition of, 141 Western Harvester Ants, 163 Whiteface Mountain, 112 White spruce, 120 White-tailed deer, 193 White-throated Wood Rat, 159 Whooping wane, 103 Wildebeest, 152, 153 Willows, 36 Wind, 9 Wisconsin, 30, 86, 86, 90, 96, 99, 113, 123

Wolf, 144 Wood rats, 159 Woods Hole, 9 Wyland Lake, 58

X Xerw (a*ums, 170 X-ray diffraction analysis, 115 Y York University, Canada, 102

W Wales.. 103,. 120 Walnut, 123-126 Warbug method, 40 Wart hogs, 155, 162, 167 Washington, D.C., 87, 100, 109, 217

Z Zebras, 176 Zooplankton, 8, 29, 31, 32, 34, 37, 40, 42, 43, 54-55, 60, 63, 64, 67

measurement of, 20-26