Ecological Bulletins, Suserup Skov: Structures and Processes in a Temperate, Deciduous Forest Reserve

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Ecological Bulletins No. 52

Suserup Skov: structures and processes in a temperate, deciduous forest reserve

Edited by Katrine Hahn andlens Emborg

SUSERUP SKOV: STRUCTURES AND PROCESSES IN A TEMPERATE, DECIDUOUS FOREST RESERVE

Ecological Bulletins No. 52

Suserup Skov: structures and processes in a temperate, deciduous forest reserve

Edited by Katrine Hahn andlens Emborg

Ecological Bulletins ECOLOGICAL BULLEfINS are published in cooperation with the ecological journals Ecography and Oikos. Ecological Bulletins consists of monographs, reports and symposia proceedings on topics of international interest, often with an applied aspect, published on a non-profit making basis. Orders for volumes should be placed with the publisher. Discounts are available for standing orders.

Editor-in-Chief

Published and distributed by:

Pehr H. Enckell

Wiley-Blackwell 9600 Garsingron Road Cowley Oxford OX42DQ

Managing Eaitor and Editorial Office: Linus Svensson Gikos Editorial Office Ecology Building S£-223 62 Lund Sweden Email: [email protected] www.oikos.ekol.lu.se

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Technical Editors: Linus Svensson/Gunilla Andersson

Editorial Board, Bjorn E. Berglund, Lund. Tom Fenchel, Helsing0r. Erkki Leppakoski, Turku. Ulrik Lohm, Link()ping. Nils Maimer (Chairman), Lund. Hans M. Seip, Oslo.

Suggested citation: Author's name. 2007. Title of paper. - Eeol. Bull. 52: 000-000.

© 2007, ECOLOGICAL BULLETINS ISBN 978-14-0515-603-5 ISSN 0346-6868 Cover: illustration by Anders Busse Nielsen

Typeset by ZooBoTeeh, Torna Hallestad, Sweden, printed by Wallin and Dalholm, Lund, Sweden.

Preface A striking feature of many western European lowland forests and forest reserves is the scarcity of long-term ecological studies. Moreover, studies are often restricted to few measurements with uneven intervals. In Denmark, two forest reserves have been studied in depth; Suserup Skov and Draved Skov. The research programme Spy-Nat-Force project was initiated in 1999 to study structures and processes in those two semi-natural forests. The purpose was to expand the existing knowledge base about regeneration, soil processes, nutrient cycling, and biodiversity in unmanaged forests and to apply this knowledge as a reference for nature-based forest management in Denmark. This ambition was fulfilled by a cooperative research action, including four research institutions: The Royal Veterinary and Agricultural University (KVL), Forest & Landscape Research Institute (FSL) , University of Copenhagen (KU), and Geological Survey of Denmark and Greenland (GEUS). Seven Ph.D. studies, and numerous M.Sc. and B.Sc. projects were included. This issue of Ecological Bulletins reports a selection of the many research projects undertaken within the Spy-Nat-Force group, focussing on the investigations in Suserup Skov, a small (19 ha), but unique deciduous forest in eastern Denmark, with long forest continuity, low human impact, and a natural disturbance regime. One of the strongest features of the research in Suserup Skov is the combination ofpalaeoecological studies and 1O-year stand-inventories with detailed in-depth studies ofgap dynamics. We focus here on two scales: 1) stand-level investigations and 2) detailed gap studies of an intensively instrumented gap. By combining the findings from the two scales with regard to structures and processes in a long-term perspective it is our hope to present a deeper and coherent understanding of natural forest stand dynamics in time and space. The research presented in this issue was made possible with great support from many sources. First and foremost thanks to Som Academy and director Jens Thomsen for permitting research in Suserup Skov, to the Danish Research Council, the Royal Veterinary and Agricultural University, University of Copenhagen, and GEUS for financial support, Skov- og Naturstyrelsen, the Arboretum, and Kongskilde Friluftsgard for practical assistance, and technicians, students and others for invaluable help in the field and laboratories. This publication has been financially supported by a grant from Aage V. Jensen Foundation for which we are grateful. Finally, the many referees are acknowledged for theif valuable input and great effort in improving the papers submitted.

Katrine Hahn andJens Emborg Frederiksberg,November 2006

ECOLOCICAL BULLETINS ')2, 2007

5

Suserup Skov: structures and processes in a temperate, deciduous forest reserve Katrine Hahn and Jens Emborg

'The history and present conditions of Suserup Skov - a nemoral, deciduous forest reserve in a cultural landscape The structure of Suserup Skov, 2002. The first re-measurement of a long-term permanent plot study of forest dynamics started in 1992 The forest cycle of Suserup Skov - revisited and revisted What is beneath the canopy? Structural complexity and understorey light intensity in Suserup Skov, eastern Denmark Suppression and release during canopy recruitment in Fagus sylvatica and Fraxinus excelsior, a dendroecological stUdy of natural growth patterns and competition Structural impact of gale damage on Suserup Skov, a near-natural temperate deciduous forest in Denmark Above and below ground gaps - the effects of a small canopy opening on throughfall, soil moisture and tree transpiration in Suserup Skov, Denmark Nitrate in soil solution and nitrogen availability in litter and soil after gap formation in the semi-natural Suserup Skov and two managed beech Fagus sylvativa forests in Denmark The carbon pools in a Danish semi-natural forest Nematode assemblges and their responses to soil disturbance differ between microsites in Suserup Skov, a semi-natural forest Gap regeneration in four natural gaps in Suserup Skov a mixed deciduous forest reserve in Denmark Growth and photosynthesis of ash Fraxinus excelsior and beech Fagus sylvatica seedlings in response to a light gradient following natural gap formation Ground flora in Suserup Skov: characterized by forest continuity and natural gap dynamics or edge-effect and introduced species? Natural forest stand dynamics in time and space - synthesis of research in Suserup Skov, Denmark and perspectives for forest management

6

7

19

]. Heilmann-Clausen, R. H. W Bradshaw,]. Emborg and G. Hannon ]. Emborg and J. Heilmann-Clausen

43

M. Christensen,]. Emborg and A. B. Nielsen A. B. Nielsen and K. Hahn

53

]. Emborg

69

]. Bigler and A. Wolf

81

L. Dalsgaard

33

103

E. Ritter

113 123

L. Vesterdal and M. Christensen L. Bj0rnlund and]. D. Lekfeldt

133 147

K. Hahn, P. Madsen and S. Lindholt K. S. Einhorn

167

K. Hahn and R. P. Thomsen

183

K. Hahn, J. Emborg, L. Vesterdal, S. Christensen, R. H. W. Bradshaw, K. Raulund-Rasmussen and ]. B. Larsen

ECOLOGICAL BULLETINS 52, 2007

Ecological Bulletins 52: 7-17, 2007

The history and present conditions of Suserup Skov - a nemoral, deciduous forest reserve in a cultural landscape Jacob Heilmann-Clausen, Richard H. W Bradshaw, Jens Emborg and Gina Hannon

Heilmann-Clausen, ]., Bradshaw, R. H. W, Emborg, J. and Hannon, G. 2007. The history and present conditions ofSuserup Skov -- a nemoral, deciduous forest reserve in a cultural landscape. - Eco1. Bull. 52: 7-17.

Suserup Skov in central Zealand, Denmark represents one of the best examples of a semi-natural beech Fagus sylvatica dominated forest in northern Europe. The forest is developed on rather variable soils, including sandy and clayey glacial tills and lacustrine sediments formed in a final stage of the Weichsel Glaciation. The humus form is generally mull and the vegetation is in most parts dominated by early flowering perennial herbs, e.g. Anemone spp. and Mercurialis perennis. The flora of shrubs and trees is species-rich including ca 30 species typical of mull soils. The most imponant tree species apart from Fagus sylvatica are .Fraxinus excelsior, Quercus robur and Ulmus glabra. The vegetation history ofthe forest has been studied by analysis ofpollen and macrofossils in a sediment core obtained from a small hollow in the forest. The analysis shows that the forest has continuity of trce cover at least back to 4200 BC, indicating it to be a direct descendent of the primeval forests which invaded Denmark after the end of the Weicshel Glaciation, ca 12000 yr ago. The forest composition and the prevailing disturbance regime have changed considerably over the last 6000 yr and the present beech-dominated forest has little in common with the primeval sitUation. Beech occurred for the first time in Suserup Skov ca 1700 BC and became dominant only ca 500 yr ago, together with oak. Before that the forest was a mixed deciduous forest with Alnus, Betula, CoryIus, Fraxinus, Quercus, Tilia, Ulmus and even Pinus sylvestris. Forest fires were occasional until AD 800 and were probably a key in maintaining vital populations of light demanding tree species. The increase of beech seems to be closely related to human impact, especially the cessation of forest fires (natural and anthropogenic) and a shift in human use of the forest landscape from 600 BC to AD 900. Despite the historical impact ftom humans, Suserup Skov is now increasingly characterized by natural disturbance dynamics and is one ofthe best reference areas for naturalness in the nemoral part of northern Europe. This has attracted several research projects focussing on forest dynamics, ecology and biodiversity which are summarized in the paper or reported elsewhere in the current issue of Ecological Bulletins.

}. Heilmann-Clausen ([email protected]), Forest and Landscape Denmark, Univ. of Copenhagen, Rofighedsvej 23, DK-1958 Frederiksberg C, Denmark (present address: HabitatVision, Skadsk@rvej 22, DK-4180 Sor@, Denmark). - R. Bradshaw, Dept ofGeography, Roxby Building, Univ. ofLiverpool, Liverpool L69 7ZT, UK - j. Emborg, Forest and Landscape Denmark, Unit;. ofCopenhagen, Rolighedsvej 23, DK-1958 Frederiksberg C, Denmark. G. Hannon, Southern Swedish Forest Research Centre, Box 49, SE-230 53 Alnarp, Sweden.

Copyright © ECOLOGICAL BULLETINS. 2007

7

Northwestern Europe has been influenced by humans for > 5000 yr, and no large natural areas have escaped cultural impact. The primeval forests, which once covered most landscapes, have vanished, and the persisting forests are fragmented and highly influenced by humans. During the last decades, the attempt to comrol natural processes in forest ecosystems seems to have reached a culmination, as it is recognized that forest biodiversity is seriously declining in the whole region, and it has been realized that traditional forestry is labour expensive and often results in ecologically unstable stands. Instead, increasing emphasis is paid to natural processes and dynamics in forest ecosystems. Nature-based forestry, mimicking natural disturbance regimes and regeneration principles, is increasingly appreciated as a relevant concept in a sustainable, multifunctional forestry which integrates timber production, conservation and an increasing demand for forests as a space for recreation. With this change in focus, semi-natural forests have attracted considerable attention, based on the assumption that such forests provide a key for understanding natural forest processes and their potential in a silvicultural context. The natural processes of semi-natural fCHests in culturally influenced landscapes should however be viewed in the appropriate spatio-temporal context. It is especially important to recognize that present vegetation patterns, even in long-protected forest fragments, reflect the interaction between natural history and cultural influence at the stand as well as landscape scale. Suserup Skov is situated in the central part of the Baltic beech forest region in northern Europe, in an area relatively rich in old beech forest remnants. Suserup Skov has been subject only to limited forest management during the last 150 yr and is one of the best examples of a seminatural beech-dominated forest in northern Europe. The forest has attracted considerable scientific interest during the last decades, culminating in the research programme "SpyNatForce". The specific aim of the present paper is to provide updated background information about Suserup Skov, with special emphasis on forest history and its importance for the present forest composition and vegetation. This will provide a reference for researchers working in Suserup Skov, now and in the future, but will also emphasise for researchers working with forest structure and dynamics in general, that former human impact is just as important to consider as a natural disturbance regime if one wants to understand structures and dynamics of present day forests.

Site description T'he general characteristics of Suserup Skov have been described in several papers. The status given below on landscape and soil development is mainly based on Vejre and Emborg (1996), while the overall vegetation patterns are

8

described inspired by Christensen et al. (1993) and Emborg et al. (1996).

Setting and climate Suserup 5kov (19.3 ha) is situated in central Zealand in the eastern part of Denmark (55°22'N, 11 °34'E)(Fig. 1). The climate of the area is cool-temperate and sub-oceanic with a mean annual temperature of 8.1 °C, and a mean annual precipitation of 644 mm. 'rhe mean temperature of the coldest month (February) is 0.8°C, while that of the warmest month (August) is 16.7°C (Frich et al. 1997, Laursen et al. 1999). The forest is situated on the northern border of the lake '1ystrup So, on undulating south-facing slopes (7-31 m above lake level). To the north and east, the forest borders farmland abandoned since 1993, on which tree growth is slowly expanding from the forest edges. To the west, the forest borders an abandoned, restored gravel pit (last digging in late 1960s), which is now a grazed wooded meadow with a fairly dense growth of 10-20 m tall trees. Further west, the wooded meadow joins with the forest Frederikskilde Skov (ca 15 ha), of which major parts have been declared as unmanaged forest since 2000. The plan for the wooded meadow is for it to remain grazed, with a minimum of human intervention. Within the next 10-20 yr, Suserup Skov will be surrounded by young forests on all sides, except for the southern border which bounds the lake. In the long run, it is planned to be part of a large natural forest area, amounting to ca 100 ha. Suserup Skov is privately owned by the Foundation of Sam Academy, while the surrounding meadows, forests and farmland are owned by the state.

Landscape and soils Suserup Skov is situated in a landscape shaped under the last part of the Weichsel Glaciation (10000-12000 BC). At that time, Tystrup So was part of a melt-water valley draining most ofsouth Zealand. The overall waterflow was northerly where the recipient water body of Kanegat was more or less ice free. At a later stage, the direction of the waterflow in Tystrup 50 reversed due to ice retreat at the southern border of the reservoir, and the water level of the lake gradually declined. The water flow was now southerly and has remained so ever since. The different stages in the ice retreat and the variable water table heights in the late glacial Tystrup So have resulted in the formation of several terraces in the present lake valley, and locally occurring glaciolacustrine sediments are higher than the present water level in the lake (Andersen 193 1). The complex late-glacial history of the area is also reflected in the soil properties within Suserup Skov, with a clear delimitation between undulating upland soils and more flat lowland areas in the central part (Fig. 2), as de-

ECOLOGICAL BULLETINS 51, 200?

Parte

Fig. 1. The location of Suserup Skov in Denmark, and its division into part A, Band C.

scribed in more detail by Vejre and Emborg (1996). The lowland is dominated by homogenous and almost stone free lacustrine sediments and can be subdivided in two distinct land units: a slightly elevated plateau consisting of heavy day soils and a slightly lower area with sandy soils. The elevated clay plateau can be interpreted as the bottom of a small glaciolacustrine lake, created in the terminal phase of the Weichsel Glaciation when the valley was partly filled with ice (Vejre and Emborg 1996). Following this interpretation, the sandy lacustrine deposits are slightly younger and were formed in a larger lake, probably the young Tysrrup So, created after the ice barriers defining the glaciolacustrine lake melted away. The uplands consist ofvarious types ofglacial tills intermixed with patches of glaciofluvial sediments (mostly gravel). Clayey and loamy tills dominate the central part while sandy tills dominate the eastern part. In the central and eastern part, several small gravel pits (diam. < 10 m) show that the glaciofluvial deposits have been exploited to some degree in former times. The highland and lowland parts are more or less clearly separated by a ca 10m high slope, which was probably formed by erosion in the late glacial Tystrup 50. In the eastern and western part of the forest, where lacustrine deposits have a limited extension, the slope continues directly to the present shores ofTystrup 50. Springs occur scattered along the slope, and in several places meter-thick travertine deposits have formed, adding to the heterogeneity of soil types within the forest.

ECOLOGICAL RUU.FTINS 52, 2007

The soil development varies considerably between the upland and lowland soils. The well drained tills of the upland have permitted a deep to very deep soil development (in places to a depth of ca 1.5 m), with extensive leaching of base cations (e.g. Ca and Mg), while the relative contents ofAI has increa.<;ed over time. The dominant humus form however, is mull, with pH in the range of 4-5 (CaCI2 ) (Vejre and Emborg 1996). In the lowland soils, a high water table and restricted drainage has prevented a deep soil development. In the lowest and wettest sandy parts, accumulation of weakly decomposed organic matter has occurred and locally regular peat layers have formed. In the more elevated part, especially in the slightly elevated dayey plateau, soil organic matter is by contrast low, and the contents ofexchangeable Ca, K and Mg high. The humus form here is a rich mull with a pH close to 6 (CaCI2 ), and high rates of biological activity are indicated by a rapid litter decomposition rate (Vejre and Emborg 1996). In addition, the lower lakeside slopes with their springs and travertine deposits are characterized by rich mull soils and a high content of base cations. Topsoil pH values exceeding 7 have been measured in this zone (Feilberg 1993, Moller 1997).

Vegetation Today Suserup Skov is a mixed deciduous forest dominated by ash Fraxinus excelsior, beech Fagus sylvatica, wych elm

9

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Fig. 2. Distribution of main deposit types in Suserup Skov, revised from Vejre and Emborg (1996), with indication of the pollen/ macrofossil core site reported in Hannon et al. (2000).

Ulmus glabra and pedunculate oak Quercus robur, with a rich occurrence of alder Alnus glutinosa along the lake border (Emborgand Heilmann-Clausen 2007). Oak is mostly present as old specimens and contributes significantly to the standing volume even though the stem number is limited. By contrast, elm occurs only as young specimens and contributes significantly to the stem numbers, while the contribution to the standing volume is negligible (Emborg and Heilmann-Clausen 2007). Of the subdominant tree species, large-leaved lime Tilia platyphyllos and sycamore maple Acerpseudoplatanus occur regularly in some parts of the forest, while wild cherry Prunus avium, crab apple Malus sylvestris, rowan Sorbus aucuparia, horse chestnut Aesculus hippocastaneum, Norway maple Acer platanoides and willows Salix caprea and S. fragilis are scattered throughout. Horse chestnut, sycamore maple and Salix fragilis are exotic species and rather recent additions to the tree flora of Suserup Skov. Large-leaved lime is also probably planted, although the species occurred naturally in the forest 5000 yr ago (Hannon et al. 2000). The shrub-layer is dominated by elder Sambucus nigra, hazel Corylus avellana and hawthorn Crataegus spp. with scattered occurrences of spindle Euonymus europaeus, gooseberry Ribes uva-crispa, wild currant Ribes nigrum, R. rubrum, wild roses Rosa spp. and dogwood Cornus sanguinea. Bramble Rubusfructicosus agg. and raspberry Rubus idaeus occur regularly in gaps created after tree death, while dewberry Rubus caesius is common along the lake shore. The various sallow species (Salix cinerea, S. viminalis) also occur along the lake shore.

10

The ground vegetation is dominated by early flowering perennial herbs, typical of mull soils. Dominant and subdominant species include Anemone nemorosa, A. ranuncu-

loides, Circaea lutetiana, Corydalis bulbosa, Galium odoratum, Lamiastrum galeobdolon and Mercurialis perennis. Of the graminoids the most common species are Carex sylvatica, Hordelymus europaeus and Melka uniflora. For more details on the ground vegetation see Thomsen et al. (2005), Hahn and Thomsen (2007). The distribution of tree and plant species is not uniform throughout the forest and Emborg et al. (1996) distinguished between three rather different forest parts (Fig. 1). The western part of the upland soils (Part A, 10.7 ha) is dominated by beech intermixed with ash and oak. Elm occurs abundantly in the understorey. Most large trees have straight boles except for a few very old (250-500 yr) oak trees, indicating a former period of more open conditions. The shrub-layer is poorly developed, except in gaps, and the flora is dominated by early flowering perennial herbs. The northeastern part B (4.9 ha) is characterized by large oaks of which many have short boles and wide crowns, intermixed with fast growing, straight boled individuals ofash, sycamore maple and beech. The shrub-layer is well developed, with large individuals of hawthorn, hazel and crab apple pointing to a more recent period of semiopen conditions. The western part bordering part A stands apart, due to occurrence of many tall, straight-boled oaks, which were most likely planted in an open forest part, early in the 19th century. The differentiation of parts A and B probably reflect differences in the past management re-

ECOLOGICAL BULLETINS 52, 2007

gime interacting with differences in the soil characteristics. The two parts are separated by a distinct earthen bank, which probably divided the forest into separate land use units before 1793 (Fritzb0ger and Emborg 1996). Grazing was most likely pronounced in pan B, which is characterized by sandy soils and a richness of thorny shrubs and low-boled oak trees. The area may have been a wooded meadow before it was fenced. Part A, characterized by more dayey soils, may have been used for feeding pigs on the beech mast and probably has longer continuity as a dosed forest. The forest facing the lake-border, part C (3.7 ha), is characterized by alder stands with a rich shrub-layer, but ash also occurs abundantly intermixed with beech in the higher parts. Two areas along the lake were grazed until ca 1925 and are now covered by rather young forest. The light, south-facing forest edges have a rich flora, containing a mixture of forest, meadow and reed-swamp plants.

The history of Suserup Skov has up to now been investigated following two different approaches. Hannon et al. (2000) analysed the forest development over the last 6000 yr based on pollen, charcoal and macrofossils extracted from a small wet hollow within the forest (Fig. 2), while Fritzb0ger and Emborg (1996) surveyed the recent landscape history of the forest based on a wide range of historical, published and unpublished sources. The two papers are summarised in the present section.

the rich mixed forests of this period (Fig. 3). The pollen composition shows that hazel, lime, pine, oak and alder were the most abundant tree species adjacent to the core site. with some presence of ash, birch, elm and willow. In addition, macrofossil records show that maples Acer campestre and A. platanoides were also present locally. The presence of Quercus petraea macrofossils is noteworthy as this species is not considered native to Zealand today (0dum 1968). Macroscopic charcoal remains and charred wood are regular in the period from 4200 to 3200 BC indicating that local forest fires occurred with intervals of 100-300 yr. A similar flre history has been documented from the nearby forest at Ncesbyholm (Andersen 1989) suggesting that the fire history of Suserup Skov is not unrypical for the region in this period. It is uncertain whether forest fires originated from lightning ignition or represents anthropogenic activity. but there are no unequivocal indicators of human activity in Suserup Skov in the period. The occasional fires helped to maintain local populations of the light demanding species birch and pine, and were most likely also beneficial to oak. There is no evidence that the forest fires were extensive, resulting in large open areas, and tree pollen percentages are constantly high throughout the period (85-90% of tOtal pollen numbers). Such values suggest dosed forest conditions, at least in the vicinity of the hollow, although pollen data alone can underestimate the extent ofopenness (Sugita et al. 1999). Plant macrofossils are very precise indicators of local forest structure and they indicate open, wet conditions at leasr near the sampling site during this period.

Suserup Skov as a mixed primeval forest

Humans move closer

The invasion of forest trees in the Suserup area after the end of the Weichsel Glaciation is not documented by local pollen or macrofossil sources, but it is most likely that the major vegetation development has been rather similar to that described from other sites in eastern Denmark (Iversen 1967). Thus, the first postglacial forests, which grew 10000 BC, were probably dominated by birch Betula pubescens, later also B. pendula and Scots pine Pinus sylvestris with some aspen Populus tremula, willows Salix spp. and junipers Juniperus communis. Plausibly this pioneer forest was gradually invaded by shade tolerant tree-species, first hazel Corylus avellanus and somewhat later also elm (mostly Ulmus glabra) and lime Tilia cordata, T: platyphylla, which became dominants between 6000 and 7000 BC. The light demanding species alder Alnus glutinosa and oak Quercus robur and Q: petraea also invaded during this period, showing that the forest still had room for species with pioneer attributes. The oldest part of the Suserup Skov sediment core, dated to ca 4200 Be and analysed by Hannon et a1. (2000) gives a very good impression of the local composition of

About 3200 BC a distinct change occurs in the pollen composition. The concentration of elm pollen decreases rather abruptly, and somewhat later the same occurs for pine pollen. Oak and ash pollen show an increasing trend, while hazel and lime pollen percentages show highly fluctuating patterns. The shift in pollen composition agrees with the timing of the "elm decline" in other parts of northern Europe and points to a distinct shift in the disturbance regime. which could be imposed in part by an outbreak of the Dutch elm decease. Anthropogenic indicators. as described by Andersen (1989), are not common in Suserup Skov in this period, bur the presence of Rumex pollen suggests human use of the forest to be likely, possibly in the form of limited cattle grazing. Forest grazing would be consistent with the lack of charcoal residues pointing to absence of forest fires in the period, and with the increase in the importance of oak. which is favoured by open conditions (Vedel1969, Van Hees et al. 1996). The deposits dating from 3200 to 2700 Be are extraordinarily rich in well-preserved macrofossils. All tree species

Forest history

ECOLOGICAL BULLETINS 52,2007

11

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r;ig. 3. Diagram of the charcoal concentration, percentage sums for trees, shrubs and herbaceous taxa, selected percentages of tree and shrub pollen (silhouettes) and plam macrofossil occurrence (dots), against calibrated calendar years and sediment depth for Core A, Suserup Skov. Abbreviations: b = bud, br = catkin or bud bract, c = cone, eu :::: eupule, f = fruit, fruidet or fruitstone, fl = flower, I == leaf, n == needle, s == seed, sh = shoot, w =:: wood.

represented by pollen are present, but in addition rowan

Sorbus aucuparia, wild apple Malus sylvestris and bird cherry Frangula alnus are represented. The macrofossils show that both small-leaved and large-leaved limes were present, the former apparently with the highest frequency. The presence of large-leaved lime in Denmark during mid to late Holocene has been disputed (0dum 1968), and the records from Suserup Skov are the first unmistakable proof that the species was indeed present. About 2700 BC a new shift in the forest composition is evident from the pollen deposits. Charcoal residues are again regular and pine pollen percentages increase, while hazel pollen decreases. Oak and lime retain a high and relatively stable occurrence for ca 2000 yr. Thus the forest composition and the disturbance regime seem to be rather similar to the situation before the elm decline. About 2000 BC, cereal and Plantago lanceolata pollen replace Rumex pollen suggesting that forest grazing ceased, while arable farming was initiated in the vicinity. Around 1700 BC beech Fagus sylvatica pollen occurs for the first time in the deposits, but with low frequency. The intensity of anthropogenic activity is uncertain, but the combination of charcoal residues and cereal pollen indicate that some agriculture may have been practised within the present forest.

12

Beech takes over Around 600 BC dramatic changes occur in Suserup Skov. The percentage of tree pollen in the deposits decreases rapidly to ca 50-60% of the total pollen sum, while pollen of Poaceae, cereals and R lanceolata increase. The decline in tree pollen percentages is especially evident for lime, while oak and birch show a weakly increasing trend. These shifts indicate that more extensive clearance for agriculture occurred around, but also within the present day Suserup Skov. It seems most likely that the local landscape in this period was a spatia-temporal dynamic mosaic of arable fields, shrubland and more or less open forest. Possible remains of Bronze Age field borders, in the form of long stony banks, are still visible in the higher parts of Suserup Skov, and suggest that agriculture might have been restricted to these forest parts. After AD 900, tree pollen increases again in importance pointing to a release in the intensity of human use and a regrowth of forest. The new forest however, differed from the forest which grew before local human cultivation, in several respects. It was still a mixed forest, with a diversity of deciduous tree species, but hazel, elm, lime and maple were far less important trees than before and at least smallleaved lime and pine became locally extinct. Another ma-

ECOLOGICAL BULLETINS 52, 2007

jor change is indicated by the absence of charcoal. Fire ceased to be a disturbance factor in the forest after at least 5000 yr of irregular burning. Beech is a particularly firesensitive species and it responds to this altered disturbance regime by increasing in abundance to local dominance. Beech was probably restricted by fire for at least the previous 1000 yr. The local disappearance of pine is also a likely result of the cessation of fire. The previous fire regime was probably largely under anthropogenic control, so the cessation of fire most likely reflects a change in human landuse. Beech shows a steadily increasing trend and becomes dominant, together with oak, ca AD 1500. The tree pollen percentages in the period is stable, ca 60-70% and is thus considerably higher than in the previous open period, but lower than the 80-90% characteristic of the lime period. The hollow from which the pollen core is taken is dose to the present forest border, and the long constant ratio between tree and non-tree pollen after AD 900 could indicate that the northern forest margin has been rather stable since that time.

Suserup Skov in the medieval The first written records ofSuserup date back to the period between AD 1202 and 1214 (Fritzboger and Emborg 1996), at which time a man named Bjorn settled in Suseruposter (East Suserup). He "cut down a great part of the wood and grubbed new land for fertile fields, and he resided there himself and his descendants for a long time" (Liber Donationum of the Cistercian Convent in Som; here cited from Fritzboger and Emborg (1996)). The actual forest clearings have most likely been east of the present Suserup Skovas the pollen deposits show no signs of intensive cuttings in the period. Slightly later records in Liber Donationum state the presence of three separate settlements: Suserup, Suseruposter and Ny Suserup (New Suserup) as well as of Suserup Skov, called Pukizeberg ("silva Susorpe dicta Pukizebiergh"). The precise location of the medieval settlements Suserup, Suseruposter and Ny Suserup are not known with certainty, but all may have been situated within the present day village of Suserup, adjacent to the old mill stream Lynge Bxk, northeast of Suserup Skov. The oldest detailed maps of the area, dating back to about 1770, show Suserup village to be more or less surrounded by forest, and Suserup Skov is coherent with extensive forest tracts to the west. A slightly younger and more detailed map, drawn upon request of the Royal Road Commission in 1799, shows Suserup Skov bordering the village of Suserup and its farmland to the north and northeast, while the western limit is less clear. Suserup Skov was in these times not clearly separated from open arable lands. Suserup village was a forest settlement and its fields were partly covered with trees, some with cereal crops and some which were partially used for grazing. Even pans of the present day forest may have been cultivated from time to

l;~COLOGIC:Al. BULLETINS

52, 2007

time during the period from dle medieval to 1800, but the permanent high tree pollen percentages indicate that the extend of such activities within the forest was limited.

Suserup Skov as a managed forest At ca 1800, Suserup Skov got its present delimitation due to land reforms which significantly changed the land use and ownership patterns in Denmark. Remaining forest, including Suserup Skov, were fenced and protected for timber production. At the same time, the remaining forest and shrub areas outside protected forests were cleared to provide timber and increase arable land. Suserup Skov thus became an isolated forest surrounded by farmland. One of the first steps taken after the conversion of Suserup Skov from multiple use forestry to modern tree production was to record both the stock of trees as well as the fellings. The Erst stock records from 1791 indicate oak was dominant at Suserup Skov with only a low abundance of beech, bur it is not until 1815 that relatively reliable data are preserved giving a more detailed impression of the standing timber volume. Oak still appears to be the most important tree species, but beech volumes are only slightly smaller. Other tree species were present, but only to a very limited extent (Fig. 4). In the next decades, beech volumes increased at the expense of oak, even though the annual felling and thinning records show that approximately equal volumes of oak and beech were removed from the forest (Fig. 5). In 1833, a management plan states that Suserup Skov "contains a considerable stock of old forest, even though it is hardly dense anywhere. An extraordinary regeneration, among which lots of ash and elm trees, have sprouted up" (Fritzb0ger and Emborg 1996). About 20 yr later, the botanist C.T. Vaupell visited the forest and describes that "the young trees have had the opportunity to try their strength against the old". As usual the oak has given no regeneration while there is plenty of elm and especially, beech (Vaupell 18(3). In the 1885 management plan most of Suserup Skov is described as "a scattered stand of huge and tall beech trees with broad canopies mixed with generally sound oak trees and ash and elm trees in different ages". Taken together, these reports give a clear picture of a forest growing gradually denser and darker, due to a vigorous regeneration of beech, ash and elm under an open canopy of old oaks. This undoubtedly reflects the cessation of forest grazing after the forest was fenced. The forest management plans give only few details abour silvicultural activities in the period, but there is rather clear evidence that a limited number of beech, oak and lime trees were planted in the 19th century (Fritzboger and Emborg 1996, Emborg et a1. 1996). Volumes of felled trees were modest and written sources from the 1850s onwards describe the forest as a minimal intervention ornamental forest park (Fritzboger and Emborg 1996). As a testimony from this time, most of the oldest beech trees in

13

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1815 1834 1863 1885 1925 1935 1945 1992 2002

18151834 18631885 192519351945 19922002

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Year

Fig. 4. The development in the estimated total standing wood volume in Suserup Skov since 1815, including trees with DBH exceeding ca 30 em. A shows the development in absolute wood volume, while B illustrates the relative importance ofthe most important tree species. In B "other species" is inclusive of Ulmus and Fraxinus. All pre-1885 measurement were made using the "Ocular Method" involving a considerable element of subjectivity. From 1885 and onwards measurements were made llsing a Vernier gauge implying a higher level of certainty. Finally, the estimates from 1992 and 2002 are based on DBH measurements of all trees in the forest. For further details on estimates before 1992 see Fritzb0ger and Emborg (1996).

Suserup Skov are marked with capital Z's for "Zir" = ornamental, not to be felled. Suserup Skov became an increasingly popular destination for the Sunday picnics of Som residents and a goal for botanic and drawing excursions from the renowned college at the Som Academy. The forest guard cottage "Sarauwsminde" functioned as a sort of tea garden for visitors and public footpaths were established in the forest.

"'0

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Interval (calender years) Fig. 5. The annual fellings in Suserup Skov 1833-1929 simplified from Fritzboger and Emborg (1996). For htrther details see that paper.

14

Suserup Skov as a forest reserve The standing timber volume of Suserup Skcw more than doubled in the period from 1885 to 1925 according to contemporary stock recordings (Fig. 4). This is remarkable as there are no records of a decreasing felling rate (Fritzboger and Emborg 1996). In particular, during World War I, considerable wood volumes were removed from the forest due to compulsory fellings. Most of the old beech and oak trees were however saved throughout the period and younger ash and elm trees apparently delivered most of the volume removed during the war (Fig. 5). It seems most likely that fellings were undertaken carefully with the aim of preserving a rather open forest landscape, and the increase in standing volume in the period was probably mainly due to growth of retained large beech and oak trees forming the canopy. In 1925, Suserup Skov was conserved formally for biological and recreation reasons. Ostenfeld (1926) provides a detailed description of the recently protected forest, which "has been treated with big caution as especially the large trees have not been cut. Only occasionally, single individuals have been removed, because they were declining, dead or because they stood in the way for the free development of particularly beautiful neighbouring trees". The aim of the protection was not to protect Suserup Skov as a strict non-intervention forest, but rather to secure a continuation of the past careful management, as described by Ostenfdd (1926): "The aim of the protection is to conserve the present appearance of the forest, in particular the magnificent old trees. These are in the western part mainly

ECOLOCICAL BULLETINS 52, 20D?

beech, in the eastern part mostly ash, elm and oak. Special attention will be taken to secure that oak and ash can remain to be the most important tree species, and to ascertain that the dominance of beech is restricted to the western part. Likewise, caution will be taken to secure that the very vigorous regeneration of elm not grow so dense that ash and oak, and the natural understorey occurring beneath these tree species, is disturbed". Suserup Skov was considered a historical monument of natural beauty, rather than a dynamic, semi-natural forest. The ideal was the romantic, picturesque, open forest, which was so often depicted on paintings from the late 18th and early 19th century. A committee was set up to secure that the protective guidelines were followed, and the correspondence between this committee and the forest managers gives good insight in the practical management initiatives. It is clear that elm was selectively cut, and attempts were made to eradicate the species from the forest. As late as 1960, it was even discussed if chemical herbicides should be used to achieve this goal. We do not know if herbicides were ever used in Suserup Skov, but the attempt to eradicate elm was only partly successful. In an inventory carried out in 1992 only two elms with a diameter in breast height (DBH) exceeding 50 em were recorded (Christensen and Heilmann-Clausen unpubl.), but the recruitment of young individuals was massive (Christensen et al. 1993). A')h and beech were also cut if they stood in the way for older trees. During World War II, even a few young oak trees were cut. Stumps of 38 large beech and oak trees were still visible in the forest in 1992 (Christensen et al. 1993). Despite the attempts to conserve the "present conditions", Suserup Skov has changed slowly. Most notably the forest grew denser to the detriment of oak. In 1834, 530 living oak trees were recorded in the forest. In 1945 this figure had decreased to 199, of which 159 remained in 2002. In 1961, the protection status was changed and all cutting of trees ceased, except for fallen trees lying across foot paths. In 1968, the buildings of Sarauwsminde burned, and a few large oak trees were cut to make space for fire engines. The effort could not save the buildings, which were later demolished. Since then the forest has invaded the old garden and lawns of Sarauwsminde (ca 0.5 ha).

Suserup Skov as a research environment In 1917, a field station was built at the margin of Suserup Skov, dose to the lake shore, under the auspices of Prof C. Wesenberg-Lund of the Univ. of Copenhagen. The field station was for several decades a highly important institution for research in freshwater biology and parasitology, culminating in the publication of "Biological studies on the River Susaa" (Berg 1948). This publication was, in its

ECOLOClCAL BULLETINS 52,2007

time, the most detailed account on the biology of running waters published worldwide. The official use of the laboratory for field courses and research ceased in 1969, due to the bad stage of the buildings, and an increasing demand for space for students and equipment. No research in forest biology was published in the time of the Suserup Laboratory, so even though the forest was protected as a scientific reserve, its first scientific era was dedicated to the nearby lakes and river. In the late 1960s the forest was increasingly used in the education in forest ecology at the Royal Veterinary and AgricultUral Univ. and a research programme was initiated by Prof. Helge Wedel and Lise Rastad focusing on forest vegetation and regeneration patterns. Unfortunately the results ofthe efforts have not been published. A third research era was initiated in 1992 by two research projects: an all forest inventory and a Ph.D. project focussing on forest dynamics. The projects were at first uncoordinated, but soon contact was established in the field between the respective research teams, and a fruitful collaboration was established bottom up. In the first project (Christensen et al. 1993) a 50 x 50 m grid was marked throughout the forest and all living trees with DBH exceeding 3 em were measured. In addition trees, living and dead, with DBH of 29 cm or more were mapped, for the drawing of a stem position map. The Ph.D. project involved detailed studies on forest structure and regeneration (Emborg et al. 1996, 2000, Emborg 1998), forest history (Fritzb0ger and Emborg 1996, Hannon et al. 2000) and the interaction between soil and vegetation (Vejre and Emborg 1996). The research projects established Suserup Skov as one of the best conserved and well described semi-natural deciduous forests of the northwestern European lowlands, and stimulated a fourth wave of research. The present issue of Ecological Bulletins is the culmination of these efforts, summarizing results from extensive research in forest ecology carried out in Suserup Skov since 1999, Apart from research in forest history, structure and dynamics, several studies have evaluated the importance of Suserup Skov for biodiversity. M011er (1997) coordinated a multi-disciplinary research project in which species richness of higher plams, bryophytes, fungi, lichens, saproxylic dickbeetles, crane flies, oribatid mites, gastropods, birds and bats were investigated in a number of natural/managed forest pairs. The study confirmed Suserup Skov to be of crucial importance for biodiversity, especially to saproxylic organisms, and two mite species new to science were recorded from crumbling beech snags. The flora and wood-inhabiting fungi have been subject to more detailed studies (Feilberg 1993, Graae and Heskj;rr 1997, Heilmann-Clausen 2001, Heilmann-Clausen and Christensen 2003). For the latter group, the locality is considered to be of European importance in a conservation perspective (Christensen et al. 2005). Finally the structure and diversity of the nematode fauna has been studied in some detail; see Bj0fnlund et al. (2002).

15

Perspectives - the value of Suserup Skov as a natural reference The development of Suserup Skov during the last 2500 yr has been closely linked with human activity in and around the forest. The increase in beech to become a dominant tree species is especially the result of human use of the landscape and the forest. The same seems to be true for most beech forests in southern Scandinavia (Bradshaw and Lindbladh 20(4). If there had never been any human activity in and around Suserup Skov, the forest would probably still be dominated by lime and maybe even be affected by forest fires now and then. From a palaeoecological perspective the forest is therefore not very natUral in its present composition. However, most of the processes and structures that characterize the present forest are natural and not results of human activity. In this respect the forest is highly natural and presents a relevant reference for silviculture, nature management and the general understanding of forest ecosystems. This reference value is even enhanced by the fact that the shift from lime dominated mixed deciduous forests to beech dominated stands has been very extensive in the northwestern European lowlands. Beech dominated stands thus dominate managed deciduous forests in Denmark and are even of major conservation interest, because the forest type has been in the region long enough to be crucial for forest biodiversity. In other words, the development of Suserup Skov during the last 6000 yr is deeply imbedded in the overall landscape history. Even though this development has been influenced strongly by humans, we find it relevant to perceive Suserup Skov as one of the most important references for natural forest dynamics, structures and composition in the modern landscape of northwest Europe. Acknowledgements - We are thankful to all members of the Suse-

rup research group for useful comments and information necessary for the complement of this paper. The foundation of SOf0 Akademi is thanked for opening the forest for our research and for practical support throughout the process. Finally the Danish Research Councils are thanked for supporting the Spy-Nat-Force program, without which the current publication would not have been possible.

References Andersen, S. A. 1931. Om ase og terrasser inden for Susas vandomrade og deres vidnesbyrd om isafsmeltningens forl0b. DGU, II rk. 54: 1-201, in Danish. Andersen, S. T 1989. Natural and cultural landscapes since the ice age. - J. Danish Archaeol. 8: 188-199. Berg, K. (ed.) 1948. Biological studies on the river Susaa. - Folia Limnol. Scand. 4: 1 -318. Bj0rnlund, L. et al. 2002. Nematode communities of natural and managed forests - a pilot survey. - Pedobiologia 46: 53-62. 0

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Bradshaw, R. H. W. and Lindbladh, M. 2005. Regional spread and stand-scale establishment of trees in north-west Europe. Ecology 86: 1679-1686. Christensen, M., Heilmann-Clausen, J. and Emborg, J. 1993. Suserup Skov 1992, opmaIing og strukruranalyse afen dansk naturskov. - Skov- og Naturstyrelsen, in Danish. Christensen, M. et al. 2005. Wood-inhabiting fungi as indicators of nature value in European beech forests. - EFI Proc. 51: 218-226. Emborg, J. 1998. Understorey light conditions and regeneration with respect to the structural dynamics ofa near-natural temperate deciduous forest in Denmark. - For. Ecol. Manage. 106: 83-95. Emborg, J. and Heilmann-Clausen, J. 2007. The structure of Suserup skov, 2002. The first re-measurement of a long-term permanent plot study of forest dynamics started in 1992. Ecol. Bull. 52: 19-32. Emborg, J., Christensen, M. and Heilmann-Clausen, J. 1996. The structure of Suserup Skew, a near-natural temperate deciduous forest in Denmark. For. Landscape Res. 1: 31 1333. Emborg, ]., Christensen, M. and Heilmann-Clausen, J. 2000. The structural dynamics of Suserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Ecol. Manage. 126: 173-189. Feilberg,]. 1993. Skovbundsvegetationen i akademiskovene ved SOf0. - Bora og Fauna 99: 23-39, in Danish. Frich P et aL 1997. Observed precipitation in Denmark, 196190. - DMI Tech. Rep. 97-8, Danish Meteorological Insr. Fritzb0ger, B. and Emborg, J. 1996. Landscape history of the deciduous forest Suserup Skov, Denmark, before 1925. For. Landscape Res. 1: 291-309. Graae, B. ]. and Heskj;er, V S. 1997. A comparison of undersrorey vegetation between untouched and managed deciduous forest in Denmark. - For. Ecol. Manage. 96: 111-123. Hahn, K. and Thomsen, R. K. 2007. Ground flora in Suserup Skov: characterized by forest continuity and namral gap dynamics or edge-effect and introduced species? EcoL Bull. 52: 167-181. Hannon, G. E., Bradshaw, R. and Emborg, J. 2000. 6000 years of forest dynamics in Suserup Skov, a seminatural Danish woodland. - Global Ecol. Biogeogr. 9: 101-114. Heilmann-Clausen, J. 2001. A gradient analysis of communities of macrohll1gi and slime moulds on decaying beech logs. Mycological Res. 105: 575-596. Heilmann-Clausen, J. and Christensen, M. 2003. Fungal diversity on decaying beech logs - implications for sustainable forestry. - Biodiv. Conserv. 12: 953-973. Iversen, J. 1967. Naturens udvikling siden sidste istid. - In: N0rrevang, A. and Meyer, T. J. (eds), Danmarks Natur, Bind 1, Landskabernes opsraen, Politikens Forlag, pp. 345-445, in Danish. Laursen E. V., Thomsen R. S. and Cappelen J. 1999. Observed air temperature, humidity, pressure, cloud cover and weather in Denmark - with climatological standard normals, 196190. - DMI Tech. Rep. 99-5, Danish Meteorological Insr. M011er, P F. 1997. Biologisk mangfoldighed i Dansk naturskov. En sammenligning mellem 0stdanske natur- og kulturskove. - Rapport 1997/41, Danmarks og Gr0nlands Geologiske Unders0gelse. 0dum, S. 1968. Udbredelsen af tr;eer og buske i Danmark. Bot. Tidsskr. 64: 1-118, in Danish.

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Ostenfeld, C. H. 1926. Naturvidenskabelige fredninger. - Naturens Verden 10: 166-174, in Danish. Sugita, S., Gaillard, M.-J. and Brostr6m, A. 1999. Landscape openness and pollen records: a simulation approach. Holocene 9: 409-421. Thomsen, R. P., Svenning, J. C. and Balslev, H. 2005. Oversrorey control of understorey species composition in a near-natural temperate broadleaved forest in Denmark. - Plant Eco1. 181:

Vaupell, C. T 1863. De danske skove. Skippershoved (re-issued, 1986), in Danish. Vede1, H. 1969. Kulturskov. - In: N0rrevang, A., Meyer, T. J. and Kehler, S. (eds), Danmarks Natur, Bind 6, Skovene, Politikens Forlag, pp. 200-240, in Danish. Vejre, H. and Emborg, J. 1996. Interactions between vegetation and soil in a near-natural temperate deciduous forest. For. Landscape Res. 1: 335-347.

113-126. Van Hees, A. F. M., Kuiters, A. T and Slim, P. A. 1996. Growth and development ofsilver birch, pedunculate oak and beech as affected by deer browsing. - For. Eco1. Manage. 88: 55-63.

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18

ECOLOGICAL BULLETINS 52, 2007

Ecological Bulletins 52: 19-32,2007

The structure of Suserup Skov, 2002. The first re-measurement of a long-term permanent plot study of forest dynamics started in 1992 Jens Emborg and Jacob Heilmann-Clausen

Emborg, J. and Heilmann-Clausen, J. 2007. The structure ofSuserup Skov, 2002. The first re-measurement of a long-term permanent plot study of forest dynamics starred in 1992..- Ecol. Bull. 52: 19-32.

Suserup Skov (19.2 ha) is an old growrh temperate forest dominated by beech Fagus sylvatica, pedunculate oak Quercus robur, ash Fraxinus excelsior, wych elm Ulmus glabra, and black alder Alnus glutinosa, admixed with lime Tilia platyphyllos and sycamore maple Acer pseudoplatanus. In 1992, a complete inventory of trees exceeding 3 em in diameter at breast height (DBH, 1.3 m above forest floor) was carried out, as a starting point to study the longterm dynamics of the forest. In 2002 a first re-inventory was carried out including all trees ~ 29 em DBH in the whole forest, while trees with DBH > 3 cm were remeasured in three 1 ha plots. Based on the new inventory changes in the forest structure are analyzed and discussed in relation to ecological stability and forest management. A stem-position map based on the 2002 data was made to present an overview of the changes since 1992 and also as a practical rool for future research. The tollowing conclusions were reached from the analysis of the results of the 1992 and 2002 inventories. 1) Between 1992 and 2002 Suserup Skov has been impacted by two important disturbances: an extreme storm and the Dutch elm disease. As an ecological system, the forest has proved relatively resistant. Although some changes have occurred in the diameter distribution, the forest ecosystem has not been pushed back into an early successional stage and no decline in the standing volume occurred. 2) The forest is still undergoing changes resulting from the cessation oflivestock grazing around 1807 and the subsequent gradual cessation of management. Oak is retreating from the stand, while beech is losing some terrain to ash, lime and sycamore maple after a period of extensive dominance. On the wetter ground at the lake-shore, alder is still dominant, but ash is increasing. 3) The ecological disturbance caused by the 1999-storm has interacted with and speeded up the ongoing gradual long-term successional changes predicted in 1992. A fair number of large beech trees were blown over in the storm, whilst trees in smaller diameter classes were less affected and have shown vigorous growth. Especially sycamore maple, lime and (to some degree) ash have increased in importance, being capable of filling many of the gaps created where mature beeches have fallen.

J Emborg (jee@life·ku.dk), Forest and Landscape Denmark, Univ. of Copenhagen, RolighedlVej 23, DK-1958 Frederiksberg C, Denmark. -J Heilmann-Clausen, HabitatVision, Skt£skfiJrvej 22, DK-4180 SorfiJ, Denmark.

Copyright © ECOLOGICAL BULLETINS, 2007

19

In a previous paper (Emborg et al. 1996) we established a basis for long-term studies of forest dynamics in Suserup Skov, which is one of the most interesting old growth deciduous forests in north-western Europe. This was done by presenting basic data on forest structUres based on fieldmeasurements carried out in 1992. Repeated measurements of basic structural data represent a simple and reliable approach to the study of forest dynamics. The problem with this type of study is, however, that they require a long period of time and a long-term commitment, i.e. they are difficult to sustain. This article represents the second step in a hopefully long chain of recordings in which long-term changes in the stand structure of Suserup Skov will be monitored. Each recording will document the actual state of the forest over time - like a time-series of photos. The first picture is from 1992. This article presents the 2002picture, documents changes since 1992, and discusses the current development of the forest ecosystem.

The site Suserup Skov (19.2 ha) is an old growth temperate deciduous forest, situated north of lake Tystrup 50, on the island ofSjadland (Zealand), Denmark, 55°22'N, 11 °34'£. The site has been intensively studied during the last decade and several scientifIC articles have been published, dealing with the history, ecology and biodiversity of the forest (Fritzb0ger and Emborg 1996, Vejre and Emborg 1996, Emborg et al. 2000, Heilmann-Clausen 2001, HeilmannClausen and Christensen 2003, Thomsen et al. 2005). It supports mixed stands dominated by beech Fagus sylvatica, pedunculate oak Quercus robur, ash Fraxinus excelsior, wych elm Ulmus glabra, and black alder Alnus glutinosa, with lime TiNa platyphyllos and sycamore maple Acerpseudoplatanus otherwise important. The soils are of glacial origin. They vary in composition and include clayey, loamy and sandier deposits as described in detail by Vejre and Emborg (1996). Much of the site supports relatively fertile, mesotrophic soils that are moderately free-draining, but locally in a low central plateau the soils are gleyed due to waterlogging. Conditions for tree growth are generally favorable, as indicated by an upper canopy height of ca 40 m (Emborg et al. 1996). According to pollen and macrofossil records it seems likely that Suserup Skov has been under more or less continuous tree cover since forest vegetation spread in the landscape after the last ice-age (Hannon et al. 2000). For various reasons the site has never been cleared completely, though it undoubtedly has a long history of human use, acting ace; a source for wood and other materials and for grazing livestock. The forest was not commercially exploited for timber during the 18-19th centuries, which is exceptional for north-western Europe. In 1854 the owner, Sam Academy, decided to protect Suserup Skov by not allowing commercial forest management. Although some

20

limited tree cutting and removal of dead wood took place until 1961, the forest has since been kept as a strict nonintervention reserve (Fritzb0ger and Emborg 1996). For an overview of the history of the forest see HeilmannClausen et al. (2007).

Methods The site was partitioned into three distinct ecological units when the study was initiated in 1992 (Emborg et at 1996). These were named part A (10.7 ha), part B (4.9 ha) and part C (3.7 ha). Each represented a distinctive set of environmental conditions and had a different forest history. In the 1992 recording, the forest (part A, B, and C) was divided into 50 X 50 m (0.25 ha) plots. All stems:2: 3 cm DBH were measured to the nearest 2-cm diameter-class in each plot and the position of trees:2: 29 cm DBH was recorded. The 2002 recording repeated the 1992 methodology, except for two points: 1) tree heights were not measured in 2002, and 2) trees with DBH:2: 3 cm were in 2002 recorded only in three 1 ha (100 X 100 m) sample plots (AI, Al, Bl) from parts A and B, representing different forest development types: plot Al was situated on undulating loamy tills and was selected to represent a typical beech/ash dominated stand with some remaining large, old oaks. Plot Al was situated on flat, fine-grained, mainly lacustrine sediments and was similar to plot AI, except for the presence of lime. Plot B1 was situated on undulating, mainly sandy tills and was selected to represent part of the former wood-pasture area, where mature oal<s were prominent amongst younger ashes and expanding sycamore maple. The fieldwork was carried out during the summer of 2002. The inventory was based on the 50 X 50 m grid established in 1992, which was marked in the field by numbered steel poles. The position and size of all trees :2: 29 cm DBH (dead or alive, upright or fallen) was recorded. The location of new trees that had recruited since 1992 was determined by sighting and measuring from the grid. The position of surviving trees was checked only where these appeared to be misplaced. The size of trees :2: 29 em DBH was measured as a circumference with a measuring tape (and converted to diameter assuming they were circular in cross-section). Smaller trees had the diameter measured with calipers.

Density, basal area and standing volume calculations The density (of trees :2: 29 cm DBH) came directly from the total inventory. Basal area (BA) was computed per diameter-class f()r each species, assuming BA ::: (d/2)2 X Tt, where d == DBH. Standing volume was computed per diameter-class for each species, using the equation SV : : ; BA X

ECOLOGICAL BULLETINS 52, 2007

h x f, where BA:::: basal area, h tree height, and f = form factor (the ratio of tree volume to the volume of a geometrical solid, here a cylinder, that has the same diameter and height as the tree, Husch et al. 2003). Multiple stems arising from one individual were recorded and treated separately for exact calculation ofbasal area and standing volume. Tree heights (h) were calculated per tree species and DBH-dass using the d/h-regressions developed by Emborg et a1. (1996): h "" H dom X «d/(d+k»3) + 1.3, where d = DBH; H d ::: dominant (maximum) tree height; and k::: constant d~~ermining the inflection point of the sigmoidal curve. The curve passes the point (0, 1.3), performs an "5" asymptotically approaching the value of H dom for increasing diameters. Species-specific d/h-regressions were computed for beech (n=482) and ash (n=214). The d/h-relation for oak was graphically estimated (n=31), whilst all other species were pooled to compute a common d/h-regression (n=215). For further details see Emborg et a1. (1996). Form factors (f) were taken from the Danish standard forestry yield tables (Madsen 1987). The error caused by using forestry yield tables is unknown, but presumably small since the tables are based on single tree volumes, having entries for both height and diameter. For other species we simply used the yield table for beech because no form factors were available for them. Annual growth rates (DBH mm yr- 1) were calculated per tree species based on trees ~ 29 em DBH in 1992 that remained alive in 2002. To provide an annual rate for each tree, overall changes in DBH over 1992-2002 were divided by ten years. Throughout the paper the term "small trees" is used for trees 2:: 3 and < 29 cm DBH, whilst "large trees" is used for trees 2:: 29 em DBH.

Climate and disturbances in the period 19922002 Certain events during 1992-2002 had an important impact on stand development. Over the decade the temperature was higher than normal. The mean annual temperature was 8.3°C (varying from 6.8°C in 1996 to 9.2°C in 2002), which was O.6°C above the long-term average (1873-2003, Cappelen 2004). The average annual precipitation was 741 mm, varying from 505 mm (1996) to 905 mm (1999), which was slightly above the long-term average of674 mm (Cappelen 2004). No exceptional drought periods or extreme winter conditions occurred but there was a majo!" hurricane event. This was the most important climatic event in the period. It struck the southern part of Denmark with severe strength on 3 December 1999, and was the strongest windstorm ever recorded in Denmark (the climatic station at Flakkebjerg, 13 km from Suserup Skov, measured gusts at 45 m $.-1). The hurricane was of rather shan duration - some eight hours at full strength -

ECOLOGICAL BULl.ETINS 52, 2007

but occurred after a period ofheavy rain. It caused massive uprooting of trees throughout Denmark and was a major disturbance event in Suserup Skov. For a more comprehensive description of the storm and its immediate consequences for Suserup Skov see Bigler and Wolf (2007). Another important disturbance agent in 5userup Skov during 1992-2002 was Dutch elm disease. This is a response to infection by the fungus Ophiostoma ulmi s1, which is spread by Sco/ytus beetles and often results in the death of elm trees (Rohrig 1996). It was observed for the first time in the early summer of 1994, at the northern edge of the forest. Since then, it has spread widely, killed a large number of elm trees, and created numerous canopy gaps.

Results Stem position map Based on the inventory we produced a 2002 stem position map, which is interesting to compare with the map of 1992. The two maps are shown in Fig. 1 and 2.

Density, basal area and standing volume, large trees The total number of trees 2:: 29 cm DBH increased in all three parts (A, B, and C) of the forest from 1992 to 2002 (Table 1). This means that the number of trees growing into the group of trees 2:: 29 em DBH exceeded the number of trees that died or fell over. The basal area and standing volume changed little in parts A and B, whilst part C experienced an increase in basal area and standing volume of almost 20%. At the tree species level, it is clear that oak decreased in density, basal area and volume in all three parts, both absolutelyand relatively (Fig. 3). Beech also showed a relative decline in standing volume in all forest parts (Fig. 3), but at the same time increased in numbers (Table 1), indicating that its decline in importance was mainly due to the loss of large trees in the 1999 hurricane. Ash increased in relative importance in parts A and C, but declined in part B (Fig. 3). This was mainly due to a loss oflarge ash trees, as the number of ash actually increased in all three parts. Of the subordinate tree species, alder, lime and sycamore maple increased in relative importance in the forest parts where they occurred (Fig. 3). This was especially evident for sycamore maple in part B and alder in part C. Despite the outbreak of Dutch elm disease, elm did not decrease in relative importance (Fig. 3) or in numbers, basal area or volume (Table 1), apparently because of significant regeneration and growth of surviving trees. Finally, changes in the combined group oflow frequent "other species" were relatively limited in all parts of the forest.

21

tv tv

'N

Ol3J

o

f~

56

~(~

~~ )~ cJ,;i ~ ......,..

o,(J)

o

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.

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Suserup skov 1992

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ill

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51 - 75

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0

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•

76 - 100

@

0

Aesculus hippocastaneum

•

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101 - 125

•

•

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~

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126 - 150

x

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0

Serbus aucuparia

176 - 200

~

Alnus glutinosa

@

Corylus avellana

>200

()

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+

Euonymus europaeus

()

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•

Sambucus nigra

•

151 - 175

100 Meters

()

•

• •

50 !

Other Fall direction

X

Dead

N

o

~

Fig. 1. Stem position map including all trees (trees;:::: 29 cm DBH) recorded in 1992. The dotted lines indicate an existing network of footpaths. Drawn by Morten Christensen, Martin Kyhn and Anders Busse Nielsen. The map is available in electronic form from the authors of the paper or download the figure as file EcoLBull.52 from <www.oikos.ekoLlu.se/appendix>.

;.2

'N

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~

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/

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0

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e

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•

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126 - 150

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0

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176 - 200

•

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®

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()

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151-175

50

I;; / ~

\ ....•. ~~-~-~~_/~/.

Species

I

./

25 - 50

• • N \.H

~

(WI)~

Fig. 2. Stem position map including all trees (trees:2 29 cm DBH) recorded in 2002. The dotted lines indicate an existing network of footpaths, Drawn by Morten Christensen, Marrin Kyhn and Anders Busse Nielsen. The map is avaIlable in electronIc form from the authors of the paper or download Ule figure;b file EcoI.BuI1.52 [rom <www.oikos.ekol.lu.se/appcndix>.

Table 1. Density, basal area and volume of large trees (::::: 29 cm DBH) in the three forest parts recorded in Suserup Skov in 1992 and 2002. No. of trees ha- 1

Basal area m 2 ha~"l

Volume m3 hal

Proportion of volume (%)

1992

2002

1992

2002

1992

2002

1992

2002

46.7 18.8 5.5 1.9 2.3 1.1 76.4

56.9 26.7 4.7 2.2 3.9 1.4 95.9

19.0 3.5 5.6 0.4 0.2 0.2 28.9

18.8 4.3 4.8 0.5 0.4 0.2 29.0

381.7 67.1 97.8 5.7 3.1 2.5 557.8

370.4 81.2 84.1 7.3 4.9 3.5 55'1.3

68.4 12.0 17.5 1.0 0.6 0.4 100.0

67.2 14.7 15.3 1.3 0.9 0.6 100.0

6.7 30.4 25.3 18.0 8.2 2.0 90.6

11.8 35.9 28.0 16.3 10.2 1.4 103.6

0.8 "10.6 7.4 14.1 1.0 0.3 34.3

1.5 10.3 7.1 13.5 1.1 0.2 33.7

11.3 209.0 150.2 244.3 14.0 4.0 632.9

20.2 201.6 143.3 235.1 13.7 3.2 617.1

1.8 33.0 23.7 38.6 2.2 0.6 100.0

3.3 32.7 23.2 38.1 2.2 0.5 100.0

75.4 30.0 20.0 3.2 4.1 2.4 135.1

88.1 34.6 24.1 2.4 4.3 4.1 158.1

9.3 10.6 4.7 2.0 0.4 0.3 27.4

12.5 11.1 6.2 1.5 0.5 0.6 32.5

126.3 208.0 93.4 34.3 5.7 3.9 471.6

172.6 216.7 123.4 25.5 6.6 8.8 554.7

26.8 44.1 19.8 7.3 1.2 0.8 100.0

31.2 39.1 22.3 4.6 1.2 1.6 100.0

Part A (l 0.7 hal

Fagus Fraxinus Quercus Tilia Ulmus Other species Total Part B (4.9 ha)

Acer Fagus Fraxinus Quercus Ulmus Others species Total Part C (3.7 ha)

Alnus Fagus Fraxinus Quercus Ulmus Other species Total

Mortality, in-growth and growth of large trees Figure 4 presents an overview of the turnover in standing volume in the three forest parts due to mortality, in-growth and growth of surviving trees. Beech, ash and oak suffered from a loss of volume due to mortality in all parts of the forest. This was especially distinct for beech, which suffered a high loss in all forest parts. Ash mortality was highest in part B, whilst oak loss was relatively even. Alder and elm accounted for a notable amount of the volume lost due to mortality in parts C and B respectively. Beech and ash accounted for most of the in-growth volume in parts A and B, whilst alder, beech and ash accounted for most of the in-growth volume in part C. In part B, elm and sycamore maple contributed significantly to in-growth volume in addition to beech and ash. In contrast, hardly any oaks passed the 29 cm DBH threshold. For beech, the increase in volume of surviving large trees exceeded the contribution from in-growth in all forest parts. For ash these two values were rather similar in parts A and B, while elm and sycamore maple had much greater in-growth than growth oflarge trees present in 1992. Average growth rates of surviving trees were calculated between 1992 and 2002. Average rates for beech, ash, syca-

24

more maple, lime and elm were between 4-5 mm yr- I (Fig. 5). For oak the growth rate 0.9 mm yr- I ) was significantly lower than in other species, while alder had a slightly, but not significantly lower (3.2 mm ye l ), growth rate than most other species. A more detailed analysis of average growth rates in ash, beech and oak (results not shown) revealed that the growth rates for beech and ash decreased significantly for trees> 69 and> 89 em DBH respectively. Oak, unlike beech and ash, showed low growth rates across its size range, no doubt related to overtopping and canopy competition from beech and ash.

Diameter distributions, large trees The distribution of trees across DBH classes changed from 1992 to 2002 (Fig. 6). In all three forest parts there was a marked increase in the number of trees smaller than ca 70 cm DBH and a less distinct decrease in the number of trees larger than ca 70 cm DBH. This was related to: 1) the loss of large trees in the 1999-storm; and 2) the vigorous recruitment of smaller trees. These changes pushed the diameter-distributions in all three parts towards a steep negative exponential curve, with a tendency to stronger recruit-

ECOLOGICAl BULLETINS 52, 2007

Part A

mem in the smaller diameter-classes and a general smoothing across the larger diameter-classes (which in 1992 had a slight peak around ca 90-100 cm DBH).

Fagus Fraxinus Quercus Tilia

Ulmus

60

Other spp.

40

Detailed study including all trees DBH, I-ha intensive plots

~3

em

20 Ot-'-...IIIiIIIi.........,.l-IIIIIIlIIiI.....--III~........--~--. . . .. . . . - - - - - .

Plot Al is, with respect to small trees (3-29 cm DBH) representative of the beech-dominated part A (without lime and sycamore maple) with elm and ash as subdominams (Table 2). The proportion of the BA in the plot made

-20 -40 -60

Part A

-80

Fagus Fraxinus Quercus Tilia

3

Ulmus

Other spp.

N

2

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0

-..

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c 0

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ker

3

Fagus Fraxinus Quercus Ulmus Other spp.

20 10 O~-'--.....

-10

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Fagus Fraxinus Quercus Ulmus Other spp.

-40 -50

(\j

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()

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ker 30

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o o

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Fagus Fraxinus Quercus Ulmus Other spp.

40

\-

()

(l)

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---

(l)

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co

30

-1

20

-2

10

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Part C

E 6

Alnus Fagus Fraxinus Quercus Ulmus Other spp.

O+-'-....IlIIIIIt...............................IIIIiIIIII.......-IIIIlIiIII~-"- ..........,..:;~........

-10 -20

4

-30

2

-40

0 ~2

Din-growth

III

Growth of surviving trees

•

rvbrtality

-4

-6

Fig. 3. Proportional increase or decrease in standing wood volume of large tress (2 29 cm DBH) for different tree species in each of the three forest parts recorded in 1992 and 2002 in Suserup Skov. The figures illustrate change in the relative contribution of each species to the total wood volume at each date. Note variable scaling of the y axes.

ECOLOGICAL BULLETINS 52, 2007

Fig. 4. The contribution to changes in wood volume between 1992 and 2002 in each of the three parts of Suserup Skov, distinguishing between "in-growth", i.e. trees growing into the survey (reaching 29 cm DBH) between 1992 and 2002, "growth ofsurviving trees" i.e. increase in standing volume of living trees (2 29 em DBH) present in both 1992 and 2002, and "mortality", i.e. trees ~ 29 em DBH in 1992, which died between 1992 and 2002. Note variable scaling of y axes.

25

7

Be

C

....... 6 (ij

~5

E 54 Q)

T§3 .c:.

~2

e

(') 1

o Quercus Alnus

Ulm us rilia

Fagus Fraxinus Acer

Tree species Fig. 5. Average diameter growth rates of the main tree species in Suserup Skov based on repeated DBH measurements ofindividual trees in 1992 and 2002. Different letters indicate tree species with significantly different average growth rates (p<0.05; ANOVA, Tukey test). up by beech was very similar for small and large trees, while ash was more prominent among the small trees (Fig. 7). Elm was represented almost exclusively by smaller trees, whilst small trees of oak were absent, even though it represented 31 % of the BA of large trees (Fig. 7). The number of small trees in the plot had decreased considerably since 1992 (Table 2). This was because some trees grew over 29 cm DBH in the period and, more importantly, because mortality was high and far exceeded recruitment (Fig. 8). Change in the total basal area was not so pronounced, because the average basal area of remaining small trees relatively increased (Table 2). Beech retained its importance among the smaller trees in the plot, and showed a distinct increasing trend in relative importance since 1992 (Table 2). Ash decreased in relative importance, because a relatively large number of trees reached 29 cm DBH and mortality was high amongst those that did not. Elm remained relatively stable, as Dutch elm disease only affected the plot slightly. In summary, this plot seems to have been rather stable with ash and beech remaining the main competitors f()f light and space. Plot Al, like plot AI, is dominated by beech, but is in a section where lime is prominent and ash scarce. Beech and elm were clearly dominant among the small trees in this plot, while lime and ash were present in smaller quantities. The relative contribution to the BA ofsmall and large trees was similar amongst beech, ash and lime (Fig. 7). As in plot AI, elm was strongly overrepresented by small trees, while oak occurred only as a large tree (Fig. 7). The number ofsmall trees in the plot increased slightly over the study period, with increases in the number oflime and elm and declines in the number of beech and ash (Table 2). Relatively, the proportion of ash declined dramatically from 13%) in 1992 to 4% in 2002. This was due to a high proportion of ash (30%) growing into the group of

26

large trees and only minimal recruitment (Fig. 8). The numbers and BA of lime and elm increased, and both increased their relative proportion of BA among the small trees. Overall, the plot seems to represent a rather steady development in which oak is losing territory, whilst elm and lime are expanding. Plot B1 is representative of the oak-rich Part B area of the forest, but has more sycamore maple than the average for part B. Among the small trees, sycamore maple, beech and elm were dominant, with the last species represented by high numbers of mostly small trees Crable 2). It is distinct that beech and ash mostly contributed to the BA of large trees, whilst sycamore maple contributed mostly to the BA of small trees (Fig. 7). Elm and oak, like in the two other plots, show completely opposite patterns. Elm thus was almost absent among the large trees but accounted for 35% of the BA of small trees, whilst oak was present only as large trees, accounting for 44% of the BA of such trees. The total number of small trees in the plot decreased considerably due to high mortality rate except in sycamore maple. In elm the decrease was mostly due to Dutch elm disease, while competition was important for decline in beech and other species. Also the number of trees reaching 29 em DBH was rather high, especially for sycamore maple and beech (Fig. 8). Sycamore maple increased its proportion of the basal area (Table 2) from 24 to 30% at the expense of all other tree species except ash. Overall sycamore maple seems to be strongly expanding in the plot, while oak and (to a lesser extent) beech is declining. Ash seems to be maintaining itself, whilst elm is in decline mainly due to the Dutch elm disease.

Discussion Disturbances and the overall stability of the systenl In 1999 Suserup Skov was hit by the strongest storm recorded in Denmark (since 1874). This gives a unique opportunity to evaluate the resistance and response of the ecosystem to this type of ecological disturbance. The storm caused severe wind-throw in many forests and plantations in southern Denmark. The total volume of downed or damaged trees exceeded 3.4 million m3, equivalent to more than twice the annual cut for the whole country (Fodgaard and Enevoldsen 2001). It was therefore surprising that over the studied 10-yr period in Suserup Skov, we found that the overall standing volume of wood actually showed a slight increase. This does not, however, mean that the forest was unaffected by the storm. The diameter distribution of trees clearly changed during the IO-yr period: partly as a result of the storm "harvesting" larger trees, and pardy because of

ECOLOGICAL BULLETINS 52, 2007

Part A 50 •

40 CI:l

02002

...c "-

ill

a.

1992

30

(/)

ill

~

20

I-

10 0 29

39

49

59

69

79

99

89

109 119 129 139 149

DBH class (em)

Part B 40 .1992 CI:l

r:

30

02002

tu

a. (/)

20

ill ill

~

10

29

39

49

59

69

79

89

99

109

119 129 139 149

159 169 179

189 199

DBH elass (em)

Part C 70 CI:l

..c: 03 a. U)

Q)

~ f-

60

.1992

50

D 2002

40 30 20 10 0 29

39

49

59

69

79

89

99

109

119

129

139

DBH class (em)

Fig. 6. Diameter class distributions (10 em intervals) oflarge trees (229 em DBH) in 1992 and 2002 in Suserup Skov. The figure shows the distributions for all trees pooled in each of the three forest parts. For each diameter class the minimum DBH is given. Note the general increase in tree numbers:S; 69 em DBH and decrease in tree-numbers> 69 em DBH in parts A and B.

ECOLO(;!CAL BULLETINS 52, 2007

27

Table 2. Density, basal area and relative proportions of small trees (23 em and < 29 em DBH) in the three intensive plots recorded in Suserup Skov in 1992 and 2002. No. of trees ha-1

Basal area m2 ha-1

Proportion of trees

Proportion of BA (%)

(%)

1992

2002

1992

2002

"[992

2002

1992

2002

412 191 362 32 997

368 118 316 20 822

41 19 36 3 100

45 14 38 2 100

5.14 3.99 2.48 0.39 12.00

5.87 3.18 2.33 0.23 11.61

43 33 21 3 100

51 27 20 2 100

209 23 41 270 33 576

180 17 48 310 27 582

36 4 7 47 6 100

31 3 8 53 5 100

3.08 0.75 0.57 1.43 0.11 5.94

2.91 0.24 0.76 1.75 0.08 5.74

52 13 10 24 2 100

51 4 13 30 1 100

122 39 141 564 61 927

80 25 114 471 34 724

13 4 15 61 7 100

11 3 16 65

3.03 0.76 2.71 4.15 0.44 11.09

2.22 0.62 2.69 3.06 0.26 8.85

27 7 24 37 4 100

25 7 30 35 3 100

Plot A1

Fagus Fraxinus Ulmus Other species Total PlotA2

Fagus Fraxinus Tilia Ulmus Others species Total Plot Bl Fagus Fraxinus

Acer

Ulmus Other species Total

a strong recruitment of smaller trees. For trees:;;::: 29 em DBH, the diameter distribution developed closer to negative exponential curve, particularly because the 1999 storm removed a lot of large trees that originally formed a "hump" in the size-distribution. It has traditionally been believed that unmanaged, old growth forests characterised by frequent but relatively small disturbances tend to develop negative exponential (reverse-J) distributions at a relatively small scale (Cousens 1974, Oliver and Larson 1990, Peterken 1996), while early successional or severely disturbed forests tend to show normal (bell-shaped) size-distributions (Hough 1932, Veblen 1992, Peterken 1996). On this background, Emborg et al. (1996) concluded that the hump in the size-distribution could be traced back to a major regeneration event in the decades after the forest was fenced against grazing animals in 1807. The approximation of the diameter-distribution in Suserup to the negative exponential function taking place from 1992 to 2002 could accordingly be interpreted as the 1999 storm counterbalancing former cultural impact. Recent reviews (Rubin et al. 2006, Westphal et al. 2006) however, have shown that the diameter-distribution in unmanaged old growth forests often have a systematic deviation from the negative exponential distribution, quite similar to the hump in the 1992 dataset. The resulting, so-called rotated sigmoid diameter distribution appear to be pronounced in virgin beech forests in SE-Europe and seem to reflect a low

28

5 100

mortality rate among vigorous canopy trees successfully reaching the canopy, succeeded by increasing mortality among very large, ageing trees (Westphal et al. 2006). Following this concept the change in diameter-distribution from 1992 to 2002 might in fact express a fluctuation away from a "natural" normal diameter-distribution in unmanaged beech forest caused by the heavy storm disturbance. The other major disturbance agent observed during the study period was Dutch elm disease. This started to spread from about 1994 (Emborg et al. 1996). By 2002 dead elm trees could be seen allover the forest and several new canopy gaps had been created where groups of 10-20 m tall elm had been killed (see Christensen et al. 2007 for more details). Considering the dramatic attack, it is somewhat surprising that this is not reflected more strongly in the results of this study. Nevertheless, among the large trees, a considerable number of elm trees have died and the net diameter-growth of surviving trees is close to zero in all three areas studied (parts A, Band C, Fig. 2). This has, however, been compensated for by plentiful recruitment of smaller elms into the group of large elms, very similar to the response reported by Peterken and Mountford (1998) from an unmanaged elm stand in the UK subjected to the same disease. The more detailed analysis of the number of small elm trees in the three intensive 1ha study plots showed a remarkable variation in turnover:

ECOLOGICAL BULLETINS 52,2007

there was a net loss in plots Al and B1, whereas in plot A2 there was a considerable net gain. This seems to reflect differences in the timing and intensity of elm disease attack. It is most likely that the attack will continue and it is too early to evaluate the full consequences ofthis relatively slow developing disturbance of the system. However, it is probable that it might produce a long rotation of small, slow-growing elm because vigorous trees are most susceptible to the disease (Peterken and Mountford 1998). Elm might therefore be able to maintain itself as an important

Plot A1

-20

~ a.

-30

E Cf)

o

~

(J)

Fraxinus Quercus

Ulmus

Other spp.

Plot A2 50

c

20

(J)

-5

30

m

20 10

Fraxinus

Tliia

Fagus

Fraxinus

Ulmus Others spp.

10

o

c o

-10

ro

-20

~

ID c ~

40

Fagus

40 30

E :::s

B

Q)

~

Plot A2

.0

£;

60

-40

I+-

Fagus

~

(l) 0)

-30

Plot 81

c

Acer

CO

o Fagus Fraxinus Quercus Tilia

B o Plot 81 C o :eo 40

Ulmus Other spp.

I+-

Q.

e

a3

co

'(j)

0..

-10

40 30

C/)

co ......

c

......

Q)

N

c

0

~ ......

g

~

S5 .,...

50

0

Other spp.

10

60

10

Ulmus

Fraxinus

N

C/)

;?

u

Fagus

20

C/)

20

~

Plot A1

..c (,)

20

m c

10

:e g,

-10

Ulmus Other spp.

o

e 0..

-20

-30

30

-40 20

-50

10

o Acer Fagus Fraxinus Quercus Ulmus Other spp.

D

Large trees (~ 29 cm)

•

Small trees (~ 3 cm and < 29 em DSH)

Fig, 7. The proportion of the basal area made up by each tree species in 2002 in the three intensive plots, distinguishing between small and large trees. Note variable scaling of y axes.

ECOLOGICAL BULLETINS 52, 2007

o

Trees reaching 29 em DBH 1992-2002

•

In-growth minus mortality 1992-2002

Fig. 8. Change in the number of small trees (~ 3 and < 29 em DBH, including all stems on each individual) between 1992 and 2002 in each of the detailed plots in Suserup Skov. White columns show the proportion of trees present in 1992 reaching DBH ~ 29 cm in 2002, while black columns show the net change resulting from new trees reaching 3 em DBH ("ingrowth") less those that died (i.e. trees present in 1992 and dead by 2002). Negative values shows that mortality exceeded ingrowth in the period, while positive values shows that in-growth exceeded mortality.

29

component of the understorey (Emborg et al. 1996) for many decades even if no trees succeed in reaching the canopy.

Successional trends Oak is distinctly retreating from Suserup Skov, reflecting a long-term successional trend from open wood-pasturage to the present day forest characterized by shady, closed stands and relatively small-scale gap dynamics. Although livestock grazing stopped in the forest ca 200 yr ago, the effects of this change in ecological conditions are still apparent in the system. Beech was the first species to benefit from the retreat of oak (Heilmann-Clausen et al. 2007), but ash, lime and sycamore maple are now distinctly expanding. The latter species was recently introduced into the forest. The status of lime is more uncertain, for although it is known that it occurred in the forest ca 3000 BC (Hannon et al. 2000), it is possible the existing trees are planted and represent a reintroduction. The results of this first reinvestigation of the forest support the assumption made by Emborg et al. (1996) that lime and sycamore maple are steadily consolidating their position and moderately expanding in Suserup Skov. These two species appear to be capable of conquering some of the domain of the other major tree species in the coming generation. They have successfully established in some of the gaps formed after the 1999-storm or due to Dutch elm disease. Thus, recent disturbances seem to have accelerated a shift in species composition of the forest. The relative importance of beech has decreased somewhat in the period primarily due to wind-throw in 1999. A considerable number of the beech trees harvested by the storm will probably be succeeded by sycamore maple or lime. In spite of this, we believe that beech will be able to maintain its present dominant position in the coming generation. Beech establishes and competes efficiently following a step-wise "stop and go" recruitment strategy based on persistent shade tolerance (Emborg 2007). Ash appears likely to maintain its position as the most important gap specialist, although lime and sycamore maple seem capable of exploiting some of the space presently held by the species - either by their ability to establish as advanced regeneration (before gap formation, ready to go when released) or due to their higher shade tolerance. It is characteristic that the relative proportion made up by the ash differs considerably among and within the intensive plots, both in space and over time. But because ash is a gap-specialist (Emborg et al. 2000, Emborg 2007), it is not surprising that the occurrence of the species is rather patchy. The species depends on episodic recruitment, especially after the irregular formation of larger gaps. The 1999 storm in this context represent an opportunity for ash to generate new regeneration patches in newly created gaps, thereby consolidating its present position.

30

While the present disturbance regime, where canopy gaps create semi-open conditions in a patchy and irregular pattern, is benefiting fast growing gap-specialist species, especially ash and sycamore maple, oak appears poorly adapted to establishment in canopy gaps where low grazing levels make way for a very strong competition for light and space (Hofineister et al. 2004). Further, oak seems to have better competitive abilities under more stressful conditions, as imposed e.g. by high grazing levels or marginal water and nutrient supply (e.g. Diekmann 1996). We therefore believe that the species will disappear from the interior of Suserup Skov, unless dramatic changes occur in the disturbance regime. However, established oaks can be very long-lived and persistent: it looks certain that at least some oak trees will remain as a component of the system for many years to come. The expansion of alder along the lake-shore (as studied in part C) conflicts partly with the prediction in by Emborg et al. (1996) that a development from alder- to ashdominance would take place in the former meadows close to the lake. However, it is still too early to evaluate this point in detail as alder is still obviously in a phase of vigorous growth and expansion. Nevertheless, it is noteworthy that ash is expanding in part C. Unfortunately no intensive study plots were placed in part C, and hence no data on small trees was available to give insight in the recruitment patterns among small trees. The long-term effects of succession processes in Suserup Skov are not possible to predict in detail, but it seems that irregular, relatively large-scale disturbances will result in pulses of rapid change followed by periods of adjustment and steady, continuous development. Our qualified guess is that in places sycamore maple and lime will be sustained together with the old inhabitants, beech and ash, whilst oak will continue to decline and even be eliminated if the prevailing conditions continue.

Conclusions The analysis of the results from inventories of Suserup Skov in 1992 and 2002 point to the following conclusions: 1) between 1992 and 2002 Suserup Skov has been impacted by two important disturbances: an extreme storm and the Dutch elm disease. As an ecological system, the forest has proved relatively resistant. Although some changes have occurred in the diameter distribution, the forest ecosystem has not been pushed back into an early successional stage and no decline in the standing volume occurred. 2) The forest is still undergoing changes resulting from the cessation of livestock grazing around 1807 and the subsequent gradual cessation of management. Oak is in retreat from the stands, whilst beech is losing some terrain to ash, lime and sycamore maple aner a period ofextensive dominance. On the wetter ground at the lake-shore, alder is still dominant, but ash is increasing. 3) The ecological distur-

ECOLOGICAL BULl l:TINS 52, 2007

bance caused by the 1999-storm has interacted with and speeded up the ongoing gradual long-term successional changes predicted in 1992. A fair number of large beech trees were blown over in the storm, whilst trees in smaller diameter classes were less affected and have shown vigorous growth. Especially sycamore maple, lime and (to some degree) ash have increased in importance, being capable of filling many of the gaps created where mature beeches have fallen.

Implications for forest management and nature preservation In Denmark, like in many other countries, the forestry ideal has for many years been influenced by the concept of even-aged monoculrures. In this context Suserup Skov is in many respects far from desirable. With an increasing interest in near-narural forestry natural forest systems are however becoming increasingly interesting study objects, as means to inspire forest management (Larsen 1995, Gamborg and Larsen 2(03). Thereby this srudy gives insight into features and mechanisms of forest ecosystems relevant in a management context. The studied ecosystem is much more strucrurally complex than most managed forests of the region. The ecological stability (resistance as well as resilience) of the system seems to be part and parcel of these complex structures (Larsen 1995). Even after the "storm of the century", Suserup Skov remained reasonably well covered by trees and in the gaps created trees were able to naturally regenerate or recover. Even though in total> 1400 m 3 of wood were blown over or killed by the storm (Bigler and Wolf 2007), reflecting a large timber volume compared to a managed forest, the standing volume measured a few years before and a few years after the storm were little different. Our srudy therefore lends support to the view that near-natural forestry, in which the structural complexity of natural forests is mimicked, may not only represent a more resistant silvicultural system in respect to ecological disturbances, but also a more stable productive system, with the potential for higher timber yields in the long run. Apparently, the intimate mixture of tree species and age classes allow different species to fill out different roles and to interact, together forming a coherent, highly productive ecosystem (but see Koricheva et al. (2006) for an alternative view). Considerations like the above suggest that insight into natural forests structures and dynamics represents a valuable source of inspiration for forest management and nature preservation. The future role of sycamore maple will be an interesting example for managers to learn from; the same is the case for the complex interactions between beech and ash. As a straightforward example we can also draw the conclusion, that oak probably is unsuitable for managed structural heterogeneous, mixed deciduous forests, at least on rich soils, unless competitor species are limited, while

ECOLOGICAL BULLETINS 52, 200!

oak recruits are carefully fostered during thinning/regeneration episodes. This represents a serious challenge for nearnatural f()festry. The problem with oak regeneration is also a serious challenge to biodiversity conservarion in unmanaged forests. Oak has a long history as an important tree species in the managed lowlands of NW-Europe, and many threatened species are dependent on veteran oaks to survive (Jonsell et al. 1998, Ranius and Jansson 2000, Dahlberg and Stokland 2004). Even Suserup Skov hosts populations of several endangered insects and fungi associated with old oaks, e.g. the oak polypore Piptoporus quercinus which is threatened allover Europe and protected by law in the UK (Boddy et al. 2004). There is little doubt that this species is at risk of extinction in the long term not only in Suserup Skov, but also in other protected unmanaged forests with old oaks dating back to a period with more open forest conditions. Thus, the conservation ofold oak-dominated, former wood-pastures represents a true dilemma, as many such areas are dedicated to non-intervention and have relatively low grazing/browsing pressure. Part of the solution could be to rely more on forest grazing in some reserves, either by organized livestock grazing in small reserves or by introducing large stocks of wild or semi-wild grazers in large reserves, while in other reserves the vegetation is left to develop with low or variable grazing pressure. Other solutions could be to provide reserves on soil types where oak has a stronger compet:itive potential (e.g. poor, sand or wet, gley soils), in case such stands are available and includes species of conservation concern. Acknowledgements ~ This paper would not have been possible without the help of several persons doing the hard job in the field and the tedious work in the GIS-laboratory. We are therefore highly thankful to ]aris Bigler, Anders Busse Nielsen, Arne Hahn, Morren Christensen, and Martin Kyhn who made the field work and produced the stem position maps. Also we want to thank Ed Mountford and Thomas Vrska for constructive and useful review comments.

References Bigler,]. and Wolf, A. 2007. Structural impact of gale damage on Suserup Skov, a near-natural temperate deCIduous forest in Denmark. - Ecc1. Bull. 52: 69-80. Boddy, L. et al. 2004. Preliminary ecological investigation of four wood-inhabiting fungi ofconservation concern - oak polypore Piptoporus quercinus (=Buglossoporus pultJinus i and the tooth fungi Hericiuml Creolophus spp. - English Nature Research ReportS, Biodiversity Programme, no. 616, Peterborough, UK. Cappelen, J. 2004. Yearly mean temperature for selected meteorological stations in Denmark, the Faroe Islands and Greenland; 1873-2003. ~ Danish Meteorological Inst., Ministry ofTransporr, <www.dmi.dk>. Christensen, M., Emborg,]. and Nielsen A. B. 2007. The forest cycle of Suserup Skov - revisited and revised. - Eco1. Bull.

52: 33-42. Cousens, J. 1974. An introduction to woodland ecology. - Oliver and Boyd, Edinburgh.

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Dahlberg, A. and Stokland,]. N. 2004. Vedlevande arters krav pa substrat - sammanstaIlning och analys av 3 600 arter. - Rapport 7, 2004, Skogssryrelsen, ]onkoping, Sweden, in Swedish. Diekmann, M. 1996. Ecological behaviour of deciduous hardwood trees in boreo-nemoral Sweden in relation to light and soil conditions. - For. Eco1. Manage. 86: 1-14. Emborg,]. 2007. Suppression and release during canopy recruitment in Fagus syivatica and Fraxinus excelsior, a dendro-ecological study of natural growth patterns and competition. -Eco1. Bull. 52: 53-67. Emborg, ]., Christensen, M. and Heilmann-Clausen, J. 1996. The structure of Suserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Landscape Res. 1: 311-

333. Emborg, ]., Christensen, M. and Heilmann-Clausen, J. 2000. The mosaic-cycle of Suserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Ecol. Manage. 126:

173-189. Fodgaard, S. and Enevoldsen, K. 2001. Stormfaldet har fordoblet hugsten. - Skoven 11: 502-505, in Danish. Fritzb0ger, B. and Emborg, J. 1996. Landscape history of the deciduous forest Suserup Skov, Denmark, before 1925. For. Landscape Res. 1: 291-309. Gamborg, C. and Larsen,]. B. 2003. 'Back to nature' - a sustainable future for forestry? - For. Eco!. Manage. 179: 559-571. Hannon, G. E., Bradshaw, R. and Emborg, J. 2000. 6000 years of forest dynamics in Suserup Skov, a semi-natural Danish woodland. - Global EcoL Biogeogr. 9: 101-114. Heilmann-Clausen, J. 2001. A gradient analysis of communities of macrofungi and slime moulds on decaying beech logs. MycoL Res. 105: 575-596. Heilmann-Clausen, J. and Christensen, M. 2003. Fungal diversity on decaying beech logs - implications for sustainable forestry. - Biodiv. Conserv. 12: 953-973. Heilmann-Clausen, J. et al. 2007. The history and present conditions of Suserup Skov - a nemoral, deciduous forest reserve in a cultural landscape. - EcoL Bull. 52: 7-17. Hofmeister, J. et al. 2004. The spread ofash (Fraxinus excelsior) in some European oak forests: an effect of nitrogen deposition or successional change? - For. Eco1. Manage. 203: 35--47. Hough, A. E 1932. Some diameter distributions of forest stands of northwestern Pennsylvania. - J. For. 30: 933-943.

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Husch, B., Beers, T and Kershaw, J. 2003. Forest mensuration. Wiley. Jonsell, M. et al. 1998. Substrate requirements of red-listed saproxylic invertebrates in Sweden. - Biodiv. Conserv. 7: 749~764.

Koricheva, J. et al. 2006. Diversification of tree stands as a means to manage pests and diseases in boreal forests: myth or reality? Can. J. For. Res. 36: 324-336. Larsen, J. B. 1995. Ecological stability of forests and sustainable silviculture. - For. Ecol. Manage. 73: 85-96. Madsen, S. F. 1987. Vedmassefunktioner ved forskellige afl;£gningsgr;£nser og n0jagtighedskrav for nogle vigtige danske skovtr;£arter. - Det Forstlige Fors0gsv;£sen i Danmark: 350: 47~242, yield-tables, in Danish with English summary. Oliver, C. D. and Larson, B. C. 1990. Forest stand dynamics. McGraw-Hill. Peterken, G. F. 1996. Natural woodland. Ecology and conservation in northern temperate regions. - Cambridge Univ. Press. Peterken, G. E and Mountford, E. P. 1998. Long-term change in an unmanaged population of wych elm subjected to Dutch elm disease. - J. Ecol. 86: 205-218. Ranius, T and Jansson, N. 2000. The influence of forest regrowth, original canopy cover and tree size on saproxylic beetles associated with old oaks. - BioI. Conserv. 95: 85-

94. Rohrig, E. 1996. Die Ulmen in Europa: Okologie und epidemische Erkrankung. - Forstarchiv 67: 179-198. Rubin, B. D., Manion, P. D. and Faber-Langendoen, D. 2006. Diameter distributions and structural sustainabiliry in forests. - For. Ecol. Manage. 222: 427--438. Thomsen, R. P. et al. 2005. Overstorey control of understorey species composition in a near-natural temperate broadleaved forest in Denmark. - Plant Eco1. 181: 113-126. Veblen, 1'. T 1992. Regeneration dynamics. -·In: Glenn-Lewin, D. c., Peet, R. K. and Veblen, T 1'. (eds), Plant succession, theory and prediction. Chapman and Hall, pp. 152-187. Vejre, H. and Emborg, J. 1996. Interactions between vegetation and soil in a near-natural remperate deciduous rorest. - For. Landscape Res. 1: 335~347. Westphal, C. et a1. 2006. Is the reverse J-shaped diameter distribution universally applicable in European virgin beech forests? - For. Ecol. Manage. 223: 75-83.

ECOLOGTCAL BULLETTNS 52, 2007

Ecological Bulletins 52: 33-42,2007

The forest cycle of Suserup Skov - revisited and revised Morten Christensen, Jens Emborg and Anders Busse Nielsen

Christensen, M., Emborg,]. and Busse Nielsen, A. 2007. The forest: cycle of Suserup Skov - revisited and revised. - Eco1. Bull. 52: 33-42.

We quantifIed changes in forest structure in Suserup Skov based on two detailed inventories offorest development phases carried out in 1992 and 2002. The inventories were based on a forest cycle model for Suserup Skov, which included five sequential development phases (innovation, aggradation, early biostatic, late biostatic, and degradation). Due to a multitude of different development processes nearly half of the total area changed phase during the 10 yr, which was more than three times the expected. To a large extent, the observed changes between developmental phases followed the basic forest cycle. However, many deviations did occur, of which the most important can be summarised as: 1) the majority of the area in the innovation phase in 2002 originated from phases other than degradation. This was caused by storm damage resulting in aggregate tree fall and the massive spread of Dutch elm disease resulting in sudden die back of patches dominated by elm trees; 2) the majority of the area in the early biostatic phase in 2002 originated from phases other than the aggradation phase, due to crown expansion of trees in the early biostatic phase surrounding canopy gaps; and 3) the majority of the area in the aggradation phase in 2002 was recruited from other phases than the innovation phase, because of a well developed understorey that gradually replaced areas with a degraded canopy. These processes are discussed and presented in a revised model of the overall structural dynamics in Suserup Skov and discussed as a reference for nature-based forest management of deciduous, temperat:e forests.

M. Christensen (moc@fife. ku. dk), J Emborg andA. B. Nielsen, Forest and Landscape Denmark, Univ. ofCopenhagen, Rolighedsvej 23, DK-1958 Frederiksberg C Denmark.

Since the introduction of the forest cycle concept (Watt 1947), researchers have described forest cycles in different ways and at different spatial resolution of units - from a coarse-grained landscape scale mosaic (Bormann and Likens 1979) to stand-scale structural mosaics studied within a few hectares of near-natural forest (Emborg et al. 2000) and managed forests (Grassi et al. 2002). In fact, Watt (1947) developed the concepts of the time-space mosaic (including the upgrading-downgrading cycle of change) from studies of both extremely fine-scale and large-scale ecosystems.

Copyright © ECOLOGICAL BULLETINS, 2007

All authors describe forest cycles as a number ofcontinuous sequential shifts between a series of upgrading and degrading developmental phases. When related to both time and space the forest cycle is referred to as the mosaiccycle (Remmert 1991), and is now widely accepted as a basic description of the natural dynamics of temperate, deciduous forests (Oldeman 1990). Here patches of trees pass through the forest cycle asynchronously from patch to patch, resulting in a shifting mosaic ofdevelopmental phases. A basic forest cycle model for Suserup Skov, Denmark was developed from an inventory in 1992 (Emborg et aI.

33

2000). 511serup Skov is a near-natural, temperate, deciduous forest dominated by beech Fagus sylvatica in mixture with ash Fraxinus excelsior, elm Ulmus giabra, and oak Quercus robur. The forest cycle describes the overall structural dynamics as a fine-grained mosaic structure main-

tained mainly by gap-dynamics where the smallest structural patches are of the size of a single small canopy tree (100 m 2) (Table 1, Fig. 1). The fine-grained mosaic makes 5userup a relevant reference for further development of the "Plenter" system, small-duster and coexisting group sys-

Table 1. Definition and duration of the five developmental phases in Suserup Skov according to Emborg et al. (2000). The phases are defined explicitly using ecological considerations and arguments and distinguished from each other by easily measurable criteria. The innovation phase

Definition: the beginning of the innovation phase is defined as the moment when regeneration is well established in a gap, that is more than ca five vital plants> 20 cm m-2 (less for larger plants). Comment: often ash establishes first due to its pioneer features, with many winddispersed seeds almost every year. Beech establishes within a few years, typically after the first mast year. In addition to the tree vegetation, herbs. grasses, bushes and smaller trees find their place in the open and light conditions. Average duration: based on tree-coring and tree height measurements the average duration of the innovation phase is estimated to 14 yr.

The aggradation phase

Definition: the beginning of the aggradation phase is defined as the moment when the established regeneration has the competing herbal vegetation under control, which is when the regeneration has reached a height of 3 m. Comment: the first part of the phase is often dominated by fast growing ash, but often with scattered small trees like elm, wild cherry and elder. Beech often dominates the lower stratum throughout the phase. Average duration: based on tree-coring and tree height measurements the average duration of the aggradation phase is estimated to 56 yr.

The early biostatic phase

Definition: the early biostatic phase begins when the trees have reached the upper canopy layer, that is has reached a height of 25 m. Comment: most often ash dominates from the beginning, but during the early biostatic phase beech completely takes over the canopy stratum. Average duration: based on tree-coring and tree height measurements the average duration of the early biostatic is estimated to 96 yr.

The late biostatic phase

Definition: the late biostatic phase begins when the trees becomes old, have wounds and scars, and tend to become more vulnerable to biotic and abiotic damages, that is when the trees have reached a DBH of 80 em. Comment: usually beech completely dominates the upper canopy stratum throughout this phase, while scattered undergrowth of elm and beech may occur. Towards the end of the phase the old beeches begin to degenerate, dropping even large branches creating small often short-lasting gaps in the canopy. Average duration: based on tree-coring and tree height measurements the average duration of the late biostatic phase is estimated to 108 yr.

The degradation phase

Definition: the degradation phase begins when degrading trees cause more permanent gaps in the canopy, large enough to initiate regeneration, that is gaps > 100 m2 , which cannot be filled by lateral in-growth ofthe surrounding trees. Comment: the phase can be regarded as an interface between the late biostatic and the innovation phase. It may start suddenly as a result of wind-throw, or it may develop gradually as old trees lose vitality and eventually die. Wellestablished regeneration in a gap defines the end of the degradation phase and the start of a new turn of the forest cycle. Average duration: based on tree-coring and tree height measurements the average duration of the degradation phase is estimated to 10 yr.

One turn of the basic forest cycle in Suserup Skov is, accordingly, estimated to 284 yr on average.

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ECOLOGICAL BULL1:TINS 52,2007

Degradation

Aggradation "'t;i'~,Y'''l!lI.'''h

Innovation

Fig. 1. Model ofthe basic forest cycle, including five developmental phases termed the innovation, the aggradation, the early biostatic, the late biostatic and the degradation phase, in accordance with Oldeman (1990). The definitions of the phases are described in Table 1.

terns which are highly topical as tools for nature-based management of deciduous forests in many NW European countries. These silvicultural systems are widely applied in nature-based forest managed to create irregular and diverse stand structures in conifer and mixed stands in central and eastern Europe (Schlitz 2002). In contrast, experiences with them in management ofdeciduous forests are limited. Forest cycle models - like the one developed for Suserup Skov - have in many cases supported the understanding of the basic dynamics in natural forests from tree generation to tree generation (Standovar and Kenderes 20(3). However, several authors have argued that their simplification can lead to misinterpretation because of the exclusion of complexity of developmental processes (Franklin et al. 2002, Standovar and Kenderes 20(3). Muth and Bazzaz (2002) describe the importance of crown expansion at gap edges for the forest dynamics and Pontailler et al. (1997) and McCarthy et al. (2001) describe the complexity of regeneration and the process of understorey trees gradually taking over the canopy layer. Similar processes have been observed in Suserup Skov. Bigler and Wolf (2007) studied the impact of the 1999 hurricane in Suserup Skov, and documented how the wind created numerous really small gaps (l0-100 m 2). A dendro-ecological study Emborg (2007) documented how beech in Suserup Skov can utilise such small temporary canopy gaps to approach the canopy, step by step, as part of a "stop and go" strategy. Finally, in a detailed study of the forest structure Nielsen and Hahn (2007) document welldeveloped understorey and concludes, that the light patterns and dynamics on the forest floor are extremely com-

ECOLOGICAL BULLETINS 52, 2007

plex and to a large extent determined by understorey characteristics and the canopy dynamics in the surroundings of any particular patch. These studies all point to a rich and detailed variation in the processes, which appears to have substantial impact on Suserup Skov. However, our understanding of their impact on the overall structural dynamics in terms of changes between developmental phases in Suserup Skov remains fragmented. A re-inventOlY in 2002 made it possible to quantify- the different development processes in terms of changes between developmental phases on the base of 10 yr of observation since the first inventory in 1992. This allowed for a critical evaluation and refinement of the basic forest cycle. Correspondingly, the objectives of this paper are to 1) quantifY changes in development phases from 1992 to 2002 with reference to the basic forest cycle model; 2) evaluate and further develop the basic forest cycle model; and 3) discuss the implications of the results in the context of nature-based forest management.

Methods and materials Study site Suserup Skov is a 19.2 ha forest reserve located in the central part of Zealand (Sjxlland) in eastern Denmark. The forest is a near-natural, temperate, deciduous forest dominated by beech in mixture with ash, elm, and oak. The soil is glacial sediments where both clay, loamy and sandy till occur (Vejre and Emborg 1996). The study was carried out in "part A" of Suserup Skov (I0.60 ha, see Emborg et al. 1996), for which pollen analysis suggests a history of forest cover during the last 6000 yr (Hannon et al. 2000). Management has been minimal since 1854 and since 1961 Suserup Skov has been a strict non-intervention reserve (Emborg and Fritzb0ger 1996, Heilmann-Clausen et al. 2(07).

Climate and disturbances from 1992 to 2002 Climatically, the 10-yr period from 1992 to 2002 was not substantially different trom previous decades. Average annual temperatures were 8.3°C, which is slightly higher than the average from 1874 to 2003 of7.6°C, and varied from 6.8°C (1996) to 9.2°C (2002). The average annual precipitation was 741 mm and varied from 505 mm (1996) to 905 mm (1999), compared to an average of674 mm hom 1874 to 2003 (Cappelen 2004). No exceptional droughts or extremely cold winters occurred in the period. On 3 December 1999 the southern part of Denmark was hit by a severe storm (mid-latitude cyclone). The storm was accompained by heavy rain after a long period with low precipitation, causing many trees in Suserup Skov to

35

uproot. Scattered single trees were damaged throughout the forest, while some areas experienced heavier damage, resulting in a range of small to intermediate sized gaps (for a detailed description of the storm and analyses of the impact on Suserup Skov, see Bigler and Wolf 2007). Another important disturbance event in the 10-yr period was the arrival and subsequent spread of Dutch elm disease caused by Ophiostoma ulmi sensu lato beginning in 1995. Elm mortality continued until 2002, and created gaps of varying size where patches of elm formed the uppermost canopy layer.

2. The expected turn over of phases during the 10-yr period was calculated using the equation: (2)

where Er is the expected turn over, Y is the studied period (10 yr), i is the duration of the phase and E <),)2 is the aggregate area of the phase in 1992. j

Results Mapping of the developmental phases The development phases were mapped in winter 1992/ 1993 and autumn 2002. The mapping was done on the basis of "stem-position maps" (1:500) including all trees >29 cm DBH (Emborg et al. 1996, Emborg and Heilmann-Clausen 2007). The canopy defined the phase of a given patch in the forest; i.e. regeneration on the forest floor was only defined as an innovation phase patch when there was a gap above, and trees between 3 and 25 m height were only defined as a patch of aggradation phase if they formed the canopy layer of that patch (Emborg et al. 2000). This way spatial overlap between neighbouring patches was avoided. The spatial resolution corresponded to a minimum patch size of 100 m 2 . Clinometers, callipers, and measure lines were used to ensure a strict mapping of patches according to the phase definitions (Table 1). Each patch of the mosaic was marked on field charts.

Shifting mosaic and aggregate area of the phases The maps of the shifting mosaics from 1992 and 2002 are shown in Fig. 2. Despite the recent disturbances caused by the severe 1999 storm and the attack of Dutch elm disease, the aggregate area of the individual phases remained surprisingly stable and close to the expected aggregate areas (Fig. 3). Moreover, the average patch size of each phase hardly changed (Table 2). The number of patches in the innovation phase, however, increased considerably, leading to an increment in the aggregate area of the innovation phase from 0.24 ha in 1992 to 0.80 ha in 2002, which was a larger increment than expected (according to eq. 1) (Fig. 3). Also, the aggregate area of the continuing upgrading phases of aggradation and early biostatic was larger than expected. In contrast, the area of the degrading phases of late biostatic and degradation was less than expected, which was a direct effect of the 1999 storm (Fig. 3).

Data analysis All development phases in the 1992 and 2002 inventories were digitized with AutoCad and incorporated into ArcGIS. Spatial Analyst and Geo Processing tools in ArcGIS were used for exact (1 m 2 ) calculation of changes in the areas of development phases between 1992 and 2002. However, the presentation of the results has been rounded off to a precision of 100 m 2 , to provide a framework for analysing and discussing the observed changes. We performed the following two sets of calculations for the expected changes, presuming a hypothetical dynamic phasic equilibrium (Watt 1947), also called the shifting-mosaic steady state (Bormann and Likens 1979) in which the aggregate area of a phase is directly proportional to the duration of that phase: 1. The expected aggregate area ofeach of the five phases was calculated, using the equation: Ea = (ill) x A

(1)

where, Ea is the expected area, i is the duration of the phase, I is the duration of the full forest cycle (284 yr), and A the area of the whole plot (10.60 ha).

36

Turn over in phases 1992-2002 A closer look into the dynamics of the individual patches

from 1992 to 2002 uncovered additional information about several important processes during the 10-yr period. For all phases, except degradation, the observed turn over in the 10-yr period was larger than expected. In total, 4.96 ha changed phase during the period corresponding to 47% of the tenal plot (10.60 ha), which was nearly three fold the expected turn over (Table 3). The high turn over in phases observed over the 10-yr period was caused by a multitude of development series which are illustrated in Fig. 4. To a large extent these mechanisms followed the basic model of the forest cycle (Emborg et aI. 2000). The most important series can be summarised as follows: 1) a major part (0.12 ha of 0.24 ha) of the innovation phase in 1992 changed into the aggradation phase in 2002. 2) A major part (0.97 ha of 2.29 ha) of the aggradation phase in 1992 changed into the early biostatic phase in 2002.3) A major part (0.16 ha of 0.28 ha) of the degradation phase in 2002 originated from areas of the late biostatic phase in 1992.

ECOLOGICAL BULLETINS 52, 2007

1992

2002

D

Innovation

Early Biostatic

Aggradation

Late Biostatic

•

Degradation

Fig. 2. Maps of the developmental phases in 1992 and 2002.

However, deviations from the basic forest cycle (Fig. 1) occurred in all the developmental phases from 1992 to 2002, of which the most important can be summarised as follows: 1) the majority of the area that changed into the innovation phase originated from phases (0.74 ha) other than the degradation phase (0.05 ha). 2) Nearly half of the area (0.84 ha) that changed into the early biostatic phase originated from phases other than the aggradation phase (0.97 ha). 3) The majority ofthe area that changed into the aggradation phase originated from phases (1.35 ha) other than the innovation phase (0.12 ha).

ECOLOGICAL BULLETINS 52,2007

Discussion Our results indicate that the development of the forest structure from 1992 to 2002 does not follow the basic forest cycle model strictly from patch to patch over time. Many different processes and changes between developmental phases that deviate from the basic model occurred, which may also serve to counterbalance each other - as illustrated by the arrows pointing back and forth between phases in Fig. 4. These deviations from the basic forest cycle model resulted from either: 1) the 1999 storm and the

37

:::1i 4_0

I

3.5 ~I] 3.0 .-

2.51

2.0! 1.51'

1.0

0.5 1

a.af

.1 Innovation

I:]

Aggradation

_ _I . Early biostatic

Late biostatic Degradation

Fig. 3. Aggregate area of the different phases observed in 1992 (black) and 2002 (grey) and expected aggregate area of the phases in 2002 (Ea> (white) according to eq. 1.

arrival of Dutch elm disea,<;e in 1995, 2) crown expansion of canopy trees in the early biostatic phase, or 3) a well developed understorey that gradually replaced the canopy. In the following each of these processes is discussed with reference to the basic forest cycle.

1) Creation of the innovation phase The aggregate area of the innovation phase increased considerably from 0.24 ha (2%) in 1992 to 0.8 ha in 2002 (8%). This is directly related to the 1999 storm and the spread of Dutch elm disease. The proportion of gaps in 2002, however, corresponds to reports from other wind disturbed NW' European beech dominated forest reserves, e.g. the Fontainebleau reserve (9-11 %) in France (Koop and Hilgen 1987). In the 10-yr period the 1999 storm was the most important initiator of gaps> 100 m 2 • The extremely strong winds during the storm (Bigler and Wolf2007) caused direct mortality and damage to both healthy canopy trees as well as senescent ones. These processes explain why approximately half the area in the innovation phase in 2002

originated from patches that were in the early biostatic or late biostatic in 1992 (Fig. 4). Bigler and Wolf (2007) found that the 1999 hurricane also created a large number of gaps (> 20% of the area of part A), ofwhich many were small gaps (10-100 m 2). The present study wa,<; too coarsegrained (only patches > 100 m 2 were monitored) to capture the effect of the small gaps on the overall forest dynamics. Crown expansion (see below) probably explains a substantial part of the decrease in gap area after the storm; 20% in 1999 (according to Bigler and Wolf 2007) vs 8% in 2002 (according to the present study). However, it seems clear from other studies (Emborg 2007; Nielsen and Hahn 2007) that small, temporary canopy openings have substantial influence on the development, growth and vitality ofsub-canopy trees. Even very small canopy gaps are reported to initiate substantial growth responses in understorey trees (Canham 1985, 1990). The spread of Dutch elm disease was the second major factor that initiated patches of the innovation phase in the 10-yr period. Dutch elm disease spread rapidly in Suserup Skov after its arrival in 1995, causing mortality ofnearly all elms> 10 em DBH by 2002. Many of the dead trees formed patches in the aggradation (and early biostatic phase). Most often, such areas changed into the innovation phase, which explains why nearly half of the area (0.35 ha) in the innovation phase in 2002 originated from patches of the aggradation phase in 1992 (Fig. 4). Similar mortality patterns of elm in unmanaged forests have also been observed in Austria (Mayer and Reimoser 1978), UK (Peterken and Mountford 1998) and Germany (Huppe and Rohrig 1996). The attack of Dutch elm disease and its impacts can be regarded as a peculiar example of the rich variety of disturbances that are involved in shaping the dynamics of temperate deciduous forests.

2) Crown expansion In forest ecosystems, light is a critical resource (Emborg 1998, Grassi et al. 2002), which is particularly patchy in nature (Nielsen and Hahn 2007); so that trees actively dis-

Table 2. Aggregate area, number of patches and average patch size observed in 1992 and 2002 according to the five developmental phases. 1992

Phase Innovation Aggradation Early biostatic Late biostatic Degradation Total

38

2002

Aggregate area (ha)

Number of patches

Average size (m 2 )

Aggregate area (ha)

Number of patches

Average size (m 2 )

0.24 2.29 3.97 3.49 0.61 10.60

5 27 27 52 16 127

476 848 1469 671 384 834

0.80 2.28 0.75 2.48 0.28 10.60

15 21 32 49 14 131

533 1088 1484 506 203 809

ECOLOGICAL BULLETINS 52,2007

Table 3. Expected and observed turn-over of phases from 1992 to 2002. _ _ _ ~~m

Phase Innovation Aggradation Early biostatic Late biostatic Degradation Total

Duration! yr

Area (ha) 1992

14 56 96 108 10 284

0.24 2.29 3.97 3.49 0.61 10.60

Expected turnover (E? 0/0 ha 0.17 0.41 0.40 0.31 0.61 1.89

71 18 10

Observed turnover)
9

1.63

100 17

0.59 4.96

96 65 26 47 97 47

---~---

Duration of phases is according to Emborg et al. (2000). See also Table "I. According to eq. 2. )) According to Fig. 4.

11

21

place their crowns towards high-light patches, such as canopy gaps (Muth and Bazzaz 2002). In Suserup Skov, we observed that patches surrounded by the early biostatic phase were most vulnerable to crown expansion processes. Prequently, small patches of e.g. innovation, aggradation and degradation simply dosed and larger patches decreased considerably in size due to crown expansion of surrounding canopy trees in the early biostatic phase. Such canopy expansions explain why one quarter of the area in the degradation phase (0.15 ha of 0.61 ha) and innovation phase (0.07 ha of 0.24 ha) changed into the early biostatic phase in 2002 (Fig. 4). There was also a 0.62 ha change from the late biostatic phase in 1992 to the early biostatic phase in 2002 (Fig. 4). This is likely the result of trees in the early biostatic phase that expanded their crowns into gaps created by the 1999-

storm related damage and mortality of trees in the late biostatic phase. Similar processes of beech tree crown expansion into canopy gaps have been reported from unmanaged temperate beech forests in central Europe (Koop and Hilgen 1987, Knapp and Jeschke 1991, Tabuka and Meyer 1999) and experimental studies on canopy displacement at forest gap edges in North American mixed hardwoods with Fagus grandifolia (Muth and Bazzaz 2002). The fact that arrows points to the early biostatic phase from about all other phases, could be taken as an indication of the "expansive vitality" ofthis phase and the derived ability to expand borders at the expense of other phases. Far fewer arrows points to the late biostatic phase which might indicate the abating ability of older uees to expand their canopy.

Early biostatic

Fig. 4. Refined forest cycle model illu~ strating area ofchanges and non-changes (in ha) 1992-2002. The numbers written next to the illustrations of the phases are areas which not changed. The thickness of the arrows indicate the importance of different processes.

ECOLOGICAL HULLEfINS 52. 2007

(0.01

39

It is not surprising that vital trees in the early biostatic phase expand their crowns toward canopy openings, thereby causing a turn-over in phases. What is surprising is the amount of shifts in phases that, according to our interpretation, can only be explained by this process. Consequently, lateral crown expansion does not only have implications for individual trees - it is also an important process for the overall structural dynamics because it initiates substantial turn-over in terms of phases. However, processes related to lateral crown expansion are seldom revealed as players in the overall structural dynamics ofnatural forests because of a coarser scale in the mapping of developmental phases. From this perspective further research into crown expansion dynamics and speed of different tree species in relation to development phases and processes could improve our understanding of the overall structural dynamics in deciduous natural forests.

3) Understorey trees taking over the canopy Understorey characteristics are often overlooked in studies of the structural dynamics in unmanaged forests (McCarthy et al. 2001, Franklin et al. 2002) and beech is often described as a heavy shading species which does not allow the understorey to develop (Knapp and Jeschke 1991, Jenssen and Hofmann 1996). However, our results document well-developed understorey in Suserup Skov and indicate that the release of understorey trees following canopy breakdown is a main driving process, enabling most patches to bypass the innovation phase. When interpreting our results, the majority of overstorey-understorey transitions appear to be from beech to beech in wind-throw patches with understorey trees (often referred to as advanced regeneration). The change from the early biostatic to the aggradation phase is a direct result of wind-throw in patches with a well-developed understorey. Since beech trees account for more than half of the total number of trees in the early biostatic phase damaged in the 1999-storm (Bigler and Wolf 2007) much of the understorey developed as advanced regeneration beneath a beech canopy. Similarly, the change from the late biostatic to aggradation phase is also a result of wind-throw. Moreover, since few ash grow to a DBH> 80 cm in Suserup Skov (Emborg et al. 2000), and because very few oaks were damaged in the 1999 storm (Bigler and Wolf 2007), trees that developed beneath a beech canopy appears to account for the majority of this change as well. This interpretation is supported by Emborg (2007) who shows that beech in Suserup Skov is able ro hold a position in the understorey for many years in the deep shade of canopy beech trees, and still remain the capacity to respond to release. Well developed understorey in wind-thrown patches explains why more than halfofthe area (1.35 of2.28 ha) in the aggradation phase in 2002 was either in the early bio-

40

static phase (0.36 ha), late biostatic phase (0.65 ha), or degradation phase (0.34 ha) in 1992 (Fig. 4). Finally, well developed undersrorey explains why nearly all the degradation phase areas bypassed the innovation phase and developed directly into the aggradation phase during the 10-yr period (Fig. 4). The character of such well-developed UIldersrorey in Suserup Skov has been exemplified on prome diagrams by Nielsen and Hahn (2007).

Concluding remarks The quantification of different developmental processes in Suserup Skov using a small minimum patch size (100 m 2 ) exemplifies the "unpredictable" nature of forest with natural dynamics. Many and complex developmental processes and an intensive dynamic were identified. The irony is that the discovered processes apparently to a large extent counterbalance each other with the result of only small changes in the aggregate area of the different developmental phases over the 1O-yr observation period. This could be used as an argument for applying a more coarse-grained scale, which is the traditional approach taken in many well-known examples of forest cycles like e.g. Leibundgut (1959) and Zukrigl et al. (1963). However, the high spatial resolution applied in the two here presented inventories of Suserup Skov (1992 and 2002) enables an interesting dive under the surface (Fig. 4) and the identification and quantification of many important processes which were only ascribed a secondary role in the hitherto understanding of the overall structural dynamics in forest (Fig. 1). During the 10-yr observation period, the turn over in phases as well as the number of processes deviating from the basic forest cycle model was surprisingly high. The effects of the 1999-storm and the arrival of Dutch elm disease in 1995 explain some of these deviations. However, the majority of deviations seem to occur because the basic forest cycle model does not incorporate the process of lateral crown expansion or the process ofcanopy replacement by understorey trees. The process related to well developed understorey manifests in patches by-passing the degrading part of the forest cycle and also the innovation phase. .As such understorey characteristics played an unexpected large role in the overall structural dynamics in Suserup Skov. From this perspective further research into these dynamics would appear to be a valuable supplement to the current focus on regeneration processes related to gap-dynamics in naturebased management of beech dominated forests in Europe. Also lateral crown expansion by canopy trees surrounding gaps or patches with up-growth played a larger role in the spatial and temporal structure and dynamics than expected. Especially trees in the early biostatic phase closed small patches and reduced larger ones dramatically by lateral crown expansion. Consequently, the results indicate that improved understanding of the processes related to

ECOLOGICAL BULLETINS 52, 2007

lateral crown expansion of individual trees and borderline dynamics between patches of trees is crucial for the further development of the "Plenter" system, small-duster and coexisting group systems that all aims at fine grained mosaic structures and structural dynamics with parallels to those observed in Suserup Skov. These selective/group systems are highly topical in the ongoing adaptation to more nature-based management of deciduous temperate forests in many NW European countries. Acknowledgements ~.~ Thanks to Jaris Bigler, Jacob HeilmannClausen for assistance in field work,]. Bo Larsen, Katrine Hahn, Merete Morsing and the reviewers Tom Nagel and Tibor Standovar for valuable comments to the manuscript. We are grateful to Som Akademi for permitting the research in Suserup Skov. The project was supported by the NatMan project (EU 5th framework programme grant QLK5-01349) and the SpyNatForce project funded by the Danish Research Council.

References Bigler, J. and Wolf, A. 2007. Structural impact ofgale damage on Suserup Skew, a near-natural temperate deciduous forest in Denmark. Ecol. Bull. 52: 69-80. Bormann, F. H. and Likens, G. E. 1979. Catastrophic disturbance and the steady state in northern hardwood forests. Am. Sci. 67: 660--669. Canham, C. D. 1985. Suppression and release during canopy recruitment in Acer srlccharum. - Bull. Torrey Bot. Club 112: 134-145. Canham, C. D. 1990. Suppression and release during canopy recruitment in Fagus grandiftlia. - Bull. Torrey Bot. Club 117: 1-7. Cappelen, ]. 2004. Yearly temperature, precipitation, hours of bright sunshine and cloud cover for Denmark as a whole; 18732003. Danish Meterological 1nst. Technical Repon 04-06, Copenhagen. Emborg,]. 1998. Understorey light conditions and regeneration with respect to the structural dynamics in a near-natural temperate deciduous forest in Denmark. - For. Ecol. Manage. 106: 83-95. Emborg, J. 2007. Suppression and release during canopy recruitment in Fagus sylvatica and Fraxinus excelsior, a dendro-ecological srudy of growth patterns and competition. - Ecol. Bull. 52: 53-67. Emborg, ]. and Fritzb0ger, B. 1996. Landscape history of the deciduous forest, Suserup Skov, Denmark, before 1925. For. Landscape Res. 1: 291-309. Emborg, J. and Heilmann-Clausen, ]. 2007. The structure of Suserup Skov, 2002. The first re-measurement ofa long-term permanent plot study of forest dynamics started in 1992. Ecol. Bull. 52: 19-32. Emborg, J., Christensen, M. and Heilmann-Clausen, J. 1996. The structure ofSuserup Skov, a near-natural temperate deciduous rorest in Denmark. - For. Landscape Res. 1: 311-333. Emborg, J., Christensen, M. and Heilmann-Clausen, J. 2000. The structural dynamics of Suserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Ecol. Manage. 126: 173~189.

E'CULOCICAL BULLETINS 52, 2007

Franklin, J. F. et al. 2002. Disturbances and structural development of natural forest ecosystems with silvicultural implications, using Douglas-fir forests as an example. - For. Eco!. Manage. 155: 399-423. Grassi, G. et al. 2002. The structural dynamics of managed uneven-aged conifer stands in the Italian ea.<;tern Alps. - For. Eca!' Manage. 185: 225-237. Hannon, G. E., Bradshaw, R. and Emborg, J. 2000. 6000 years of forest dynamics in Suserup Skov, a semi-natural Danish woodland. - Global EcoL Biogeogr. 9: 101-114. Heilmann-Clausen,]. et al2007. The history and present conditions ofSuserup Skov - a nemoral deciduous forest reserve in a cultural landscape. - Eco1. Bull. 52: 7-17. Huppe, B. and Rohrig, E. 1996. Ein Mischbestand mit Bergulmen im Kommunal-Forstamt Haina (Hessen). - Forstarchiv. 67: 207-211. Jenssen, M. and Hofmann, G. 1996. Der natlirliche Entwicklungszyklus des baltischen Perlgras-Buchenwaldes (MelicoFagetum). - Forstwirtschaft und Landschaftsokologie 30: 114-124. Knapp, H. D. and Jeschke, L. 1991. Naturwaldreservate und Naturwaldforschung in den ostdeutchen Bundeslandern. Schriftenreihe fur Vegetationskunde, Bundesforschungsanstalt fUr Naturschutz und Landshaftsokologie 21: 21-54. Koop, H. and Hilgen, P. 1987. Forest dynamics and regeneration mosaic shifts in unexploited beech (fagus sylvatica) stands at Fontainbleau (France). - For. Eco1. Manage. 20: 135-150. Leibundgut, H. 1959. Uber Zweck und Methodik del' Strukturund Zuwachsanalyse von Urwaldern. Schweizerische Zeitschrift fur Forstwesen 110: 11-124. Mayer, V. H. and Reimoser, F. 1978. Die Auswirkungen des UImensterbens im Buchen-Naturwaldreservat Dobra (Niederosterreichisches Waldviertel). - Forstwiss. Centralblatt 97: 314-321. McCarthy, B. c., Smaal, C. J. and Rubino, D. L. 2001. Composition, structure and dynamics of Dysart woods, an oldgrowth mixed mesophytic forest ofsoutheastern Ohio. - For. Eca1. Manage. 140: 193-213. Muth, C. C. and Bazzaz, F. A. 2002. Tree canopy displacement at forest gap edges. - Can. J. For. Res. 32: 247~254. Nielsen, A. B. and Hahn, K. 2007. What is beneath the canopy? Structural complexity and understorey light intensity in Suserup Skov, eastern Denmark. - Eco1. Bull. 52: 43-52. Oldeman, R. A. A. 1990. Forests: elements of silvalogy. - Springer. Peterken, G. F. and Mountford, E. P. 1998. Long-term change in an unmanaged population of wych elm subjected to Dutch elm disease. - J. Eco1. 86: 205-218. Pontailler, J.-Y., Faille, A. and Lemee, G. 1997. Storm drive successional dynamics in natural forests: a case study in Fontainbleau forest (France). - For. Ecol. Manage. 98: 1-15. Remmert, H. 1991. The mosaic-cycle concept ofecosystems - an overview. - In: Remmert, H. (ed.) , The mosaic-cycle concept of ecosystems. EcoL Stud. 85: 1-21. SchUtz, J. P. 2002. Silvicultural tools to develop irregular and diverse forest structures. - Forestry 75: 329-337. Standovar, T. and Kenderes, K. 2003. A review on natural stand dynamics in beechwoods of east central Europe. - AppL £col. Environ. Res. 1: 19-46. Tabaku, V. and Meyer, P. 1999. LUckenmunster albanischer und mitteleuropaischer Buchenwalder unterschiedlicher Nutzungsintensitat. - Forsarchiv 70: 87-97.

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Vejre, H. and Emborg, J. 1996. Interactions between vegetation and soil in a near-natural temperate deciduous forest. - For. Landscape Res. 1: 335~347. Watt, A. S. 1947. Pattern and process in the plant community.J. Ecol. 35: 1~17.

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Zukrigl, K., Eckhardt, G. and Nather, J. 1963. Standonskundliche und waldbauliche Untersuchungen in Urwaldresten def niederosterreichischen Kalkalpen. - Mitteilungen Forst Bundesversuchanstalt Wien 62.

ECOLOGICAL BULLETINS 52. 2007

Ecological Bulletins 52: 43-52,2007

What is beneath the canopy? Structural complexity and understorey light intensity in Suserup Skov, eastern Denmark Anders Busse Nielsen and Katrine Hahn

Nielsen, A. B. and Hahn, K. 2007. What is beneath the canopy? Structural complexity and understorey light intensity in Suserup Skov, eastern Denmark. - Ecol. Bull. 52: 43-

52. A detailed understanding of the structural complexity and its effects on understorey light intensity in natural forests are important references for the further development of nature-based forest management. Based on a full inventory of a I-ha plot in Suserup Skov, a near-natural temperate deciduous forest in Denmark, this research describes the structural complexity in three dimensions and identify structural factors, which determine the relative light intensity in the understorey, using profile- and crown-projection diagrams related to relative light intensity (RLI) measured one metre above the ground. The horizontal pattern showed a fine-grained mosaic of trees in different developmental phases resulting in a variable canopy height ranging from 1 to 40 m. Beneath the canopy one to three understorey layers were common. The main reasons for this well developed stratitlcation were irregularity in canopy cover among small neighbouring structural units and the presence offour co-occurring tree species with different reproductive strategies and life cycles. Relating the spatial structure to the understorey light intensity, we found the continuous cover of dense growing understorey layers across neighbouring structural units to be the main determinant for RLI.

A. B. Nielsen ([email protected]) and K Hahn, Forest and Landscape Denmark, Univ. of Copenhagen, Rolighedsvej 23, DK-1958 Frederiksberg Denmark.

c:

Structure of vegetation and its effects on the understorey light intensity in natUral forests are complex and notoriously difficult to explain due to varying canopy height, understorey tree layers, and advance regeneration (Brown and Parker 1994, Franklin et aL 2002, Grassi et aL 2003). In spite of this, understorey data is in many cases overlooked in studies of unmanaged forests (McCarthy et aL 2001, Franklin et aL 2002). Moreover, understorey light intensity is often described as having a simple correlation with the developmental phases of the canopy trees (Emborg 1998, Grassi et al. 2003). Such simplifications can be

CopyrighT @ ECOLOGICAL BULLETINS, 2007

regarded as one of the reasons why the spatial structure of natural forest ecosystems is neither easy to understand nor to communicate, as indicated by Franklin et al. (2002). From this perspective, a more detailed understanding of the structural complexity and the relationship between structure and understorey light intensity in natural forests is an important reference for further development of nature-based forest management. One important method applied for detailed studies of vegetation structure is profile and crown-projection diagrams. A profile diagram is a depiction of a vertical section

43

through the forest, while the crown projection diagram is the corresponding map. This method has gained interest during the last century, especially where mixed-forest management has been practiced, indicating that the more complex the structures are, the greater the needs for integrative visual tools (Gustavsson 1986, 1988, Koop 1989, Nielsen and Nielsen 2005). The earliest use of crown projection diagrams date back to the late 1870s where Blomqvist (1879) made drawings ofboreal forests (Sarvas 1958). This was followed by profile diagrams ofEnglish forests by Watt (1925) and soon after by many other forest ecologists in central and eastern Europe and the tropics (Gustavsson 1986, Koop 1989). Since then, scientist and teachers in t()festry, forest ecology and landscape architecture have used profile diagrams (sometimes including crown projections) as descriptive tools illustrating and documenting forest structures (Baker and Wilson 2000). In contrast to the widespread use of profile- and crown projection diagrams as descriptive tools, their use for analyses have, to our knowledge, mostly been limited to identitlcation of stratification in forest canopies (Baker and Wilson 2000). However, when applied as tools for analysis, such visual tools provide information about many other facets of the structural conditions (Gustavsson 1986). In this research, profile- and crown projection diagrams are combined with quantitative measurements in order to describe the vegetation structure in a 1-ha plot in Suserup Skov, and how the structural complexity affects the understorey light intensity. The research questions were: 1) How does the forest structure influence the relative light intensity in the understorey? 2) Which structural factors determine the understorey light intensity?

Materials and methods The study was carried out in a 120 X 80 m (0.96 ha) plot in the least disturbed NW part (10.6 ha) of Suserup Skov (19.2 ha) (Fritzb0ger and Emborg 1996, HeilmannClausen et al. 2007). The tree vegetation is dominated by beech Fagus syltJatica in mixture with ash Fraxinus excelsior, elm Ulmus glabra, and pedunculate oak Quercus robur. The ground cover consists predominantly of perennial species adapted to utilise the light in early spring before leafing (Anemone nemorosa, Mercurialis perennis, Corydalis bulbosa). Closed canopy characterises most of the plot, with clear signs ofan old, now overgrown gap in the SW parr of the plot and a young storm-induced, E-W oriented gap (1999) ca 40 m from the N edge of the plot. The plot is situated on an elevated plateau cur through by a shallow NW-SE depression with a 6 m elevation drop. Two small footpaths cross the plot. The plot was selected on the basis of its representative forest structure and the presence of a small bog in the NE quarter (500 m 2) for pollen studies (Hannon et a1. 2000). A local grid system with permanent corner posts was laid out, dividing the plot into eight

44

transects of 120 X 10 m (transects no. 1-8). Each transect was again split into six blocks of20 X 10m to ease the field mapping of crown projections and drawing of profile diagrams (Fig. 1). All trees were recorded according to the methodology of Koop (1989). Trees> 3 m height were given a unique number, whereas seedlings < 3 m height were recorded either as number m-2 (areas with high densities) or as individuals (areas with scattered seedlings). Horizontal characters (tree positions, crown projections, footpaths, lying dead wood) were positioned and drawn on field charts at scale 1:200 for the whole plot. Crown projections of individual trees were made on transparent sheet-overlay, according to the methodology of Koop (1989). All vertical characters (top height, height at the greatest width of the crown periphery, height of the crown base, height of the first living fork, standing dead wood, and dead branches) were recorded according to Koop (1989) in tables on site. Hand drawn proflle diagrams (viewed from west) were made for transects 2 and 4, each 120 X 10 m (1200 m 2 ). Tree positions, crown periphery and vertical characters were used to support the profile drawings on site. Mapping crown projection was carried OlIt in early spring 2002 before leafing and profile diagrams were drawn in the leafing period in order to maximize the precision of height-measurements, distinguish dead and living branches and drawing of crown architecture. In order to keep the profile drawings readable the method of nested transects (Koop 1989) was used for delimitation of the trees to be included in the profile. Trees taller than 10m were drawn for the full 10 m transect width (1200 m 2), trees 2-10 m tall were drawn for a 5 m wide strip (600 m 2) and trees < 2 m height were drawn over a 2 m wide area (240 m 2 ) around the centre line. By use of transparent overlay, all crown-projec[ions and profile diagrams made in the field (paper size A4) were transferred to one sheet, which was copied to aquarelle pa-

Fig. 1. The studied plot with elevation COntours, footpaths, bog and the division of the plot into 8 transects of 120 X 10m, each subdivided into 6 blocks of 20 x 10m. Transects 2 and 4 are drawn in the profile diagrams (Fig. 3 and 4).

ECOLOGICAL BULLETINS 52, 2007

per and coloured. Finally the drawings were scanned and adapted into image software (Photoshop 7.0). Relative light intensity (RLI), calculated as percent of light intensity measured in a nearby open field, was determined along the centre lines of transect 2 and 4 with two m intervals by use ofmeasurements ofleafarea index (LAl) with aLi-Cor LAl 2000 instrument. Two simultaneous measurements were taken with cross-calibrated sensors. One sensor was placed in a nearby open field and one sensor was used for measurements under the forest canopy (1 m above ground). The measures ofLAI were converted to RLI (photosynthetic photon flux densities, PPFD, /lillol m- 2 S-I) in the 400-700 nm wavelength, using an equation based on correlation tests ofLAI and PPFD from measurements in similar beech dominated forests in eastern Denmark (Madsen and Larsen 1997). The conversion to RLI was done in order to ease the intuitive understanding of the inverse relationship between canopy cover and light intensity. RLI was first measured in late August 2002 and again in early July 2004. In the analyses, data from 2004 was used, as this dataset was more complete. There were no major differences in the spatial patterns of the RLI values between the two years. Data were described and analysed both quantitatively and qualitatively with the two approaches supporting each other. For the analysis ofthe small to very small-scale structural patches in the plot, where even single-tree patches were recorded, we assigned individual trees to specific developmental phases (see also Grassi et al. 2003), well aware that that developmental phases are typically assigned to groups (cohorts) of trees. The developmental phases for the individual trees were defined in accordance with Emborg et al. (2000), supplemented with a division of the aggradation phase into an early and a late aggradation phase (Table 1). First, the developmental phases were described quantitatively according to tree species, tree density, and relative share of canopy cover. Weighing paper cuttings of all phase projections and thereafter relating the weight of each phase to the weight of the full plot paper cut, the area of each phase was calculated. Secondly, the spatial complexity was analysed qualitatively by use of the profile- and crown projection diagrams. The profile dia-

grams from transects 2 and 4 were analysed qualitatively for structural attributes and divided into sub-zones and zones based on two approaches: First, the transects were divided into sub-zones based on the developmental phase of the canopy trees. Second, these sub-zones were grouped into larger zones reflecting both canopy and understorey characteristics. The idea behind these two approaches was to test the effect of densely growing or shady understorey trees on the light intensity. The tests were performed by statistical analyses of how much RLI varied within and between the different zones for the two principles (SAS PROCGLM).

Results The studied one-hectare plot contained 778 measured individual trees plus an estimated number of 50 000 ash and beech seedlings established in gaps and under the surrounding canopy (Table 2). Beech was the only species well represented in all developmental phases, whereas ash, elm, oak, and shrubs; elder Sambucus nigra, rowan Sorbus aucuparia, hazel Corylus avellana, and spindle Euonymus europaea, were limited to one or two developmental phases each. Ash was most common in the innovation phase (and early biostatic phase), elm was most abundant as scattered seedlings « 3 m height) and small trees in earlyaggradation phases below canopy, while oak was limited to few individuals in the late biostatic and degradation phases (Table 2). The horizontal pattern of the structural units, defined by the development ph~'ies of the canopy trees, revealed a fine-grained mosaic with spatial overlap of trees in different phases (i.e. height). Every site in the plot was, on average, covered by two canopy-layers assigned to different phases (ca 200% canopy cover) of which trees in early aggradation, late aggradation, and early biostatic phase together accounted for ca 150% canopy cover (Table 2). Seedlings in innovation phase predominately occurred as dense blankets in the larger 1999-gap and four small gaps, but also as scattered regeneration beneath closed canopy (Fig. 2A). Ash seedlings dominated the gap regeneration

Table 1. Definition of the developmental phases as applied to individual trees in this study. Developmenta I phase

Definition

Innovation Early aggradation Late aggradation

Seedling> 20 cm, but < 3 m. Trees> 3 m, which have competing ground vegetation under control. Trees> 15 m, the competition from elm on ash and beech declines due to Dutch elm disease. Canopy trees> 25 m but < 80 cm DBH. Canopy trees> 80 cm DBH, still vital enough to fill smaller gaps by lateral growth. Degrading and dying trees.

Early biostatic Late biostatic Degradation

FCOl.OCICAL BULLETINS 52, 2007

45

Table 2. The developmental phases described according to number of trees, distribution to species and canopy cover. Developmental phase Beech Innovation (estimated, in gaps) Innovation (scattered, closed canopy) Early aggradation Late aggradation Early biostatic Late biostatic Degradation Total (minus innovation) Total

1000 16 114 137 48

Number of trees in the plot Elm Oak Ash Shrubs

49000 4 23 49

9

'I

7 331

5 82

with a density of 10-100 trees m- 2 while the scattered regeneration mainly consisted of elm supplemented by beech) elder) rowan) hazel and spindle (Table 2). Trees in the early aggradation phase were scattered in small, welldispersed groups of elm and beech, primarily in the northern part of the plot (Pig. 2B), while trees in the late aggradation phase dominated the S part of the plot, being scattered in the N part (Fig. 2C). The trees in the early biostatic phase formed three independent E-W oriented groups (Fig. 2D). Small groups of beech and oak trees characterised the late biostatic phase (Fig. 2E), while few beech, oak and elm trees were classified as being in the degradation phase (Fig. 2F). The spatial overlap of trees in different developmental phases resulted in a complex structure varying from one to four canopy layers (Fig. 2G)) where the height of the canopy varied between 1 and 40 m above the forest floor (Fig. 3 and 4). In general, the undersrorey light intensity in Suserup Skov was rather low. In transect 2, RLI ranged from 0.5 to 4.8% and in transect 4 from 0.6 to 7.1 % (Fig. 3 and 4). The division of each of the transects into sub-zones based on the developmental phase of the canopy trees (approach 1) showed that for transect 2 there were only significant differences (p< 0.005) in RLI between early biostatic (RLI mean= 1.4) and late biostatic (RLI mean=0.7), while there were no significant differences in RLI between any of the phases in transect 4. In contrast, the division into larger zones, reflecting canopy as well as understorey characteristics (approach 2), showed significant differences (p< 0.005) in RLI between zone 1 and 2, and between zone 2 and 3 for both transects. In both transects, zone 2 (around the 1999 gap) had higher mean RLI (transect 2=2.1, transect 4=2.9) than zones 1 north of the gap (transect 2= 1.2, transect 4= 1.1) and 3 south of the gap (transect 2=0.7, transect 4=1.1). Thus, it appeared that the subzones based on the canopy were not reflected in the understorey light intensity whereas the larger zones based on a combined approach including the understorey characteristics much better reflected the understorey light intensity.

46

104 200 18

20 5 3

13 335

2 5

01<) canopy cover

Total

51000

21.9

323 178 97 12

40.0 56.0 52.6 24.6 5.7

28

25

778 200.9

Discussion Well aware that the identification of canopy layers to individual crowns is, to some degree, a subjective interpretation of a spatially restricted zone (Baker and Wilson 2000) the study showed that a mixed deciduous forest dominated by beech in eastern Denmark has the potential to develop a multi-layered structure. Without the presence of other species, naturally beech-dominated stands may grow into a regular uniform, even-aged appearing forest structure, which covers large areas Gones 1945, Knapp and Jeschke 1991, Jenssen and Hofmann 1996). When analysing the profile- and crown projection diagrams, we flnd that the development of a multi-layered structure, besides from the effects of medium-scale disturbances as e.g. ofthe 1999-storm (Bigler and Wolf 2007) , is based a number of specific processes: 1) the presence of four co-occurrence tree species with different regeneration strategies and life cycles, 2) the vertical stratification among beech trees due to competition in the early and late aggradation phases, 3) the process of beech gradually taking over the canopy space from old degenerating ash and oak trees, and 4) the presence of elm as a typical understorey species, adding to the spatial structure as advance regeneration or as a scattered understorey of trees in early aggradation beneath closed canopy. The four dominant tree species, beech, ash, elm and oak, each contributed to the spatial structure in a specialised way. Beech, as a shade-tolerant and late-successional species, was well-represented in all the developmental phases from the innovation to the late biostatic phase. Typically beech trees dominated the canopy and understorey layers in combination with ash trees in the early biostatic phase. The many small groups ofsuppressed beech trees in the early aggradation phase indicate that the majority of these have lost the competition to their neighbours. Spatially seen) these suppressed trees make up one or two understorey layers. Ash, being a gap-specialist, had established intensively in the young (1999) E-W oriented gap, whereas regenera-

ECOLOGICAL BUI.LETINS 52,2007

Fig. 2A. The spatial pattern of namra! regeneradon in gaps and scanered advance regeneration (innovation phase, < 3 m height) The large canopy gap initiated dense regeneration of ash and bccch in the gap as weU as advance regeneration of primarily dm Nand NW of the gap. In addition the pattern of seedlings indicates four small gaps in the E part of the plot (Fig. ZG). Dashed lines indicate the twO transects drawn in profile djagrams (Fig. 3 and 4).

Fig. 2B. The spatial pattern of trees in the early aggradation phase (3-15 m) is charncterised by a high number ofsmall groups and individual tlttS. In the S pact of the plot, the pattern suggests that the trees have lost the competition to the taller crees in the latc aggrndation phase (Fig. ZC). In the N part of the plot the early aggradation phase is dominated by elm, which utilizes the radiation from the large canopy gap. Dashed lines indicate the twO transects drawn in profile diagrams (Fig. 3 and 4).

Fig. 2C. The spatial pattern of trees in the late aggradation phase

(15-25 m) is characterised by scattered trees in the N part contrasted by dense cover in the SW part of the plot. The dense cover in the SW part relates to the presence of an old, now overgrown gap here. The SW area was registered as canopy gap in 1992. Dashed lines indicate the two transects drawn in profile diagrams (Fig. 3 and 4).

Fig. 20. The spatial pattern of trees in early biostatic (> 25 m bur DBH < 80 em) is characterised by three more or less parallel strips. Comparing the width and orientation of the strips with the width and orientation of the present canopy gap (Fig. 2G) it is suggested. that the trees in the early biost3tic phase all were established in former gaps. Dashed lines indicate the [\yo transects drawn in profile diagrams (Fig. 3 and 4).

ECOLOGICAL BULLETINS 52, 2007

47

'(U.....~ >:~~~,_.' :~ ..

:'.

Fig. 2E. The spacial pattern of trees in me late biosrauc phase (> 80 em DBH) shows ascattered pattern ofsmall groups of 1-5 old oak and beech trees. Dashed lines indjcate the cwo transecrs drawn in profile diagrams (Fig. 3 and 4).

'-..r~. r.:,:?? ·.. . \:.\.-----=--.S....., ~ /.,..'

.

./:( \'" Fig. 2F. The spatial pam:rn of trees in the degradation phase (incl. young trees damaged by me beak down of other [Itt$ or Dureh dm diseasc:) is rarher fragmenred. Dashed lines indicare

the two rranse= drawn in profile diagrams (Fig. 3 and 4).

Fig. 2G. The spatial pattern of rhe canopy according ro developmental phases shows a fine-grained mosaic with spatially overlapping trees in different developmental phases (i.e. height). Beside the fine-grained mosaic pattern, the main character is the E-W orienred canopy gap one-third from the N edge of the plot. Dashed lines indicate the twO transects drawn in profile diagrams (Fig. 3 and 4).

tion was spa"" in all other pans of the plot. Where the early biosratic phase was present, ash formed the canopy, typically with a layer of beech in the late aggradation or even early biosraric phase growing beneath. Here, we expeet beech gradually to rake over the canopy, either by growing through openings in the ash canopy. or by degradation of the ashes due ro their shorter Ijfecycle. Emborg et al. (2000) has described this mechanism as a micro-succession from ash to beech. Also in places where oak dominares the canopy (Iare biosraric), it is expected that the vital subcanopy of beech trees in late aggradation and early biostatic phase will gradually take over as the oaks start degrading

48

(lose more major branches or die). Spatially seen, this can be compared to the situation with micro-succession from ash ro beech. Elm is presently a characteristic undecstorey species according ro its dominance as scattered seedlings and trees beneath closed canopy. The main reason for this parrern is a eombinarion of rhe historic fdJings of elm trees (-1940) and the invasion ofDurch elm disease in 1994 (Emborg et al. 2000), which caused high mortality among the large elm crees (> 15 m height). This again led to recruitmenr of Ile\V dm trees by initiation of shoots from the stem base. Advance regeneration of elm seems ro be able ro esrablish

ECOLOGICAL BUu.EllNS 52. 2007

I ...

L",

~

I

'$

~

10 6 6 4

,,

[o.

-.

0

1: ""

---.-

%

3

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

... .....

2 0

...

£A

20

~

40

60

60

...... 100

120

Fig. 3. Profile diagram, RLI and crown projection diagram for transect 2. Based on the developmental phases of the canopy trees, the rransecrwas divided into eight suh·zones, whereas a more spatial approach reflecting both canopy and undcrsrorcy characteristics led ro a division into only three larger zones (1-3). The different sub-zones and zones are described below. Description ofsub·zones along the (ransen according to the developmental phase of the canopy trees: EB I : slim ash trees in the early biostatic phase form the canopy, clearly separated from the undersrorcy of beech in late/early aggradation, beneath which umbrella shaped elms up [Q 7 m height form a scattered undcrstorcy. LA 1: the canopy consists ofbccches in the late aggradation phase ofwhich one is located east of, but overlapping, the transcct. Below this, a scanered understorey of umbrella shaped elm up to 7 m height. EB2: the canopy is made up by a beech in the early biosratic phase loalted. east of, bur overlapping, the transect, dearly divided from a scattered understorey of beech in the early aggradation phase. The forest floor is covered by dense ash regeneration, 20--100 cm height (Fig. 38), which is nor shown in the profile diagram. FA: the breakdown ofa large beech in the I999·srotm created this gap. To day dense innovation of ash (not depicted in the profile diagram) and scattered umbrella-shaped elm in the early aggradation phase make up the canopy (Fig. 2A, 8, G). The umbrella shaped elm and the beech was established. as advance regeneration prior to gap formation. EB3: a group ofslim ash trees in the: early biostatic phase form the canopy, below which dense growing beeches in late aggradation form a well-developed understorey. The forest floor is aJmost free of vegetation, resulting in a relatively high room (ca 8 01) beneath the canopy. LB: an oak and a beech (standing in front ofbur overlapping the transect, see Fig. 2G) in late biosratic form the canopy below which dense growing beeches in late aggradation, as in zone E, form a well-developed understorey. Below chis is scattered elm. 1....'\: dense growing beeches in late aggradation form the canopy, below which there is a scattered understorey of beech and elm in early aggradation. Standing beech snags (107 and 112 m) refer to the previous tree generation. EB~: slim ash in early biostatic forms the canopy. Below this is an undecsrorey of beech and elm with a wcll-devcloped stratification. Description of the zones reflecting both canopy and undcrstorey characteristics: I: this zone is characterised by very irregular canopy and undersmrey structures. 2: the gap in the canopy and the dense innovation of ash (and beech) at the forese floor characterise this rone (Fig. 2A. G). 3: a regular and closed canopy layer of beech in the late aggradation phase (Fig. 2C), overlapping, or overlapped by, a varied number of canopy-layers, characterise this large zone. Drawings by Anders Busse Nielsen.

ECOLOGICAL BUlLETINS j2, 200l

49

,,

,,

,,

Fig. 4. Profile diagram, RLI and crown projection diagram for transect 4. Based on the devdopmental phases of the canopy trees, the transect was divided into six sub-zones. whereas a more spacial approach reflecting both canopy and undersrorcy characteristics led to a division into only three larger woes 0-3). The diff'ercm sub-zones and zones are described below. Description of sub-zones along the transect according to the developmenral phase of the canopy trees:

LB I : the canopy is made up by three beeches in late biosraric, twO of them standing east of. bur overlapping, the transect (Fig. 2G). Beech and elm in

me early aggradation phase form a scartered undcrscorey from I co 13m hright, dtarly divided from me canopy.

EB I : four slim ash and cwo beeches in me early biosrn.cic phase form the canopy. which is dearly divided from the undersmrcy of beech and elm in early aggradation. LA: the break down ofa large beech in me 1999-s
stems of the beech trees indicate the suppression. LB,: me canopy is defined by a beech tree in me lare biostat;c phase standing east ofbut overlapping the uansect (Fig. 2G). Beech and elm on turn from early (0 late aggradation form a well·developed undcmorey at 6-18 m height, Dutch dm disease has caused stem and basal shoocs on many of the elm trtts, and these secondary "crowns" together with a frnt suppressed dms form a mird. scattered canopy layer at 1-4 m height. EB,: slim ash trees in the early biostatic phast form the: canopy, which is clearly separa[ed from [be dense under$mrey ofbeeeh in [he la[e aggradacion phase. Umbrella shaped elm in [he early aggradation phase form a second. scaner«! unders[orey layer. An old beech-snag (m 102) refers [0 [he former tree genera[ion. Descrip[ion of me zones reflecting bo[h canopy and under$[orey charac[eris[ics: 1: a more or less dense unders[Orey of umbrella shaped elm and suppressed beech in early aggradation characterise this zone (Fig. 28). 2: a dense folia from 10 [0 30 m heigh[ below which mere is a nearly naked forcs[ floor, charac[crise mis zone. 3: like in uansec[ cwo, [he souchern part of the cranscc[ is characccrised by a dense growing undeTScorey of beech (and elm, 84-90 m) in me lace aggradation phase, overlapping or overlapped by a varied number ofcanopy-layers. Drawings by Anders Busse Nielsen.

me

50

ECOLOGICAL BULLFI1NS 52, 2007

as soon as the regularity of the upper canopy layer(s) decreases. An example of this is the broad establishment of elm trees in the S part of the plot, which in 1992 contained a gap, and in a similar process elm is establishing north of the present (1999) gap. The relatively low levels oflight reaching the forest floor (ranging from 0.5% under closed canopy to 7.1 % under light canopy cover) in our study were similar to the findings of Emborg (I 998), also from Suserup Skcw. However, the variation in RLI was related not only to the developmental phase of the canopy, as suggested by Emborg (I998) and Grassi et al. (2003), but also to understorey characteristics. We found that in areas with regular closed understorey layers of beech in late aggradation (50-120 m in Fig. 3 and 4) RLI was consistently low, even where the total number of canopy layers and the developmental phase of the canopy trees varied. This can be explained by an intense inter-tree competition (high number ofindividuals and the ongoing stratification) in the aggradation phases, which makes the crowns "melt together" as if they where part of the same multi-stemmed tree. The findings by Brown and Parker (1994) suggesting that leaf area density is highest among trees in the early developmental phases support this interpretation. A relatively low canopy height may also decrease the amount oflight in the understorey (Brown and Parker 1994). Based on these findings, we suggest that the understorey light intensity is a product of the density and height of the sub-canopy layers more than the developmental phase of the canopy trees or the number ofcanopy layers. From a silvicultural point of view this finding highlights the importance ofpaying as much attention to the density ofsubcanopy layers as to the species and developmental phase of the canopy when deciding management actions aiming at initiating natural regeneration.

Conclusion We demonstrated the spatial complexity of the forest structure in a I-ha plot in Suserup Skov visually by use of profile- and crown projection diagrams. By linking the diagrams to quantitative measurements of understorey RLI and data on individual trees it was possible to refine the understanding of the spatial complexity of vegetation structure and identifY structural factors which determine the understorey light intensity. The horizontal pattern showed a fine-grained mosaic of trees in different developmental phases resulting in a variable canopy height ranging from 1 to 40 m height. Beneath the canopy one to three well-developed understorey layers were the most frequent spatial structures across developmental phases and dominant species in the canopy. The canopy cover was, on average, double-layered, calculated as the sum of the layers of trees in different developmental phases. The main reasons for this well-developed stratification seemed to be irregu-

ECOLOGICAL BULLETINS 52, 2007

larity of the canopy layers across small neighbouring structural units in combination with the presence of four cooccurring tree species with different regeneration strategies and life cycles. A comparison of the spatial structure to understorey light intensity indicate that RLI in the understorey, varying from 0.5 to 7.1 %, is as much a product of the density of the sub-canopy layers as the developmental phases of the canopy or the numbers of canopy layers. In fact, we found the continuous cover of dense growing understorey trees across neighbouring structural units to be the main determinant for RLI one m above the ground. Acknowledgements - Thanks

to Som Akademi for permitting research in Suserup Skov, to Jens Emborg for providing unpublished data from the 1992 Silvistar recordings, and to Jaris Bigler and Arne Hahn for help with data collection. The project was supported by the NatMan project (EU 5th framework programme grant QLK5-99-01349) and the SpyNatForce project (Statens Jordbrugs- og Veterinxrvidenskabdige Forskningscad).

References Baker, P.]. and Wilson,]. S. 2000. A quantitative technique for the identification of canopy stratification in tropical and temperate forests. - For. Eccl. Manage. 127: 77-86. Bigler, J. and Wolf, A. 2007. Structural impa<.:t ofgale damage on Suserup Skov, a near-natural temperate deciduous forest in Denmark. Ecol. Bull. 52: 69-80. Blomqvist, A. G. 1879. Eine neue Methode den Holzwuchs und die Standortsvegetation bildlich darzustellen. - Kannedom av Finlands nature och Folk. Finska Vetenskaps-Societ. H. 31, from Sarvas, R. 1958. Brown, M. J. and Parker, G. G. 1994. Canopy light transmittance in a chronosequence of mixed-species deciduous forests. -- Can.]. For. Res. 24: 1694-1703. Emborg, J. 1998. Understorey light condition and regeneration with respect to the structural dynamics ofa near-natural temperate deciduous forest in Denmark. - For. Ecol. Manage. 106: 83-95. Emborg, J., Christensen, M. and Heilmann-Clausen, J. 2000. The structural dynamics of Suserup Skov, a near-natural temperate deciduous forest in Denmark. For. Ecol. Manage. 126: 173-189. Franklin, J. F. et al. 2002. Disturbances and structural development of natural forest ecosystems with silvicultural implications, using Douglas-fir forests as an example. - For. Ecol. ~anage. 155:399-423. Fritzb0ger, B. and Emborg, J. 1996. Landscape history of the deciduous h)rest Suserup Skov, Denmark, before 1925. For. Landscape Res. 1: 291-309. Grassi, G. et al. 2003. The structural dynamics of managed uneven-aged conifer stands in the Italian eastern Alps. - For. Eco1. Manage. 185: 225-237. Gustavsson, R. 1986. Struktur i lovskogslandskap. - Srad oeh Land 48, Ph.D. thesis, Swedish Univ. of Agricultural Science, Alnarp, in Swedish. Gustavsson, R. 1988. Naturskogar i Blekinge. Skogsarkitetur, dynamik. Ti-adens strategier oeh framgang i deras vilda familjeliv. Blekinges Natur special issue 1988: 15-49.

51

Hannon, G., Bradshaw, R. and Emborg, J. 2000. 6000 years of forest dynamics in Suserup Skov, a semi-natural Danish woodland. - Global Ecol. Biogeogr. 9: 101-114. Hei1mann~Clausen,J. et al. 2007. The history and present condi~ tions of Suserup Skov ~ a nemoral, deciduous forest reserve in a cultural landscape. ~ Eco1. Bull. 52: 7~17. Jenssen, M. and Hofmann, G. 1996. Der naturliche Emwicklungszyklus des baltischen Perlgras- Buchenwaldes (MelicoFagetum). - Forstwirtschaft und Landschaftsokologie 30: 114-124. Jones, E. W 1945. The structure and reproduction of the virgin forests of the North Temperate Zones. - New Phytol. 44: 130~~148.

Knapp, H:. D. and Jeschke, L. 1991. Naturwaldreservate unci Naturwaldforschung in den ostdeutchen Bundeslandern. ~ Schriftenreihe fur Vegetationskunde, BundesforschungsanstaIr flir Naturschutz und Landshaftsokologie 21: 21-54. Koop, H. 1989. Forest dynamics. Silvi-Star: a comprehensive monitoring system. - Springer.

52

Madsen, P. and Larsen, ]. B. 1997. Natural regeneration of beech (Fagus sylvatica) with respect to canopy density, soil moisture and soil carbon content. - For. Eco1. Manage. 73: 37-43. McCarthy, B. c., Small, C. J. and Rubino, D. L. 2001. Composition, structure and dynamics of Dysart Woods, an oldgrowth mesophytic forest of southeastern Ohio. ~ For. Eco1. Manage. 140: 193-213. Nielsen, A. B. and Nielsen, J. B. 2005. The use of profile diagrams for mixed stands in urban woodlands-- the management perspective. - Urban Forestry and Urban Greening. 3: 163-175. Sarvas, R. 1958. Ein Verfahren zum der Kronenkarten. ~ Papers from 12th IUFRO Congress, Oxford 2: 51--56. Watt, A. S. 1925. On the ecology of British beechwoods with special reference to their regeneration. Part II, section II and III: the development and structure of beech communities on the Sussex Downs (continued). ~ J. £co1. 13: 27~73.

ECOLOc.;lCI\L BULLETINS 52. 2007

Ecological Bulletins 52: 53-67,2007

Suppression and release during canopy recruitment in Fagus sylvatica and Fraxinus excelsior, a dendro-ecological study of natural growth patterns and competition Jens Emborg

Emborg, J. 2007. Suppression and release during canopy recruitment in Fagus sylvatica and Fraxinus excelsior, a dendro-ecological study of natural groVl'th patterns and comapetition. - Eco!. Bull. 52: 53-67.

In this dendro-ecological study stem radial growth patterns were used to reconstruct the growth patterns of and competitive interaction between beech Fagus sylvatica and ash !'raxinus excelsior in a semi-natural temperate deciduous forest in Denmark. The site, Suserup Skov, has a long history of low human impact under a relatively calm natural disturbance regime. The structural dynamics of Suserup Skov can be described by the forest cycle concept (gap phase dynamics). According to previous studies the climax micro-succession from ash to beech is an integral part of the forest cycle. The objective of the present study was to compare the growth and recruitment patterns of ash and beech with respect to the forest cycle. Tree ring cores from 100 ash and 151 beech trees, from sapling size (> 5 em DBH) to canopy tree size, were sampled. Growth rates under release were significantly higher than growth rates under suppression - a factor 3 for ash and 5 for beech. Most sampled trees of ash (89%) and beech (99%) had experienced suppression as well as release (beech 76%, ash 96%). Beech experienced more and longer periods of suppression, than ash, and spent 80% yr in suppression, while the ashes only spent 40% yr in suppression. Accordingly, ash trees were significantly higher and thicker than beech trees of the same age. The study revealed clear, distinct and significant differences in the growth patterns of beech and ash. The results can be interpreted as a "rush" competitive strategy for ash, to establish first in new gaps and then to stay in front while rushing towards the canopy. The interpretation for beech is a "stop and go" competitive strategy, step by step slowly approaching a dominant position in the canopy. The described growth patterns of ash and beech are in accordance with the suggested model of the forest cycle, including climax micro-succession from ash to beech. The growth patterns and competitive strategies found confirms with other studies of the ecology of ash and beech ~ ash is a light demanding gap specialist and beech is a shade-tolerant "climax" species. However, the full picture is far more complex. For instance, ash and beech are equally shade-tolerant in youth - for ash this feature ceases with age which creates a complex competitive pattern. The example from Suserup Skov explains some of the forest dynamics that allows long-term co-occurrence ofearly and late successional species in late successional ("climax") forest.

.! Emborg ([email protected]), Forest and Landscape Denmark, Unit). of Copenhagen, Rolighedsvej 23, DK- J958 Frederiksberg C, Denmark.

Copyright (<;) ECOLOGICAL BULLETINS, 2007

53

The concepts of succession and climax including the ecological roles of pioneer and climax species have been intensively discussed for many years (Warming 1895, Clements 1916, Gleason 1926, Raup 1957, McIntosh 1985, GlennLewin et al. 1992). In this work, I refer to the well known concepts of succession and climax as a basic conceptual framework. Taking the dynamic nature of forest ecosystems and the role of natural disturbances into account, readers should be aware of the conceptual character of the "climax stage" as a relative stable hypothetical "end-point" to succession. In most recent literature the more pragmatic notion of "late successional stage" is preferred. I use both terms, partly to ease reference to older as well as more recent literature. Bormann and Likens (1979) concluded that the temperate deciduous forests, exemplified in Hubbard Brook, NH, USA, would develop into a shifting mosaic of developmental phases, assuming a calm (smallscale) disturbance regime. In the shifting mosaic steady state, the stand as a whole would be uneven-aged with representation of many tree species, including some early successional species on a continuing basis. The scale of the mosaic that develops depends on the typical disturbance agents in the area (hurricane, fire, flooding, insects, wind, etc.). Smaller or larger canopy gaps represent an opportunity for some relatively light demanding species to achieve a position and maintain a presence in the upper canopy layer (Whitmore 1989) - even in late successional ("climax") forest characterised by small-scale gap-dynamics (Forcier 1975, Grubb 1977). In late successional forest, establishment of light demanding species in gaps succeeded by intrusion of more shade tolerant species is referred to as climax micro-succession (Forcier 1975, Grubb 1977). Climax micro-succession is regarded as one of the mechanisms that allow for permanent co-occurrence of early and late successional species within the climax stage, through long-term cyclic replacement processes in canopy gaps (Forcier 1975, Grubb 1977). Forcier (1975) studied the cyclical replacement of Betula alleghaniensis by AceI' saccharum and Fagus grandifOlia in the Hubbard Brook ecosystem. Climax micro-successions from Betula pendula to Fagus sylvatica have been described in central Europe (Remmert 1985, 1987, 1991, Wissel 1991), and ashbeech replacement within the forest cycle has been described in southern England (Watt 1925, 1947). This indicates that climax micro-succession might be an integral part of the natural dynamics in many temperate forest ecosystems. This seems to be the case in Suserup Skov, a well studied semi-natural temperate mixed deciduous forest site in Denmark (Emborg et al. 1996, Heilmann-Clausen et al. 2007). A conceptual model of the particular forest cycle of Suserup Skov has been proposed (Emborg et al. 2000) and further elaborated by Christensen et al. (2007). According to the model, micro-succession from ash Fraxinus excelsior to beech Fagus ~ylvatica occurs as an integral part of the forest cycle. Ash typically establishes first in new gaps because of its pioneer features (light, wind-dispersed

54

seeds, seed production almost every year etc.), while beech establishes within a few years, typically at the first mast year after gap formation (Emborg 1998). Ash usually grows ahead of beech towards the canopy, while beech survives in a more or less suppressed position in the shade underneath the ash trees. During the early biostatic phase, beech usually displaces ash in the upper canopy stratum and gains full control of the canopy layer, according to the model. Eventually, the beech trees grow old, fall apart, fall over, or just die ,~ creating new canopy gaps. A new gap might represent an opportunity f()r ash to establish in dIe gap and start a new cycle of the "climax micro-succession'. The described forest c)'cle model is to be considered as an idealised conceptual model - a simplified abstraction that seeks to grasp the core features of a much more complex reality (Christensen et al. 2007). Nevertheless, the concept ofclimax micro-succession points to the complexity of forest dynamics and the difficulties, in practice, of distinguishing the climax stage (as a relatively stable endpoint to succession) from the preceding successional stages. Attempts to untangle the relationship between successional processes and the emerging relatively stable (hypothetical) climax stage, brings the competitive interaction among tree species into focus. The basic distinction between light-demanding (pioneer) species versus shade-tolerant (climax) species is part of this discussion (\X'hitmore 1989). However, the competitive patterns of different tree species are far more complex than indicated by this basic distinction (Whitmore 1989). The studies of Canham (1985, 1988, 1989, 1990) exemplifY how various shadetolerant species perform distinctly different responses to canopy gaps - representing various growth patterns or "survival strategies". Such detailed studies of the ecological roles and competitive patterns of different tree species are highly relevant to understand how trees interact to form the overall dynamics of the forest ecosystem. The present study focuses on the competitive interaction between beech and ash, in order to better understand the overall dynamics of the whole ecosystem in Suserup Skov. If the described climax micro-succession from ash to beech is a fairly accurate depiction of reality, it should be reflected in the growth patterns of ash and beech trees. According to the model, ash trees are expected to have a history of continuous rapid, i.e. released, growth from seedling or sapling to canopy size; as compared to beech trees, expected to have a history of more suppressed groV\.rth - because beech typically will grow up in the shade of larger (ash) trees, before they eventually conquer a position in the upper canopy layer. However, the picture might not be as clear as expected according to this conceptual model. As an example it is well known that ash, in youth is very shade tolerant (Gia 1927), which might add surprising competitive interactions to the model. This study centres on the growth patterns of ash and beech. By a dendro-ecological approach the historical stem radial growth patterns of ash and beech trees, were used as

ECOLOGICAL BULLETINS 52, 2007

a proxy to reconstruct the typical growth patterns of beech versus ash trees as they grow up from saplings to full size canopy trees. The specific objectives of the study were: 1) to determine the typical growth patterns of ash versus beech, from saplings to canopy trees, under natural competitive conditions (non-intervention forest), and 2) to discuss the growth patterns ofash and beech with regard to the specific forest cycle model of Suserup Skov and the general concepts of succession and climax.

Materials and methods The site The study was conducted in Suserup Skov, a near-natural deciduous forest in Denmark (19.2 ha, 55°22'N, 11 °34' E). Suserup Skov was chosen for this study, due to its long history of relatively natural growing conditions with limited human impact (Heilmann-Clausen et al. 2007). It was assumed that the competitive interaction between beech and ash at this site could be studied appropriately in the spatial and temporal scales of this study. The climate of the site is cool-temperate, and sub-oceanic (Troll and Paffen 1963). The annual mean temperature is 8.1°C, and the annual mean precipitation is 635 mm with maximum occurring in late summer and autumn. Most of the soils have developed from glacial loamy till (Vejre and Emborg 1996). The growth conditions are generally favourable, as indicated by tree heights of up to 41 m (Emborg et al. 1996). The study was conducted in the northwestern part ofSuserup Skov (part A, 10.7 ha), regarded as the least disturbed part of the forest according to Emborg et al. (1996). Beech dominated part A as the most prominent species in the upper canopy layer accounting for 64% of the total basal area (BA). Beech was present in all canopy layers from the forest floor to the upper canopy. Ash accounted for 13% of the BA in part A and was present in all canopy layers. However, ash had a more patchy appearance than beech, because it typically establishes in canopy gaps. Oak Quercus robur accounted for 15% of the BA, but is distinctly retreating from Suserup Skov representing a long-term successional trend (Emborg and HeilmannClausen 2007). There were hardly any saplings or sub-canopy trees of oak in the whole forest, so oak was only represented by a few very large specimens. Wych elm Ulmus glabra accounted for 6% of BA. Wych elm basically performs in the shrub-layer (and in gaps), and only rarely specimens achieve a height above 15~20 m. The present study concentrats on beech and ash as they represent the two main tree species currently competing successfully to conquer and hold positions in the upper canopy layer of Part A in Suserup Skov. This interpretation of the dynamics in Suserup Skov is in accordance with the conclusion of Emborg et al. (2000) and Christensen et al. (2007) regard-

ECOLOGICAL BULLETINS 52, 2007

ing ash and beech as the two most important tree species that currently drives and shapes the overall dynamics - the forest cycle. Suserup Skov is considered one of the best existing examples of relatively undisturbed semi-natural deciduous lowland forest in the northwestern Europe, with a long history of relatively low human impact (HeilmannClausen et al. 2007). The long-term as well as the more recent histoty of Suserup Skov has been studied in detail (Fritzb0ger and Emborg 1996, Hannon et al. 2000), and an overview has been presented by Heilmann-Clausen et al. (2007). The continuity in tree cover dates at least back to 4200 BC and consequently probable dating back to the primeval forests invading after the last glacial (some 12000 yr ago). Mter 1792 Suserup Skov was fenced, to protect against grazing livestock. For various reasons Suserup Skov was never systematically exploited for timber. In 1854 Suserup Skov was formally protected against commercial cutting, in 1925 it was legally protected for nature preservation, and since 1961 the forest has been kept as a strict non-intervention forest reserve (Fritzb0ger and Emborg 1996). Ever since the first survey (1815) of Suserup Skov the growing stock of part A has increased -- to a current level of ca 550 m 3 (trees> 29 em DBH) in 1992 and 2002 (Fritzb0ger and Emborg 1996, Emborg and Heilmann-Clausen 2007). No major natural disturbances, within the last 200 yr, have lead to major perturbations of the ecosystem. The largest natural disturbances were the hurricanes of 1967 and 1999 (Emborg et al. 1996, Bigler and Wolf 2007). Both hurricanes caused considerable wind-throw, but they did not set the whole ecosystem back to early successional stages (Emborg and Heilmann-Clausen 2007). Despite the small size of the plot (part A, 10.7 ha), the overall sizeclass distribution, including all tree species, resembled a negative exponential function (Emborg et al. 1996), and the shifting mosaic of the studied plot (mapped in 1992 and 2002) was presumed to be dose to the steady state (Emborg et al. 2000, Christensen et aI. 2007). These results indicate that Suserup Skov in many senses can be regarded to represent a late successional stage of a temperate lowland European beech forest.

Sampling and measurements A total sample of 151 beech trees and 100 ash trees were sampled within part A. Tree ring samples were taken at breast height (BH, 130 em above ground) with an increment borer (i.e. all ages are given as "age at BH"). The selection criteria for sample trees were: 1) trees were sampled from the under-storey, from the sub-canopy stratum as well as from the uppermost canopy layer. 2) The sampling of full-size trees from the top canopy layer (h > 30 m) was restricted to trees having recently obtained a position in the upper canopy stratum (i.e. avoiding "big old trees" by

55

evaluating individual trees in the field). 3) The selected trees should represent all height classes (5-m intervals) from under-storey trees to canopy trees (the distribution to height-classes can be seen in Table 3). Only trees> 5 em DBH (diameter at BH) were sampled and only one core per tree was taken to minimise the damage to living trees. In order to optimise the total research outcome of the work as many trees as possible were sampled within the so-called Silvi-Star plot (0.96 ha), located centrally in part A, designed for detailed studies of the forest structure and dynamics (Nielsen and Hahn 2007). To achieve a more balanced sample of beech and ash (beech is more frequent than ash) a limited number of ash were sampled according to the above criteria in the forest just outside the Silvi-Star plot. Tree rings were recorded to nearest 0.01 mm, starting from the bark, using a microscope and a moveable stage, connected to a computer (ADDO Arsringsmatmaskin, Sweden). If any core missed the centre of the trunk by more than about 1 em the core and the tree was rejected from the analysis. Cross-dating and other dendro-chronological standardizations were not carried out for this study It is likely that the tree-ring record of some trees were not complete due to occasional partially or totally missing annual rings (Fritts 1976, Canham 1985, 1990). In line with Canham (I985, 1990) the analyses carried out in this study of growth patterns were not considered particularly sensitive to the absence of a few rings in any core.

Analyses It is well known that the social position of individual trees (e.g. dominant, co-dominant, intermediate, overtopped) is clearly reflected in the radial stem growth (Fritts 1976, Canham 1985, Cook 1987, Rohrig and Gussone 1990, Smith et. al 1997). Therefore it is possible to study the growth patterns of individual trees in retrospect, by using the annual radial stem growth over time, as a proxy variable. This approach was applied by Canham (1985,1990), in studies ofcanopy recruitment in shade tolerant tree species in northern hardwood f(xests in the Adirondack Mountains, USA. He documented that the growth of (suppressed) trees beneath closed canopies was distinctly and significantly lower than (released) trees growing in a wide range of canopy openings. Based on this knowledge he used the patterns of radial growth to reconstruct the history of suppression and release during canopy recruitment of Acer saccharum (Canham 1985) and Fagus grandijolia (Canham 1990). In the present study a similar approach was used to study the growth patterns and competitive strategies ofbeech and ash in Suserup Skov. The entire study comprised three sub-studies: 1) growth rates of ash and beech under suppressed versus released conditions, 2) growth patterns and competitive strategies of ash and beech, and 3) recruitment of ash and beech.

56

It should be remarked that the study did not include a spatially explicit analysis or interpretation of the data i.e. the specific competitive interaction between individuals was not studied.

Growth rates under suppressed versus released growing conditions As a precondition for the subsequent analyses the growth rates under suppressed versus released growing conditions were studied. Suppression can be defined as a marked reduction in growth caused by crowding or shading from neighbouring trees, whilst release can be defined as a marked increase in growth due to removal of competitors, occurring in even small gaps (Fritts 1976). In order to determine the species specific threshold between suppressed growth and released growth, as expressed by the tree ring width, a sub-sample of 98 sub-canopy trees were selected after evaluation in the field: Each of the selected trees represented one of two alternatives, a clearly "suppressed" (growing in complete shade, under closed canopy) or a clearly "released" condition (access to light and space, due to smaller or larger canopy openings, gaps), referring to the above definitions of Fritts (1976). The growing conditions (suppressed/released) of the (estimated) last 10 yr of each selected tree were evaluated in order to avoid trees with a record of recently (i.e. within the last 10 yr) dramatic change in growing conditions, because the aim was to achieve a pure estimate of growth under either suppressed or released conditions. As an example. trees released by the fall/death ofa larger neighbouring tree within the last 10 yr (estimated) were excluded. A total of 32 released ash, 19 suppressed ash, 15 released beech, and 32 suppressed beech trees were analysed. The nine most recent tree rings (1983-1991) were taken into account for this specific study, to secure a dose relationship between growth rates and current/recent growing conditions (suppressed versus released). The threshold bervveen suppressed and released growth (to be used in subsequent analyses) was defined as the arithmetic mean of the average annual radial stem growth under suppressed and the average annual radial stem growth under released condition. In this way it was possible to achieve a site- and species specific estimate for annual tree-ring grO\vth under suppression and release for ash as well as for beech in Suserup Skov.

Growth patterns and competitive strategies of ash and beech "Periods of suppressed growth" was distinguished from "periods of released growth", by the method suggested by Canham (1985, 1990). Periods of suppression were defined as intervals in which there were four or more years of

ECOLOG1CAL BULI.IT1NS 52,2007

growth below the threshold (between suppressed and released growth, described above), during which there were no periods of three or more years of consecutive growth greater than the threshold. Periods of release were defined as intervals in which there were four or more years of growth above the threshold, during which there were no periods of three or more years of consecutive growth lower than the threshold. This method is considered a rather conservative approach, that eliminates the effect of shorrterm fluctuations in growth, e.g. due to climatic effects (Canham 1985). Based on the tree-ring record ofeach tree, the periods of suppression and release were determined by counting from the centre ofthe core towards the periphery. The chosen method is in line with Canham (1985, 1990), leading to a rather strict and unequivocal result. Other (less conservative, more sophisticated and/or more subjective) approaches to define the cut (or shift) between periods of suppression and release were considered, but rejected with reference to the methodological discussion and conclusion of Canham (1985), and for comparing with similar studies (Canham 1985, 1990). Problems defining a precise cut (or "shifting-year") arise in cases ofslow, gradual change where growth rates happen to swing above/below the threshold over a longer period (as opposed to the cases shown in Fig. 2 and 3, showing nice and clean shifts between suppression and release periods). However, in practice this problem only occurred in a limited number of cases - for both ash and beech. The number and length of the periods of suppression and release, and the total number of years spent in suppression (Ts) and release (Tr), were determined for each tree. The age, OBH, and height (h) ofeach tree of the whole material (l 00 ash and 151 beech trees) were measured. Age ("at breast height") was determined as the number of treerings counted at each core. OBH was measured with callipers and heights were measured by an (Blume-Leiss) altimeter. Overall figures for the two tree species were computed and compared. Tc.) compare the recruitment patterns of ash and beech in more detail with regard to the age and height of the trees the material was analysed by 10-yr age classes and by 5-m height classes. The complete set of data was used to determine possible differences in growth patterns and competitive strategies of ash and beech.

Recruitment of ash and beech Since both ash and beech trees compete to achieve a "permanent" position in the upper canopy layer it is ofparticular interest to study the recruitment history of trees that actually succeeded (or were in positions having obvious potential) to conquer a position in the upper canopy layer. Such trees we call "the recruits" in line with the definition of canopy recruitment suggested by Canham (1985): the year in which an individual began the period of release during which it grew to its current position in the canopy.

ECOLOGICAL BULLHINS 52, 2007

To study the growth patterns of the recruits a sub-sample of trees was analysed. The sample consisted of trees that recently had achieved a position in the upper canopy stratum, as well as trees in a released position in a favourable canopy opening, (estimated) being able to reach a position in the top canopy layer in a series of consecutive released growth. The transect profile diagrams of Nielsen and Hahn (2007) from the Silvi-Star plot gives a good impression of the forest structure and possible recruits in the sample area. The sample criteria implied that even trees in the late aggradation phase (h > 15 m) could be considered as recruits, if they were in a favourable position forming or being part of the uppermost canopy layer of the particular growing spar. The sample included 47 trees (32 ash, 15 beech). The recruitment history of these trees were analysed in terms ofduration and sequence ofsuppression and release periods as reflected in the tree-ring sequence from sapling to (potential) canopy tree.

Statistics Linear regressions were computed by the least squares method. T-tests were used to compare means of samples drawn from assumed normal distributions. Mann-"Whitney's (non-parametric) U-test was used to compare means when data were not assumed to be normally distributed. A X2 test (Fowler and Cohen 1990) and a generalised linear model for ordinal response (McCullagh and Nelder 1989) were used to compare frequency distributions.

Results Released versus suppressed growth for ash and beech The analysis of radial stem growth of trees under suppressed versus released conditions showed that a.o:;h as well as beech grew distinctly and significantly faster under released than under suppressed conditions. On average relea.<;ed ash grew 2.28 mm ye l (n=32, sample standard deviation SO=0.93) and suppressed ash grew 0.75 mm yr- I (n=19, SO=0.51). Released beech grew 3.14 mm yr 1 (n= 15, SO= 1.43) and suppressed beech grew 0.60 mm yr-I (n=32, 50=0.45). For both species the difference between suppressed and released growth were highly significant (p
57

Comparison of the growth patterns of ash and

beech The overall result (Table 1) shows clear and significant differences between the growth patterns of ash and beech in Suserup Skov" Most individuals of ash (89%) and beech (99%) had experienced period(s) ofsuppression, and most individuals of ash (96%) and beech (73%) had experienced released period(s) as well. The longest period ofsuppression recorded was 83 yr for beech and 61 yr for ash. The longest period of release was 57 yr for beech and 74 yr for ash. Most beech trees (76%) started their sapling life (height, h> 1.3 m and 0 BH>5 cm) under suppression, while most ash trees (71 %) started their sapling life in release. The number of release episodes, as well as the number of suppression episodes per core varied between 0 and 4 for both species. The frequency distributions of number of released episodes for ash and beech were compared by a chisquare test showing that ash and beech did not have the same frequency distributions (p=O.OOl). The overall difference between ash and beech is illustrated by the results presented in Table 1, showing that ash on average had more and longer release episodes than beech, and had spent significantly (p
standard deviations, Table 1). At the overall level, the result quite consistently indicate that the beech trees generally have a record of much more suppressed growth than ash, and that the ash trees generally have a record of much more released growth.

Beech and ash compared by age classes The analysis across age-classes (Table 2), at a more detailed level, documented pronounced and significant differences in the growth patterns of ash and beech. The average age was similar for ash and beech in all age-classes (no significant differences) easing the statistical comparison of the other variables, as presented below without hlrther precautions regarding this aspecc Ash was taller and thicker than beech for all age classes. All differences were highly significant, p
Table 1. Overall result of the dendra-ecological study of the growth patterns of ash Fraxinus excelsior and beech Fagus sylvatica, in the temperate deciduous forest, Suserup Skov" Sample standard deviations in parentheses. Significance is indicated for T-tests and U-tests (** = p
Number of cores Mean age (in BH) of cored trees (yr) Mean diameter of cored trees (cm DBH) Mean height of cored trees (m)

100 55 (12) 24 (12) 23 (7)

100

Number of cores with release periods Mean number of release periods/core Mean length of release periods/core (yr) Mean total length of release/core (yr)

96 1.5 22 33 (19)

96

Number of cores with suppression periods Mean number of suppression periods/core Mean length of suppression periods/core (yr) Mean total length of 5uppression/core (yr)

89

89

1.4 16 22 (17)

58

Test

Beech

%

%

151 60 (12) 15 (8) 14 (6)

100

110 1.2 10 12 (14)

73

150 1.8

99

27 48 (16)

**T *** T *** T

*** U

*** U

ECOLOGICAL BULLETINS 52, 2007

rn

n

o

5CJ

8 t:tl

C

~

>-J

~

N

§ Table 2. Dendro-ecological analysis of the growth patterns of ash Fraxinus excelsior and beech Fagus sylvatica across age classes. (n) number of trees sampled l (0) mean diameter DBH, (H) mean height, (Age) mean age, (Nr) number of release periods, (Lr) mean length of release periods, (Tr) mean total time spent under release, (Ns) mean number of suppression periods, (Ls) mean length of suppression periods, (Ts) mean total time spent under suppression, (Trffs) release/suppression ratio. T-test (D1 Hand Age) and U-test (Nr, Tr, Ns and Ts) results indicated for ash and beech compared by age classes, ns = not significant p>0.05, * = p<0.05, ** = p
Species Ash

n

o (cm)

H(m)

Age (yr)

Nr

50-59 60-69 70-79 Total

13 18 27 31 11 100

12 '15 20*** 22*** 28*** 38***

13 ns 22*** 23*** 25*** 28***

35 115 45 ns 55 ns 64 115 72 n5

1.0ns l.4 ns 2.0*** 1.5"5 1.3"5

30-39 40-49 50-59 60-69 70-79 80-90 Total

6 26 41 50 18 10 151

10 12 15 15 19 22

10 12 14 14 17 18

37 46 54 65 73 84

0.8 1.0 1.0 1.3 1.3 1.4

Age class 30-39 40~9

Beech

V"I

\.0

Released Lr (yr)

Tr (yr)

Ns

15 21 17 24 41

15 m 30*** 33*** 37*** 53***

1.2 11S 1.YS 1.9n l.4"S 1.1 ns

8

6 9 10 13 16 21

1.7 1.7 1.6 1.9 1.8 2.1

9 10 10 12 15

$

Suppressed Ls (yr) Ts (yr)

TrlTs

TrlTr+Ts

Tsffr+Ts

18 12 12 20 17

2OIlS 16*** 22*** 28*** 19***

0.75 1.88 1.50 1.32 2.79

0.43 0.67 0.60 0.58 0.74

0.57 0.36 0.40 0.44 0.26

19 22 27 27 32 30

31 37 44 52 57 64

0.19 0.24 0.23 0.25 0.28 0.33

0.16 0.20 0.19 0.20 0.22 0.25

0.84 0.80 0.81 0.80 0.78 0.76

es were highly significant, p
Beech and ash compared by height classes The analysis by height-classes (Table 3) provided a more detailed picture of differences in growth patterns between beech and ash. The results consistently documented that beech trees generally had a history of many years of suppressed growth and few years of released growth, as opposed to ash that generally spent more time in release and less time under suppression. The results needs to be interpreted cautiously, since two of the height-classes ofash versus beech (15-20, 25-30 m) show significant (though small, 1-2 m) differences between average heights. A positive correlation between height and age was generally evident for both species, even though the average age only increased moderately with increasing height (in particular for beech). For all height classes the age of ash was lower than the age of beech (highly significant, p
60

was decreasing with increasing height for both species. This result indicates that the most successful individuals, for both species, are those who are favoured by a relatively high proportion of growth seasons under released conditions.

Analysis of the canopy recruits The analysis of the recruits (the "successful" canopy individuals) of ash and beech showed significant differences between the two species (Table 4). The average ages (Table 4) were not significantly different between the recruits of ash (n=32) and beech (n=15). The ashes were significantly higher (p
Discussion and conclusions Growth patterns of ash and beech - and the forest cycle The overall conclusion is that there are clear and significant differences, in the growth patterns of beech and ash under (relatively) natural growing conditions, as found in Suserup Skov. The beech trees had experienced more and/ or longer periods of suppression than the ash trees. Consequently, beech rrees were significantly shorter than ash trees of the same age. The number and length of suppression episodes found in the present study for beech in Suserup Skov are in the same order of magnitude as for Fagus grandifllia in The Adirondack Mountains (Canham 1990), and as for eight different American, European, and Asian Fagus species (Peters 1992). Even though the results seems clear and statistically significant it should be kept in

ECOLOGICAL BULLETINS 52, 2007

cr1

8 5 Cl

n ~

to

C

rr~

~

N N

'.J

Table 3. Dendra-ecological analysis of the grawth patterns of ash Fraxinus excelsior and beech Fagus sylvatica across height classes. (n) number of trees sampled, (D) mean diameter DBH, (H) mean height, (Age) mean age, (Nr) number of release periods, (Lr) mean length of release periods, (Tr) mean total time spent under release, (Ns) mean number of suppression periods, (Ls) mean length of suppression periods, (Ts) mean total time spent under suppression, (TrITs) release/suppression ratio. T-test (D, H and Age) and U-test (Nr, Tr, Ns and Ts) results indicated for ash and beech compared by age-classes, n5 = not significant p>0.05, * = p<0.05, ** = p
Species Ash

Beech

0\

........

n

D(cm)

H(m)

Age (yr)

Nr

0-10 10-15 15-20 20-25 25-30 > 30 Total

4 13 15 23 33 12 100

7 115 9* 17'15 21 115 29 n5 47

7115 12 n5 18* 22 115 28** 33

45 115 46*** 54 115 54*** 58 11s 66

1.0115 0.8 11s 1.6ns 2.0 ns 1.6'15 1.2

0-10 10-15 15-20 20-25 25-30 > 30 Total

38 44 38 23 7 1 151

9 12 18 23 34 35

7 12 17 22 26 31

57 57 60 68 63 71

0.7 0.9 1.6 1.7 1.9 3.0

Height class

Released Lr (yr)

Suppressed Ls (yr)

Ts (yo

TrlTs

Tr/Age

Ts/Age

l.3 ns lAns 1.7n5 1.8115 1Ails 0.7

22 26 18 13 12 11

28** 36*** 30* 23*** 17 115 8

0.64 0.28 0.80 1.35

0040

0.62 0.78 0.56 0.43 0.29 0.12

1.6 1.6 2.0 2.0 1.7 3.0

42 32 22 24 18 8

51 51 43 49 30 23

0.10 0.12

Tr (yr)

Ns

18 13 15 15 26 49

18115 10ns 24* 31 ** 41 ns 59

12 7 11 12 17 16

5 6 18 20 32 48

2041 7.38

0042 0041 1.07 2.09

0.22

0044 0.57 0.71 0.89

0.09 0.11 0.30 0.29 0.51 0.68

0.89 0.89 0.72 0.72

0048 0.32

Table 4. Dendra-ecological analysis of canopy recruits (as defined in the methods section), of ash Fraxinus excelsior and beech Fagus sylvatica. (n) number of cores, (Tr) average total time in release, (Ts) average total time under suppression, (Ns) number of suppression periods, (SD) sample standard deviation. T-test (T) and Mann-Whitney's U-test (U): ns == not significant p > 0.05, * == P < 0.05, ** == P < 0.01, *** == P < 0.001. Ash (n=:32)

Variable

Beech (n==15) SD

SD Age (yr) DBH (cm) Height (m) Tr (yr) Ts (yr)

Ns

60 36 29 46 14 1.0

10.8 12.1

62 27 21 31 31 1.8

4.3

mind that the conservative approach to determine the shift between suppressed/released (and visa versa) could have some effect on the result. Since most ashes (71 %) started, as saplings, in release and most beeches (76%) started under suppression, the conservative approach could create an "added effect". However, since most trees experienced both suppression and release this effect, to a large extent, should be counter-balanced, because the conservative mechanism works both "shifting-ways" (suppression/release, release/ suppression). I assume that the total effect is limited and about equal for both species. The different growth patterns discovered can be interpreted in terms of competitive "strategies" of ash and beech. The "recruitment strategy" of ash can be described

Test

7.2

T

9.4

T* T *** U ** U *** U **

7.1

ns

as a "rush strategy", to establish immediately in new gaps and then rush towards the canopy. The strategy of beech can be described as a "stop and go strategy", to establish and survive and then slowly, step by step, approach the canopy. The growth patterns and competitive strategies of ash and beech, as concluded from the results, are exemplified in Fig. 2 and 3. The chosen beech (Pig. 2) had two periods in distinct release with a period of> 50 yr of suppression in between. The diagram shows how this beech tree has been able to react with pronounced diameter growth after many years of consecutive suppression. The chosen ash (Fig. 3) started with a short period of suppressed growth before it grew into a long period of released growth.

50 .,.....,--------..~---_ . _---~."~~~"-~-~.---~'~-----~~----~...,

45 4035"" 30·

'#.

25"

20 15 10

5

o..

+ ------1-_ _

o

1

2

3

Number of suppression periods (Ns) Fig. 1. Growth patterns of canopy recruits (as defined in the methods section), of ash Fraxinus excelsior and beech Fagus sylvatica. The diagram shows the frequency distribution across the number ofexperienced suppression periods (Ns) for ash (white) and beech (black).

62

ECOLOGICAL BULLETINS 52, 200?

Beech (core 4-78)

4

7 10 13 16 19 22 25 28 31 34 37 40 43 46 49 52 55 58 61 64 67 70 73 Tree-ring no.

Fig. 2. The growth patterns of a beech tree Fagus sylvatica, selected from the material to illustrate the typical growth pattern and competitive strategy of beech, as concluded in the study. The dotted line indicates the threshold between suppression and release (1.9 mm yr- I ). The tree-ring number (counted from the core) is given on the x-axis, and the radial stem growth for each tree-ring is given at the y-axis (in mm).

Ash (core 35-a8) 9

8 7

E6

S

:5 5 ;:

~ 4

en

:!

"a::

m

3

2

o 4

7 10 13 16 19 22 25 28 31 34 37 40 43 46 49 52 55 58 61 64 67 70 73 Tree-ring no.

Fig. 3. The growth patterns of an ash tree Fraxinus excelsior, selected from the material to illustrate the typical growth pattern and competitive strategy ofash, as concluded in the study. The dotted line indicates the threshold between suppression and release (1.5 mm yr- 1). The tree-ring number (counted from the core) is given on the x-axis, and the radial stem growth for each tree-ring is given at the y-axis (in mm).

ECOLOGICAL BULLETINS 52, 2007

63

The results, including the "rush strategy" of ash and the "stop and go strategy" of beech, are in concordance with the growth patterns expected for ash and beech according to the suggested model ofthe forest cycle, including climax micro-succession from ash to beech. However, this conclusion should not be brought too far. Other flCtors, patterns and processes could theoretically lead to similar growth patterns, than the direct interaction between ash and beech, as suggested by the model. This study was not spatially explicit, which means (as an example) that it is not possible to conclude that the "stop and go" growth patterns of beech trees, generally occur under ash canopies (and gaps), as suggested by the forest cycle model. Field observations suggest that beech in many places develop under ash canopies, bur it is equally clear that beech also can survive in the sub-canopy layers under beech (Nielsen and Hahn 2007). The profile diagrams and discussions of Nielsen and Hahn (2007) provide a good basis for evaluating the structure and competitive environment in the sub-canopy layers in Suserup Skov, as a basis for more detailed and nuanced discussion of the competitive interactions among tree species. They conclude that the light-conditions, competitive environment and dynamics at the forest floor and in the under-storey are, indeed, very complex and irregular. This must be kept in mind when trying to derive generalities about the Suserup ecosystem. Despite the clear and significant differences in the growth patterns ofash and beech, the results also point to a large individual flexibility within both species. Considering the suggested rush strategy of ash, it is interesting that many ash trees actually had experienced substantial periods of suppression (often> 20 yr) before release. This is only possible due to the well known shade tolerance of ash in youth (Gia 1927, Gardner 1975, Mayer 1980). The initial shade tolerance of ash decreases with age (Mayer 1980), which is considered as a typical gap specialist feature (Oldemann 1990). Ts/Tr+Ts for ash decreases with age-class (Table 2) as well as with height-class (Table 3), which could reflect the ceasing shade-tolerance of ash with age/height. Beech shows a much more stable and consistently high Ts/Tr+Ts ratio across age- as well as height classes (Table 2 and 3). In fact, the result indicate that the cessation of shade-tolerance of ash might be more strongly correlated to height than age, since T')/Tr+Ts, for ash, decreases much more with height (Table 3) than with age (Table 2). This conclusion is supported by the tlnding of ashes that proved to survive a period of up to 61 yr under suppression. The shade tolerance ofyoung/small ashes enables ash to establish in advance and compete with genuine shade tolerant species; a competitive advantage especially in the case of slowly developing gaps e.g. under degenerating trees (Emborg 1998, Emborg et aL 20(0). Interestingly, and in line with the results of the present study, Wolf et aL (2004) in a study of mortality in Draved Skov (a seminatural temperate deciduous forest in western Denmark) found that slow growth (diameter increment) increased

64

the risk of "standing death" for all tree species studied (including beech and ash) - and that ash with larger diameter (DBH) even had an increased risk. 'rhe ceasing shade-tolerance with age/height for ash represents a possible explanation behind these results. Einhorn (2007) discusses the strategies of ash versus beech in the first two growth seasons after establishment. She concludes that ash during the first growth season "invests" most resources into the development of a strong root system - in order to rush (explosively) upward, ahead of beech (and other competitors) in the following years. Beech, on the other hand invested more resources in horizontal growth, i.e. developing branches and shade-leaves rather than a fast growing top shoot. These results fit nicely with the competitive strategies of ash and beech as saplings and onwards, suggested in the present study. Ash grows according to Rauh's growth model (Oldemann 1990), a rhythmic growth pattern favouring a rapid height growth with a straight orthotropic stem typical for early successional species. The frequent seeding of winddispersed, light seeds and the rush recruitment strategy of ash reflects a light demanding early successional species, while shade tolerance in youth reflects an intermediate successional species (Oldemann 1990). This, in combination with the results of the present study, suggests ash to be regarded as a typical early/intermediate successional species, or more precisely a gap specialist species, with an initial shade tolerance, that decreases with increasing age/or size. Beech grows according to Troll's growth model (Oldemann 1990), which means that all axes are plagiotrophic. Leaves can easily be pushed in lateral direction to intercept rays of (the scarce) through-falling light. This growth pattern is typical for late successional species (Oldemann 1990). Beech has heavy seeds concentrated in mast years, a long life and a relatively slow growth rate (Oldemann 1990). The stop and go recruitment strategy of beech reflects a typical shade tolerant species, capable of reaching the canopy in the absence of (larger) gaps (Canham 1988, 1989, Veblen 1992). For an overall consideration, beech can be regarded a typical shade-tolerant, late successional or "climax" species.

Long-term co-occurrence of early and late successional species The specific example from Suserup Skov shows some of the possible forest dynamics behind the long-term co-occurrence of early and late successional tree species in late successional (climax) forest. Results from a small-scale pollen record from the studied plot in Suserup Skov indicate that ash and beech have co-occurred for> 2500 vr (Hannon et al. 2(00). During this period, the natnr;l conditions, disturbance regime and human impacts have changed considerably as summarised by HeilmannClausen et al. (2007). Despite the historical impact from

ECOLOGICAL BULLETINS 52, 2007

humans, Suserup Skov is now increasingly characterized by natural disturbance dynamics. Climax micro-succession as described in Emborg et a1. (2000) and supported by the dendro-ecological results of this study, offers part of a possible explanation of the long-term co-occurrence of ash and beech in Suserup Skov. Pollen and macrofossil studies of Suserup Skov show that the forest has never been com-

pletely cleared, but periods of relatively open and light forest conditions have inter-changed with periods of more dense and dark forest conditions (Hannon et al. 2000). Landscape historical studies show how Suserup Skov since its enclosure against grazing livestock around 1800 has changed from a relatively open condition to the present densely stocked and dark condition (Fritzb0ger and Emborg 1996). The recent ecological studies (Emborg et al. 1996, Emborg 1998, Emborg and Heilmann-Clausen 2007) do not indicate that ash is disappearing or retreating from the ecosystem, even though the forest has become darker. In fact, ash currently seems to expand (together with sycamore maple Acer pseudoplatanus and lime Tilia platyphyllos) at the expense ofbeech. Detailed studies of the disturbance history of, and impacts on, Suserup Skov are needed for a more thorough and specific discussion of the long-term co-occurrence of early and late successional species here. A specific study of the occurrence and size of canopy gaps in the sample area and time period covered in this study has not been carried out. Generally the gaps in Suseup Skov seem to be relatively small, in the scale from < 100 m 2 up to ca 0.2 ha (Emborg et a1. 2000). Occasionally large disturbances might account considerably to the ability ofash to maintain a persistently high representation in the forest. In 1967 Suserup Skov was hit by a hurricane that created several large gaps the largest up to about 1.5 ha (Emborg et al. 1996, 2000). However, none of these large gaps occurred within the sample area of this study. The 1999 hurricane (Bigler and Wolf 2007) created a number of new gaps, some of them rather large, which should promote establishment of ash and favourable conditions for successfully performing the rush strategy. The study of Bigler and Wolf (2007), and several other studies that touches on the natural disturbance regime and gapformation in Suserup Skov (Emborg et al. 1996, 2000, Emborg 1998, Emborg and Heilmann-Clausen 2007, Nielsen and Hahn 2007), clearly show that a huge variety ofgap-types and -sizes occur in Suserup Skov - from slowly degrading old trees, over rather sudden single-tree fall of large canopy trees (e.g. due to rot and/or wind) to large gaps created by storm or e.g. Dutch elm disease (Christensen et al. 2007). It seems evident from the present study, in combination with the above cited literature that various-scale gap-dynamics contribute to the long-term survival of ash as well as beech in the Suserup ecosystem. This conclusion does not reject that climax micro-succession from ash to beech could be important as well. Similar patterns of long-term co-occurrence of pioneer and climax tree species have been described in other tem-

ECOLOGICAL BULLETINS 52,2007

perate mixed deciduous forests (Watt 1925, 1947, Forcier 1975, Grubb 1977, Remmert 1985, 1987, 1991, Wissel 1991). In Harvard Forest, those species growing immediately to the over-storey after a disturbance, were distinguished from those stratifYing beneath, later accelerating (in gaps) to the over-storey (Oliver and Stephens 1977). Quercus rubra was characterised by a constant steady diameter growth, like ash in Suserup Skov (Fig. 3). Acer rubrum followed a stepwise growth pattern, indicating a series of crown suppressions and releases, like beech in Suserup Skov (Fig. 2). Piovesan et a1. (2005) explains how the shade-tolerance of beech, adapted to a frequent, small-gap disturbance regime explains how it as a species (under certain circumstances) can dominate and exclude other species from the ecosystem (as also suggested by Poulson and Platt 1989). The results of the present study suggest that this is not about to happen in the case of Suserup Skov. Stewart and Rose (I990) studied the competitive interaction between Nothofizgus menziesii and N fUsca in New Zealand. They concluded that differences in the two species "life history strategies" (including shade-tolerance, juvenile mortality, and growth rates) could explain their long-term co-existence at the site -~ rather than the "regeneration niche" as suggested by Grubb (1977). In Suserup Skov it seems to be the case that differences in the regeneration niches (as discussed by Emborg 1998), the establishment and early competitive strategies (as discussed by Einhorn 2007) as well as differences in the "life history strategies" between ash and beech contributes to the possible coexistence of the species in a late successional ecosystem. Based on the above discussion two overall conclusions can be drawn: 1) that climax micro-succession, under certain conditions, represents a possible explanation of longterm co-occurrence of early and late successional tree species, and 2) that the studied example from Suserup Skov confirms the general impression across the worlds temperate forests (Rohrig and Ulrich 1991) that different species play similar roles - the overall dynamics are the same, even though the taxa differ.

Implications for research and management Through this study of a large number of tree-ring samples from Suserup Skov it was possible to document clear and significant differences in the general growth patterns ofash and beech. However, the material also documented a rich variation in growth patterns within each species, due to variation in specific historical, environmental and competitive impacts having influenced each individual tree. Within the studied material it was in fact possible to find beech trees with a tree-ring record that resembled the typical ash record, e.g. a "lucky" beech tree that got the chance to rush straight towards the canopy. Likewise it is possible to find ash trees that succeeded to approach the canopy through several stop and go actions. The extreme and detailed vari-

65

ation and the role of chance, randomness and unpredicta~ bility should be kept in mind whenever trying to generalize, construct models or predict rules about forest ecosystems. A spatially explicit dendro-ecological study or detailed long-term permanent plot studies could provide interesting insight on how the competitive interaction among individuals of ash and beech plays out in more detail. The differences in the growth patterns and ecological features ofdifferent tree species, as reflected in the structural dynamics of natural forests, can be utilised in forest management. The interplay between shade-tolerant "climax" species and less shade-tolerant gap-specialists, as described in this study, might serve as a source of inspiration for development of specific nature-based forest management systems. As an example, ash could be managed as a gap-specialist species (e.g. groups of ash in a matrix of beech-dominated forest) rather than a pioneer species managed in pure stands. In suitable places, a first step might be to introduce groups of ash trees in presently pure beech stands to create a potential for (nature-based) management of ash-beech stands by mimicking climax microsuccession from ash to beech in gaps. Acknowledgements - This project was supported by The National Forest and Nature Agency, The Danish Academy of Science and The Danish Forest and Landscape Institute. I would like to thank the owner of Suserup Skov, Sow Akademi, represented by Jens Thomsen for help and permission to do research there, Jacob Heilmann-Clausen, Flemming Nielsen and Jens Zofting-Larsen for good hours spent on field work, and Lise Bak for counting tree-rings. Further, I am grateful to Henrik Stryhn for advice on the statistics and J. Bo Larsen, Henrik Vejre, Merete Morsing, Jens Dragsted and others for constructive and useful comments on the manuscript.

References Bigler,]. and Wolf, A. 2007. Structural impact of gale damage on Suserup Skov, a near-natural temperate deciduous forest in Denmark. - Eco1. Bull. 52: 69~80. Bormann, F. H. and Likens, G. E. 1979. Catastrophic disturbance and the steady state in northern hardwood forests. Am. Sci. 67: 660-669. Canham, C. D. 1985. Suppression and release during canopy recruitment in Acer saccharum. - Bull. lorrey Bot. Club 112: 134-145. Canham, C. D. 1988. Growth and canopy architecture ofshadetolerant trees: response to canopy gaps. Ecology 69: 786795. Canham, C. D. 1989. Different responses to gaps among shadetolerant tree species. Ecology 70: 548-550. Canham, C. D. 1990. Suppression and release during canopy recruitment in Fagus grandifllia. - Bull. Torrey Bor. Club 117: 1~7. Christensen, M., Emborg, J. and Nielsen, A. B. 2007. The forest cycle of Suserup Skov revisited and revised. - Eco1. Bull. 52: 33-42.

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Clements, F. E. 191 G. Plant succession: an analysis of the development of vegetation. - Pub!. no. 242, Carnegie Inst. of Washington, Washington DC. Cook, E. R. 1987. The decomposition oftree-ring series for environmental studies. - Tree-ring Bull. 47: 37~~57. Einhorn, K. S. 2007. Growth and photosynthesis of ash Fraxinus excelsior and beech Fagus sylvatica seedlings in response to a light gradient following natural gap formation. - Eco1. Bull. 52: 147-165. Emborg, J. 1998. Understorey light condition and regeneration with respect to the structural dynamics ofa near-natural temperate deciduous forest in Denmark. - For. Eco1. Manage. 106: 83-95. Emborg, J. and Heilmann-Clausen, ]. 2007. The structure of Suserup Skov, 2002. The first re-measurement of a long-term permanent plot study of forest dynamics started in 1992.Ecol. BulL 52: 19-32. Emborg, ]., Christensen, M. and Heilmann-Clausen,]. 1996. The structure ofSuserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Landscape Res. 1: 311-333. Emborg, J., Christensen, M. and Heilmann-Clausen, J. 2000. The structural dynamics of Suserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Ecol. Manage. 126: 173-189. Forcier, 1. K. 1975. Reproductive strategies and the co-occurrence of climax tree species. - Science 189: 808-810. Fowler, J. and Cohen, 1. 1990. Practical statistics for field biology.~ Wiley. Fritts, H. C. 1976. Tree rings and dimate. - Academic Press. Fritzboger, B. and Emborg, ]. 1996. Landscape history of the deciduous forest Suserup Skov, Denmark, before 1925. For. Landscape Res. 1: 291--309. Gardner, G. 1975. Light and the growth of ash. -In: Evans, G. c., Bainbridge, R. and Rackham, O. (eds), Light as an ecological factor II. The 16th Symp. of the British Ecological Society, 26-28 March 1974, Blackwell, pp. 557-563. Gia, T. D. 1927. Beitrag zur Kentnis der Schattenfestigkeit verschiedener Holzarten. -- Forsrwissenschafdisches Centralblatt 46. Gleason, H. A. 1926. The individualistic concept of the plant association. - Bull. Torrev Bor. Club 53: 7-16. Glenn-Lewin, D. C, Peet, R. K. and Veblen, T. T. 1992. Plant succession, theory and prediction. Population and community biology ser. 11. - Chapman and Hall. Grubb, P.]. 1977. The maimenance of species richness in plant communities. The importance of the regeneration niche. BioI. Rev. 52: 107-145. Hannon, G. E., Bradshaw, R. and Emborg,]. 2000.6000 years of forest dynamics in Suserup Skov, a semi-natural Danish woodland. - Global Ecol. Biogeogr. 9: 101·~114. Heilmann-Clausen, J. et al. 2007. The history and present conditions of Suserup Skov - a nemoral, deciduous forest reserve in a cultural landscape. - Eco!. BulL 52: 7--17. Mayer, H. 1980. Waldbau aufsoziologisch-okologischer Grundlage. - Gustav Fischer. McCullagh, P. and Nelder, J. A. 1989. Generalized linear models, 2nd ed. - Chapman and Hall. Mclntosh, R. P. 1985. The background of ecology. Concept and theory. Cambridge Univ. Press. Nielsen, A. B. and Hahn, K. 2007. What is beneath the canopy? Structural complexity and understorey light intensity in Suserup Skov, eastern Denmark. - Eeal. Bull. 52: 43~52.

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Oldemann, R A. A. 1990. Forests: elements of silvology. Springer. Oliver, C. D. and Stephens, E. P. 1977. Reconstruction of a mixed-species forest in central New England. - Ecology 58: 562-572. Peters, R. 1992. Ecology of beech forests in the northern hemisphere. - Proefschrift, Wageningen Landbouwuniversiteit Wageningen. Piovesan, G. et aL 2005. Structure, dynamics and dendroecology of an old-growth Fagus forest in the Apennines. - J. Veg Sci. 16: 13-28. Poulson, T. L. and Platt, W]. 1989. Gap light regimes influence canopy tree diversity. - Ecology 70: 553-555. Raup, H. M. 1957. Vegetational adjustment to the instability of the site. - In: Anon. (ed.), Proc. 6th Tech. Meeting, Int. Union Conserv. Nat. and Nat. Resources, Edinburgh 1956, pp. 36-48. Remmert, H. 1985. Was geschieht im KIimax-Stadium? Naturwissenschaften 72: 505-512. Remmert, H. 1987. Sukzessionen im Klimax-System. Verhandlungen der GeseUschaft fur Okologie (Giessen 1986) Band XVI, pp. 27-34. Remmert, H. 1991. The mosaic-cycle concept ofecosystems - an overview. - In: Remmert, H. (cd.), The mosaic-cycle concept of ecosystems. Eco1. Stud. 85, Springer, pp. 1-21. Rc)hrig, E. and Gussone, H. A. 1990. Waldbau auf okologischer grundlage, zweiter band: Baumartenwahl, Bestandesbegrundung und Bestandespflege. - Paul Parey. Rohrig, E. and Ulrich, B. (eds) 1991. Ecosystems of the world 7, temperate deciduous forests. - Elsevier. Smith, D. M. et al. 1997. The practice of silviculture. Applied forest ecology. - Wiley.

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Stewart, G. H. and Rose, A. B. 1990. The significance of life history strategies in the developmental history of mixed beech (Nothoftgus) forests, New Zealand. - Vegetatio 87: 101-114. Troll, C. and Paffen, K. H. 1963. Seasonal climates of the Earth. Weltkarten zur Klimakunde. - Heidelberger Akademie der Wissenschaften, Heidelberg, 2nd cd. 1980. Veblen, T T. 1992. Regeneration dynamics. - In: Glenn-Lewin, D. C, Peet, R. K. and Veblen, T T (eds) , Plant succession, theory and prediction. Chapman and Hall, pp. 152-187. Vejre, H. and Emborg,]. 1996. Interactions between vegetation and soil in a near-natural temperate deciduous forest. - For. Landscape Res. 1: 335-347. Warming, E. 1895. Plantesamfund, grundmek af den 0kologiske plantegeografi. - P. G. Philipsen, K0benhavn, in Danish with English summary. Watt, A. S. 1925. On the ecology of British beechwoods with special reference to their regeneration. Part II, sections II and III: the development and structure of beech communities on the Sussex Downs. - ]. Eco1. 13: 27-73. Watt, A. S. 1947. Pattern and process in the plant community. ]. Eco1. 35: 1-17. Whitmore, T. C. 1989. Canopy gaps and the two major groups of forest trees. Ecology 70: 536-538. Wissel, C. 1991. A model for the mosaic-cycle concept. - In: Remmert, H. (cd.), The mosaic-cycle concept ofecosystems. Eco/. Stud. 85, Springer, pp. 22-45. Wolf, A. et al. 2004. Storm damage and long-term mortality in a semi-natural, temperate deciduous forest. - For. Eco1. Manage. 188: 197-210.

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ECOLOGICAL llUIIEflNS 52, 2007

Ecological Bulletins 52: 69-80, 2007

Structural impact of gale damage on Suserup Skov, a nearnatural temperate deciduous forest in Denmark Jaris Bigler and Annett Wolf

Bigler, J. and Wolf: A. 2007. Structural impact ofgale damage on Suserup Skov, a nearnatural temperate deciduous forest in Denmark. - Ecol. Bull. 52: 69-80.

Suserup Skov, a semi natural, mixed deciduous forest of 19.2 ha in Denmark was on December 1999 hit by the most severe gale ever recorded in Denmark with gusts ex~ ceeding 45 m S-l at a nearby meteorological station. All trees> 15 cm diameter at breast height were monitored and damages were sorted into four categories: fallen, leaning, broken trunk, and crown loss. The role ofspecies, size and structure for the rate and type of damage were investigated. The species and size of the trees were parameters determining the rate and type of damage quite well, and different species play vitally different roles in the storm resistance of the forest system. The observed damages also correlate with the actual developmental stages of the forest. Three topics regarding structural changes were selected for detailed investigation: 1) the build-up of different types of coarse woody debris, 2) the soil disturbance caused by the turnover of the root mats, and 3) the creation of canopy gaps. The gale resulted in a great variety of habitats not occurring under a calm disturbance regime, especially more favourable conditions for shade intolerant species and species favouring exposed mineral soil. This might help to maintain a higher biodiversity better than the fine grained single tree gap mosaic alone. The gale rejuvenated the top soil at one percent of the forest floor and is believed to be an integrated factor in the deciduous temperate forest ecosystem.

J

Bigler (jaris.bigler@sko!ekom.dk), M@llevej 9, DK-4130 Viby 5j., Denmark. -A. Wolf Forest Ecology, Universitiitstrasse 16, ETH-Zentrum, CH-8092 Zurich, Switzerland

Intensively managed, even-aged monoculture stands are the dominating management scheme in northern Europe. Since the introduction of modern forestry in Denmark ca 250 yr ago, this type of forest has gradually replaced stands with a mixture of species and tree generations (Larsen 1997). One advantage of this management scheme is the possibility to develop quite precise models of annual increment and standing volume. This enables forest managers to plan accurately for economic optima and in that way increase the economic value of the forest.

Copytight © ECOLOGICAL BULLETINS, 2007

However, the intensively managed forests are gradually losing economic competitiveness to other investments and therefore more labour extensive systems are needed (Larsen 1997). At the same time the economic losses have increased through the years due to the low resistance of these monocultures to disturbances such as pests, fire and wind throw, as the stands are to a large extent dominated by introduced species and proveniences not fully adapted to the Danish climate (Larsen 1995). Furthermore, the lack of micro climate typical for forest stands

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over large areas might result in a delayed recovery of the forest ecosystem, which further increases costs. A solution to these problems is the change in the management scheme towards nature based silvicultural methods, meaning that the natural dynamics of the forest ecosystem are supported rather than ignored. Therefore the natural dynamics must be understood - also when it comes to rare but extreme events such as wind throw. Where literature is quite comprehensive when it comes to describing wind throw in even aged stands of Norway spruce Picea abies, there are only few studies dealing with the effect on natural stands in Denmark. In general, the severity of gale disturbance depends primarily on the velocity of the wind, but the impact on a forest is additionally influenced by many other factors, such as species, size, local forest structure, phenology (e.g. amount of leaves), variations in the edaphic conditions, weather conditions, stand exposure, and damage by other falling trees (Helles 1983, Konig et aL 1995, Everham and Brokaw 1996, Webb 1999, Gardiner and Quine 2000, Mason 2002, Redde and von Lupke 2004). Following the severe gale, which hit Denmark on December 1999 and caused widespread damage in forests, we studied the effects of gale disturbance in Suserup Skov - a non-intervention forest reserve. The following hypotheses were tested: 1) species and size of the tree are signiflcantly correlated to damage rate and type. 2) Damage by other falling trees and the local forest structure alter the species and size response significantly. Detailed studies of further impact of the gale were done, investigating the soil disturbance caused by the turnover of the root mats, the creation of canopy gaps and the accumulation of different types of coarse woody debris. Finally we discuss the consequences of storms on habitat and species-diversity within natural forests.

Study site Suserup Skov (55°22'N, 11°34'E) is a semi-natural, mixed deciduous forest at the northern side of Lake Tystrup, situated in the central part of Zealand, Denmark. The climate is cool-temperate, sub-oceanic with an annual mean temperature of8.1 °C and an annual mean precipitation of 635 mm with a maximum occurring in July-December (Emborg et al. 1996). The physiographic setting of Suserup Skov is an undulating elevated plateau to the north and ca 10-15% downward slopes toward a lower terrace along the lakeside. The low terrace consists oflacustrine soils, developed through a slow land reclamation process along the lakeside, which is caused by accumulation oforganic material, intermingled with pockets ofsediments rich in clay. The elevated parts are mainly developed from glacial calcareous till (Vejre and Emborg 1996). The forest comprises 19.2 ha, and consists of three parts (A, B and C) with different management history (Emborg et al.

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1996). Part A (10.7 ha), the most undisturbed part (Emborg et al. 2000), is dominated by beech Fagus sylvatica, though ash Fraxinus excelsior and elm Ulmus glabra are also important species. Its dynamic has been described by a model using five phases: degradation (degradation phase), innovation (regeneration phase), aggradation (building phase), early biostatic (mature phase) and late biostatic (ageing phase) (Christensen et al. 1993, Emborg et al. 1996,2000), which were mapped in 1992 (Emborg et al. 2000). In part B (4.9 ha), past management by grazing created open conditions resulting in an oak-dominated Quercus robur canopy layer. Maple Acer pseudoplatanus is most abundant in this part of the forest. Part C (3.7 ha) is situated along the lakeside, and is dominated by alder Alnus glutinosa on the wettest parts and beech on the slightly more elevated sites. In 1992 all trees with a DBH (diameter at breast height) > 29 em were positioned using a 50 X 50 m grid. All trees with a DBH exceeding three cm (n=18451) were noted in 2-cm classes. All data referring to the pre-storm situation (e.g. DBH, numbers, volumes etc.) are based on the 1992 survey (Emborg et al. 2000). All post-storm measurements were carried out in 2000-2001 (Bigler 2002). Further details of measurements and calculations are given in the respective results section.

The gale The gale in December 1999 was a mid-latitude cyclone. The strongest gusts (mean of 3 s) at Flakkebjerg meteorological station (55°19'N, 11 °23'E), an exposed location 13 km southwest ofSuserup Skov, were 45.1 m S-1, and the highest 10-min mean was 27.1 m S-l (Anon. 1999). The wind direction was mainly west. The gale was the strongest ever recorded in Denmark. The precipitation in the month before the gale was less than normal: 15 mm ofrain instead of60 mm precipitation (average 1961-1990) for November in the southern and western part ofZealand (Cappelen and J0rgensen 2000).

Definitions and derived variables All changes in the structure of individual trees are referred to as "damage", but the term does not imply any economic or biological evaluation. When referring to the situation before the storm only trees that in the 1992 survey were> 14 em DBH are included and an increment of one centimetre in DBH since this last survey (seven year earlier) is assumed. The standing volume (SV) of damaged trees was computed per diameter class for ash, beech, oak and the rest of the species pooled, using the following equation: SV = BAx hx f

ECOLOGICAL BULLETINS 52, 2007

The basal area (BA) was calculated for each DBH-class. The height (h) was estimated using a graphically heightl DBH-relation for oak and individual height/DBH-regressions (h j = a X (OBH/(OBH j + b))3 + 1.3) for beech, ash and "other species", all derived for Suserup Skov by Emborg et al. (996). The form factor (f) was derived from the Danish standard volume functions (Madsen 1987).

Results and discussion

Table 1. List of additional collected data, depending on the type of damage. Geographical orientation of fall a Length of tree Fall type (rotational or hinge) according to Beatty and Stone (1986)a Angle between forest floor and trunkb Height of breaking poinf % Crown lossd If the tree was afallen, bleaning, csnapped or experienced dbranch loss.

Disturbance to structure All trees damaged during the gale with a DBB exceeding 15 em were recorded. The position of the tree as well as the orientation of the debris (based on the 50 X 50 m grid previously constructed) was noted on a map. Species, DBH and vitality status of the tree (dead or alive at the time of the gale incident) was noted. The cause of fall was judged from the mark<. on the damaged trees and from the sequence of the fallen logs, resulting in the subsequent assignment to two categories: 1) direct wind damage or 2) indirectly damaged by another falling tree. For the last category the identity of the damage causing tree was noted as welL For 12 trees out of421 damaged, the cause ofdamage could not be determined. Additional data were collected depending on damage type, Table 1. Ifthe roots were broken at the base ofthe stem, the tree was classified as snapped tree. In the entire Suserup Skov 421 trees (> 15 em DBH) were damaged, representing a BA (basal area) of 101.4 m 1 • The damage rate of the seven most abundant tree species is shown in Table 2. The damage rate differs among species; note especially the absence of damages among alder and the rather high damage rate oflime Tilia platyphyllos. The mean DBH of the species does not explain the differences in damage rate. The distribution of damage types for each species is presented in Fig. 1. The difference in damage type distribution among species was highly sig-

niflcant (X 2 = 52.97, OF = 18, P < 0.0001), with a low uprooting-proportion for oak compared to the rather high proportion of beech, lime, and elm. The mean DBB (all species) differed between damage types (Table 3), whereby larger trees suffer mainly from crown loss and the smaller trees end up leaning (ANOVA,

p
Table 2. Damage rate and mean DBH of the trees damaged by the gale at 3 December 1999. "Other" includes: one fallen horse-chestnut Aesculus hippocastanum, one fallen birch Betula pendula, one fallen and one leaning cherry Prunus avium and one fallen mountain ash Sorbus aucuparia. Species

Number of trees prior to gale

Number of trees damaged in gale and damage rate (%)

Mean DBH (em) of damaged trees

Beech Elm Ash Alder Oak Maple Lime Other Sum

2492 1198 1035 444 H31 156 48 208 5762

240 (9.6) 63 (5.3) 70 (6.8) 0(0.0) '15 (8.3) '16 (10.3) 10 (20.8) 5 (2.4) 419 (7.2)

33.9 19.9 32.1 32.8 96.5 23.9 30.3 19.9 30.4

ECOLOCICAL BULLETINS 52, 2007

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~

CD

C)

(2.7)

60

ro E ro

fZl Crown loss

6 (30.1)

o Snapped

"'C

-5ro

iii Leaning

40

(J) '+-

~

o

Fallen

~

20

o Oak

Ash

Maple

Beech

Lime

Elm

Fig. 1. Relative distribution ofdamage-types. The labels show the number of trees that suffered from this particular type of damage and in brackets the corresponding total basal area (m 2). The species are sorted after increasing proportion of uprooting (leaning + fallen out of total damages).

The direct force of the wind damaged 245 trees (BA 89.1 m 2), whereas indirect damage caused by the fall of another tree, effected 164 trees (BA 11.8 m 2 ), which is equivalent to a ratio of 0.67 indirectly damaged trees for each directly damaged. The overall mean DBH ofthe indirectly damaged trees is only 44% of the DBH of the trees damaged directly by wind (p
The five developmental phases: innovation, aggradation, early biostatic, late biostatic and degradation (Emborg et al. 2000), were analysed in more detail for part A focusing on the three dominant species beech, ash and elm. For beech, the rate of indirect damages is ca 50% in the first stages (innovation - early biostatic) and decreases in the last two stages. For ash the pattern is opposite, with an increasing proportion of indirect damaged trees in the later stages (Fig. 2). Elm is generally more susceptible to indirect damage than beech and ash. In terms of total lost volume per hectare (sum of fallen, leaning and snapped trees all species) the late biostatic phase experiences the greatest losses (214.4 m 3 ha- I ) and the aggradation phase has by far the lowest losses (24.7 m 3 ha- I ), Table 6. The degradation phase appears to be the

Table 3. Mean DBH of the four damage types. The letters a, band c label significant different mean DBH values (ANOVA,

p < 0.001). Damage type

Mean DBH (em)

Standard deviation

Range (em)

Leaning Fallen Broken trunk Broken branch

26.8 a 42.5 b 47.8 b 84.7

3.7

2.6 2.9

15-68 15-144

72

C

5.3

15---204 24·-132

ECOLOGICAL BULLETINS 52, 2007

Table 4. Significance of the logistic regression to test the importance of species and DBH on damage type (GENMODprocedure). If the interaction term size x species was significant, the model was reduced, including only species and size x species to test for the significance of the species effect. If the interaction term size x species was not significant, the model was reduced to test the main factors species and size. Damage type

Site

Species

Species

DBH

Fallen Leaning Leaning Snapped Broken branch Broken branch

A A B A A B

ash, beech, elm ash, beech, elm ash, beech, elm all species beech, lime, oak beech, maple, oak

0.0735

<0.0001

n.s. n.s.

Excluded n.s. Excluded Excluded n.s.

0.0712 0.0617 n.s.

species x DBH n.S. a

0.0390

a

0.0396 <0.0001

n.s. a

n.s.

": as interaction sign. DHB was excluded in the final model, n.s. if p>O.l.

most structurally unstable phase in terms of gap area resulting from the gale, but also the aggregation phase is vulnerable. The relative damage rate of each DBH class (only beech) has a distribution with two peaks: the first weak peak occurs at a DBB around 50 em followed by more storm resistant trees around 80 em. The trees> 80 em DBH experience increasing damage rates, but these rates are constructed on the basis of low numbers, due to the low overall number of such large trees. In the most untouched part A, larger trees had an increased risk to fall due to the gale, independent of species. For other damage types, like breakage of stem or branches, size was also an important factor to determine damage risk, but additionally there was a significant difference between species in their susceptibility to those types of damages. This is probably caused by species differences in tissue strength and flexibility. Damage rate were further closely correlated with the phase of the cyclic dynamics of the f()rest, and the structure developed according to these dynamics (Tables 3, 4, 6, Fig. 1). The correlation between size and damage type was less strong in part B, but the irregular DBH distribution caused by the former higher rate of human interference (Emborg et al. 1996) might influence these results. A gradient exists between species, which tended to break above ground and species more likely to suffer from failure in root anchorage. As we did not study the rooting depth of the trees that were still standing after the gale, we can only speculate that higher rooting depth decrease the uprooting risk for a tree, bur increases the risk for break..'1ge.

But placement of species in one or the other end of the scale (Fig. 1) was also found in other studies (Andersen 1954, Allen 1992, Wolf et al. 2004). The loss of crown parts or major branches is known to be a typical damage for oak (GandilI932, 1934, Cutler et al. 1990). In Suserup this effect was more pronounced than expected as there have been mainly large oaks found (Emborg et al. 1996), and the largest trees are the ones that suffered most from crown loss, which was also found in Draved Forest (Bigler 2002), another mixed deciduous forest in Denmark. The large size of oaks also explains why no oak was found leaning after the storm, as a large uprooted tree is more likely to be drawn down to the ground by its own weight. The opposite pattern with a lot ofleaning trees was observed for elm, which is mainly due to the rather large population of relatively small elm trees found in Suserup (Emborg et al. 1996). Interestingly, alder was not harmed at all despite its exposed position close to the lake and the moist soil conditions. The constant wind exposure could have lead to a structural adaptation (Andersen 1954) bur deep rooting (0dum 1980) and former coppice management (Christensen et al. 1993, Emborget al. 1996) might also be contributing factors. Trees of any size could cause damage to smaller trees. Nevertheless, larger trees tend to damage a higher number of trees. The mean DBH of the indirectly damaged trees was only 44% of the mean DBH of the directly damaged ones. This notable difference was also found by Clinton and Baker (2000) in a study from the southern Appalachians. The shifting dominance of the canopy layer from ash to beech during the forest cycle and the role of elm as an

Table 5. DBH of trees damaged directly by the wind pressure ("Direct"), damage causing trees ("Damage makers") and trees damaged by the fall of another tree ("Indirect"). Category Directly hit Damage makers Indirectly hit

ECOLOGICAL lIULLETINS 52, 200?

Numbers

Mean DBH (cm)

Standard error

Range (cm)

245 72 164

58.1 82.8 25.8

2.4 36.2 1.2

15-204 19-192 15-132

73

100

of the forest cycle does also suffer mortality even the trees are younger. We conclude that species and tree size are important factOrs determining the risk of gale damage, as well as the type of damage to the single tree. Large falling trees cause additional damage, by hitting smaller trees. The result of this domino effect depends on the developmental phase of the forest, but under storey species like elm constantly suffers from these indirect damages.

80 (l)

OJ (1j

E (1j "0

60

'0

~

is

~,

Elm

-----

~Ash

...----

.!::

'0

~Beech

:#

Aggradation

Early biostatic

Late biostatic

Accumulation of dead wood

Degradation

Fig. 2. Proportion ofindirect damage to beech, ash and elm in the

last four phases. understOrey species (Emborg et al. 2000), is reflected in the rates of indirect damage of the three species (Fig. 2). We found an increased risk of damage with increased tree size (Table 4), a result supported by Ida (2000) and also found on stand scale in Switzerland (Dobbertin and Seifert 2000), United Kingdom (Andersen 1954), North America (Foster 1988, Webb 1989, 1999) and east European boreal forest (Ulanova 2000). Other studies showed a different pattern, for example a bell-shaped distribution of damage risk, with intermediate sized trees being most vulnerable (Falinski 1978, Pontailler et al. 1997), but the last survey used total and not relative damage numbers. In some studies, the risk-size relationship was also depending on the damage type (Peterson 2000, Wolfet al. 2004). The increased risk of damage with size is explained, by the increased exposure of taller trees. Another important aspect is tree age, which is higher in larger trees and hence senescence and an increased risk of stem rot are of potential importance. It is very likely, that there are differences between species and sites in the importance of those risk factors. Consequently, the precise composition of species, the soil conditions and tree growth prior to the gale could explain the differences in response pattern between the studies (Webb 1999, Gardiner and Quine 2000, Wolf et al' 2004). Table 6 demonstrates that damage in terms of volume in general follows the volume build-up through the phases. But in terms ofgap area and number oftrees the first stages

The snag volume was calculated as the cylinder, based on basal area, times the height to breaking point of fracture. The standing snag volume of trees with 100% crown loss was calculated as the lower 2/3 of a cone based on the DBH and the height of the tree derived from the relevant height/diameter-regression. The coarse woody debris (CWD) volume deposited on the forest floor resulting from these trees where calculated as the deficit between total tree volume derived from volume tables and the standing snag volume. Neither stem volume nor crown parts from trees with < 100% crown loss where included in the calculations. In the entire forest 112 broken trees resulted in 94 snags above a height of05 m (Table 7). The mean standing snag volume was 8.5 m 3 ha- 1 of which ca 65% was beech, 20% oak and 15% ash. The mean size per tree was 1.7 m3 , but 6.6 m 3 for oak. 4.9 snags per ha seem rather low compared to the provisional benchmark,; for dead wood in British forests, where 0-10 standing snags per ha is categorised as "low" (Kirby et al. 1998). As we only know the number of snags resulting from the most recent storm and lacking information about the pre storm situation the numbers are not directly comparable. But the low number of snags caused by even this severe gale leads to the conclusion, that gales are not the major factor creating snags in Suserup. Snag creation is rather a continuous process of slow decay of standing trees (Barden 1981). Nevertheless, indirect damage and cascade effects resulted in a concentration of damages in certain areas and hence influencing the spatial distribution of snags, which is not typical in periods between two gales.

Table 6. Impact of the gale on the five phases of the forest cycle (Emborg et a!' 2000). All fallen, leaning and broken trees are included, but not the trees suffering from crown lossl since they are expected to survive. Phase

Innovation Aggradation Early biostatic Late biostatic Degradation Total

74

Area in the 1992survey (ha)

(% of phase area)

Volume fallen l leaning or broken (m 3 ha-1) and number (n ha- 1)

0.2 2.3 4.0 3.3 0.6 10.4

0.008 (4.1) 0.512 (22.3) 0.508 (12.7) 0.583 (17.7) 0.186 (31.1) 1.797 (16.8)

128.6 (20.0) 24.7 (38.3) 57.6 (28.0) 214.4 (29.7) 119.4 (35.0) 102.1 (30.2)

Gap area (ha)

ECOLOGICAL BULLETINS 52, 2007

Table 7. Three types of dead wood resulting from the gale: standing snags, trees lying on the ground and trees leaning in other trees. The category /lTop part of snapped trees" covers the trees broken beneath 0.5 m and the top parts from the snapped trees with a standing snag higher than 0.5 m. Numbers shown are volume (m 3 ha-1) and in brackets number (ha-1). Position of CWO

Origin

Part A

Part B

Part C

Whole forest

Lying Lying Leaning Standing

Top part of snapped trees Fallen Leaning Standing snags> 0.5 m height Sum

18.8 (0.6) 57.1 (13.5) 4.1 (5.8) 9.4 (6.6) 89.3 (26.4)

37.9 (2.0) 11.1 (3.3) 1.7 (1.6) 10.8 (4.1) 61.5 (11.0)

10.0 (0.5) 13.2 (2.7) 1.7 (0.3) 2.9 (0.8) 27.8 (4.3)

22.0 (0.9) 37.0 (8.8) 3.0 (3.7) 8.5 (4.9) 70.5 (18.3)

The total volume of lying coarse woody debris ranged from 27.7 m3 ha- 1 in part C to 78.9 m 3 ha- 1 in part A and the total volume ofleaning trees from 1.7 m 3 ha- I in part B and C to 4.1 m3 ha- 1 in part A (Table 7). Beech dominated, but the distribution among species reflects the composition of the different sites. The volume is high compared to the total volume including CWD before and after the gale of 163 m 3 ha- I which was measured in 2002 using a line transect method (Christensen et al. 2005). Nearly half of this volume was created by the gale bringing the volume up considerable above provisional British benchmarks values where 40 m 3 ha- I is considered a high volume, oldgrowth temperate deciduous forests values ranging from 46 m3 ha- I to 132 m 3 ha- 1 (Kirbyet al.1998) and the average of 134 m3 ha- 1 (range 33-284) of18 beech dominated European lowland forests (Christensen et al. 2005). The snag volume may not be severely affected by the gale since snags are regularly produced over time due to wood decaying fungi. The volume of lying CWD on the other hand is often boosted considerably after a severe gale. Another typical gale feature is the accumulation of CWD in certain areas due to cascade effects. In the near future even more CWD might be added in these areas due to the increased exposure to wind of gap cornering trees. This concentration of snags and lying CWD is of substantial importance, especially for invertebrates and fungi with limited dispersal capabilities. CWD found aggregated rather than uniformly scattered over the forest meet the requirement of those species better (Samuelsson et al. 1994).

Disturbance to soil Mound height, mound thickness and mound diameter were recorded for fallen trees. The type ofthe deepest lying soil horizon exposed by the falling tree was assessed using the guidelines ofFAO-UNESCO (Anon. 1990) whereby divisions were only made between an A-horizon, a B/Ehorizon and a C-horizon. The A-horizon is characterised by a dark colour resulting from the mixture of organic matter and the mineral soil, the C-horizon by mineral soil not disturbed by the weathering processes and the B/E horizon is placed in between A and C.

ECOLOGICAL BULLETINS 52.2007

Distinction was made between "rotational" and "hinge" fall types according to Beatty and Stone (1986). The rotational type was characterised by root breakage in the leeward side and the root ball is functioning as a ball bearing resulting in the mound placed inside the pit. The hinge type is characterised by the leeward roots resisting breakage and functioning as a hinge and the mound is therefore placed outside the pit. "Mound height" was defined as the vertical distance from mound top to the bottom of the mound, mound diameter is the horizontal distance between the outermost parts of the mound where soil is intruded between the roots and mound thickness is the greatest distance at a right angle between the former forest floor and the exposed mineral soil at the opposite side. The vertical area of the mound was calculated as half an ellipse based on mound diameter and mound height. In the case of hinge fall type, the root mat volume was calculated as a half cylinder assuming that the complete root plate is ofan equal thickness (Beatty and Stone 1986). In the case of rotational fall type the root mat volume was calculated as one quarter of an ellipsoid because the shape of the root mat resembled more a rounded ball than a plate. The root plates created by the simultaneous fall of more than one individual with DBH exceeding 15 cm were left our of the calculations of average sizes, as it was difficult to divide the common root plate into fragments originating from each of the different trees. When calculating the total area and volume, these collective root plates as well as the ones resulting from the fall of standing dead trees were included in the calculations. All together 197 trees created mounds. In 11 cases the forest floor was elevated but not cracked, and therefore thickness was not measured. The most common species to create root mats was beech (122 root mats produced = 6 ha- 1), followed by ash (n=26, ca 1 ha~l) and elm (n=22, ca 1 ha- I ). The largest volume turned over by a single tree was 28.8 m 3 - a rotational fall of a beech, and the smallest rotational fall was an elm with a volume of only 0.014 m 3 • Hinge fall mound volumes ranged from 22.1 m3 (beech) to 0.0073 m 3 (ash). A summary of mount volume and pit area for the three parts of the forest are given in Tables 8 and 9. The average mound volume after fallen living trees

75

Table 8. Mound volume (m 3 ha-1 ) and in brackets number of mounds (ha- 1 ). Site

Part A

Part B

Part C

All

Rotational type Hinge-type Sum

44.7 (12.8) 3.5 (1.0) 48.2 (13.8)

4.2 (3.1) 1.0 (1.2) 5.2 (4.3)

5.8 (1.6) 0.0 (0.0) 5.8 (1.6)

26.9 (8.2) 2.2 (0.9) 29.1 (9.1)

was 3.3 m 3 (derived from 180 trees with a mean DBH of 41.1 em) and the corresponding average mound after dead trees was only 0.98 m 3 (derived from six trees with a mean DBH of75.0 em). The pit area created by a rotational fall was positively linearly correlated with the size of the falling tree (pit-are~ecch ::= 0.33 X DBH i - 4.32, R2::= 0.83, only beech). The number of trees falling according to the hinge type was too low to get a significant correlation. The DBH was correlated with the volume of the root mats of the rotational (mound-volumebeech = 0.001 X DBH j 2.0271, R 2 == 0.70) and hinge falls. Using the entire data set, the mean root mat volume of the rotational-type significantly exceeded that of the hinge-type (F == 39.18, DF = 1, P < 0.0001) even if the data were corrected for tree size (DBH) and species. The geographical orientations of the fallen trees exhibited bell shaped curves around a peak at 62°E (Fig. 3). This resulted in 50Q'O of the former forest floor sides of the root mats facing within 17° and 90% to face within 47° to each side of the mean. The exposed mineral soil sides on the other side of the root mats naturally performed a similar pattern and are oriented to the W around a mean value of 242°. In 62% of the uprooted trees, the exposed soil reached down to the B horizon, deeper uprooting was observed in 27% and only in 11 % of all uprooted trees the deepest horizon was an A (Table 10). Large amounts of soil were turned over by large single trees, bur the variation of mound size between individual trees was enormous. The larger mounds were generally created by the rotational fall of large beech trees. In contrast, the mean mound volume of dead trees was much smaller than the mean mound created by a living tree, especially if corrections for DBH of the trees were made. This is supported by Lyford and MacLean (1966) and underlines the importance of gale induced wind throw for the rejuvenation of the top soil layer. When comparing the root plate radii and root plate thickness of Suserup with a survey from Great Britain

(Cutler et al.l990) and Draved Forest, Denmark (Bigler 2002) we find Suserup to be between the two other surveys. It seems that root plate radii is positively related to shallowness of the rooting, which in turn might be determined by the soil moisture conditions as for most tree species root growth is low in soils with even temporary water saturation (Ellenberg 1996). The rotational and the hinge fall type create different microsites; the hinge type pit has no root mat and the entire soil volume is displaced to the forest floor (Beatty and Stone 1986). This might be an important feature in a moister ecosystem where the mounds would assemble "islands" of drier conditions in a "sea" of moist soil (Lyford and MacLean 1966, Beatty and Stone 1986). However, the majority of Suserup Skov is placed on well drained soils, and the hinge fall type was not abundant. The most important effect of the mound and pit creation in Suserup is therefore the exposure of mineral soil and the rejuvenation of the soil (Lutz 1940), influencing the regeneration (Lyford and MacLean 1966, Beatty and Stone 1986), the mean temperature (Millikin and Bowden 1996), the daily and yearly temperature amplitude (Lutz 1940, Beatty and Stone 1986), and even the deposition of seeds seem to be lower (Clinton and Baker 2000). The creation of mounds may have a strong influence on the future forest composition (Clinton and Baker 2000) by favouring pioneer species such as birch (Lyford and MacLean 1966, Rohrig 1991). Yet, not only the diversity of trees and shrubs is increased due to the turnover ofsoil, but also shade intolerant ground floor species can be found on soil held by roots in south facing gaps (Schnitzler and BorIea 1998), and the number of bryophyte species were found to be higher at mounds compared to the undisturbed forest floor Qonsson and Esseen 1990). The effect of the formation of larger mounds and pits are often long lasting, for example, mound and pit complexes have been found to last up to 500 yr (Stephens 1956) resulting in a hummocky micro-relief. Mueller and Cline (1959) found that most of a forest floor has been

Table 9. Pit area (m 2 ha~l) and in brackets number of pits (hal). Site

Part A

PartS

Part C

All

Rotational type Hinge-type Sum

11 9.8 (13.1 ) 14.0 (1.0) 133.8 (14.'1)

14.6 (3.3) 6.3 (1.2) 20.9 (4.5)

12.9 (1.9) 7.4 (0.5) 20.3 (2.4)

77.4 (8.4) 10.8 (1.0) 88.2 (9.4)

76

ECOLOGICAL BULLETINS 52,

2007

N

Table 10. Proportion (%) of pits exposing the A-, B- or a Chorizon as deepest horizon.

80 NV\(

60

/

NE

Soil horizon

A B C

SE

s Fig. 3. Fall directions of fallen trees, direct or indirect damage.

disturbed by mound creation within the previous 500 yr, suggesting the phenomenon to be a vital part of the forest ~cosystem instead ofa rare event. The strong preference of different species to certain microsites (the unaffected forest floor, the mound and the pit) found by Beatty (1984) also supports the conclusion, that creation of mounds and pits has an important role in forest communities. We conclude, that the creation of mounds and pits by the gale resulted in an increase in the amount ofa variety of habitats compared to the undisturbed forest. The disturbance of the soil seems to be a vital and integrated part of the forest ecosystem.

Part A

Part B

Part C

All

8.6 60.7 30.7

20.8 75.0 4.2

20.0 50.0 30.0

10.9 62.1 27.0

don (Fig. 4) shows a peak at gap sizes of 100 m 2 • The largest gap covered 0.45 ha. Pontailler et al. (1997) found a mean gap size of 175 m 2 in a beech dominated forest in Fontainebleau (France) after a gale of similar magnitude, other authors report larger mean gap sizes from deciduous temperate forests (Clinton and Baker 2000), but the great differences in the assumed minimum gap size could explain the different mean values. A positive correlation between the mean gap area and the time passing between two storms (Pontailler et al. 1997) might also contribute to the different values, as disturbance interval differed between the studies. The creation of large gaps is a typical feature of gale damage (Quine et al. 1999) partly due to multiple tree falls. In Suserup Skova damage-causing gap maker resulted, on average, in the fall of 2.2 other trees, thereby creating larger, multi-tree gaps. The increased structural roughness of the canopy layer once a hole is created will create higher turbulences and therefore induce greater wind forces on the surrounding trees, which might eventually collapse under the increased stress (Allen 1992, Quine et al. 1995). The characteristic of the gap closure is an important factor to determine the future species composition. At very low values ofthe D/H-ratio (diameter ofgap/height ofsurrounding trees) the gap will be mainly closed by the lateral extension of the surrounding trees (Runkle 1990). If the D/H ratio is large enough, the lateral growth will not close

Creation of gaps

On -+--sum of area

16

The area of a gap was defined as the surface delimited by the vertical projection of the edges of surrounding crowns (Runkle 1990, Pontailler et al. 1997). Maps showing the horizontal extension of gaps > 10m2 were constructed based on field observations combined with maps showing the position of single trees. The gaps were cur from the map and weighed on a Mettler scale (type H5, 1 div. = 10 mg) and the weights were used to calculate the gap size. If gaps extended into neighbouring forest parts their total area where included in the calculation of mean size. All together 49 gaps with a mean size of451 m] covered 20.4% of part A immediately after the gale. Of these 49 gaps, four were considered to be old gaps (corresponding to 1.2% ofpart A), three of which had expanded considerably during the gale. The total gap area was 14 times greater after the gale than before the gale. The gap size distribu-

ECOLOGICAL BULLETINS 52, 2007

1.0

,,/

14

~_./

11/

if)

g.

10

OJ

"0 Q;

8

.n

E ::>

z

0.8

1

12

I

6

ro 0.6

/

0.4

£ co ~ co

ro

:§

4 0.2

2

...,.'~..-/ .~/

+-

0 1.5

0.0

2.0

2.5

3.5

3.0

Gap sIZe 10 x m 2

or

Fig. 4. Gap size distribution and total gap area each size class in part A. The x-axis is divided into intervals ono' m 2 , {x", 1.5; 2.0; 2.5; 3.0; 3.5}.

77

the gap and suppressed trees, re-sprouting damaged trees, advanced regeneration or trees originating from seeds will compete to reach the canopy. Here, microclimate and the soil conditions will influence the regeneration and hence future species composition. In Suserup Skov the re-sprouting of a snapped tree is an especially common and temporary successful feature among elm (Emborg et al. 2000). The available sun light at the centre of the gap increases with the D/H ratio and reaches maximum (full daylight) at a value of approximately two (Runkle 1985). The two largest gaps in Suserup exceed this limit assuming the surrounding canopy height to be 30 m and gaps defined as circles. The great heterogeneity ofsolar radiation in gaps in temperate regions contributes to high species diversity (Runkle 1989, Whitmore 1989, Schnitzler and Borlea 1998). Larger gaps generally favour shade intolerant pioneer species and smaller gaps generally favour the climax species (Runkle 1985, Rohrig 1991, Quine et al. 1999, Clinton and Baker 2000). The success of the pioneer species in larger gaps is due to their abundant production of light seeds, their high tolerance of frost and drought and a fast juvenile growth rate (Rohrig 1991). However the seed banks of other species may alter the competitive situation (Connell 1989). Even smaller gaps might have a diverse regeneration as a result of the variety of gap shapes, differences in surrounding canopy height and different exposure to solar radiation due to elevations in terrain. In summary, the gaps created by the gale are often multi-tree gaps and hence larger than the ones created by single trees due to senescence or disease. The structural changes are expected to have considerable influence on the regeneration of the system and the maintenance of a high biodiversity, due to the rise in structural diversity and creation of habitats important for specialized organisms. Many of the different microhabitats do not occur under the "normal" disturbance regime or their frequency and extent are drasticallyaltered by the gales. Perhaps more important, the interaction with the new gale-induced features might lead to new habitats available for specialists (for example sun exposed lying dead wood).

ing trees resulted in additional damage on smaller trees growing in the sub-canopy strata. This in particular resulted in large amounts ofadditional damages among elm, due to the high amount of young elm trees in the sub-canopy stratum. Whether the described increase in available habitats will result in higher species diversity or not, depend among other variables on the available seed sources. A pollen diagram (Hannon et al. 2000) from Suserup tells the story of a past forest on the site much richer in species. The forest we see now with few dominating species is the result of anthropogenic clearance for agricultural purposes at ca 600 BC. On the other hand, species like lime has likely been reintroduced by humans and other new species like maple has arrived to the forest and are expected to expand further (Emborg et al. 1996, Hahn and Thomsen 2007). The result of the combined effect of gale induced structural change and the availability of seed sources of species, that until the gale struck were rare in the system, should be monitored in the years to come. In conclusion, adaptation ofstructure and species composition to the site-specific exposure and edaphic conditions might reduce immediate losses due to gale damage but also secure a faster regeneration ofthe forest ecosystem. And when gales strike managed forests, it might be worthwhile accepting rather than fighting the change in forest structure and the pioneer species adapted to this type of disturbance. Acknowledgements - The authors wish to thank Sam Akademi for permitting research in Suserup Skov, Morten Christensen and Jacob Heilmann-Clausen for their support collecting the data concerning the impact on the individual trees, Ebba Bigler for the great effort with the collection of data concerning soil disturbance and Thomas Christensen, Peter Krogsgaard Kristensen and Christian Anton Rahbck for providing the gap-data. Thanks to Thomas Hansen for great and valuable statistical support. Thanks to the P. W S. Errboes Foundation for financial support to the transport action involved.

References Conclusion and perspectives A strong gale like the one that passed over Denmark 3 December 1999 resulted in serious perturbation to the non-intervention forest Suserup Skov, but still no gaps> 0.45 ha occurred. The adaptation of structure and/or species composition to the site-specific exposure and edaphic conditions seems to secure the resistance of the system, and a total collapse of the forest structure, as monitored in many even aged spruce-plantations (Enevoldsen 2000), was not observed. The damage type and rate depended on tree size and species, and was correlated closely with the actual phase of the cyclic dynamics of the forest. The damage causing fall-

78

Allen, J. R. 1. 1992. Trees and their response to wind: mid Flandrian strong winds, Severn Estuary and inner Bristol Channel, southwest Britain. - Phil. Trans. R. Soc. B 338: 335-364. Andersen, K. F. 1954. Gales and gale damage to forests, with special reference to the effects ofthe storm of 31st January 1953, in the northeast of Scotland. - Forestry 27: 97-121. Anon. 1990. Soil map ofthe world - revised legend. - World Soil Resources Rep. 60, Food and Agriculture Organization of the United Nations. Anon. 1999. Orkanen 3.-4. december 1999 i tal- forel0big version udarbejdet 5. december 1999. - <www.dmi.dk> 1 March 2001. Barden, L. S. 1981. Forest development in canopy gaps of a diverse hardwood forest of the southern Appalachian Mountains. - Oikos 37: 205-209.

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Beatty, S. W 1984. Influence of microtopography and canopy species on spatial patterns of forest understorey plants. -Ecology 65: 1406-1419. Beatty, S. Wand Stone, E. L. 1986. The variety of soil micro sites created by tree falls. - Can.]. For. Res. 16: 539-548. Bigler,]. 2002. Gale damage in Draved forest -- impact on struc~ ture in a near natural temperate deciduous forest. - Part of Master thesis, The Royal Veterinary and Agricultural Univ., Copenhagen. Cappelen, ]. and ]0rgensen, B. (eds) 2000. Danmarks klima 1999 - med till;£g afF;£r0erne og Gmnland. - Trafikministeriet, Danmarks Meteorologiske Inst. Christensen, M., Heilmann-Clausen, ]. and Emborg,]. 1993. Suserup Skov 1992. OpmaIing og strukturanalyse af en dansk naturskov...- Skov- og Naturstyrelsen, in Danish. Christensen, M. et ai. 2005. Dead wood in European beech (Fagus sylvatica) forest reserves. - For. Eco1. Manage. 210: 267282. Clinton, B. D. and Baker, C. R. 2000. Catastrophic wind throw in the southern Appalachians: characteristics of pits and mounds and initial vegetation responses. - For. Eco1. Manage. 126: 51-60. Connell,]. H. 1989. Some processes affecting the species composition in forest gaps. - Ecology 70: 560-562. Cutler, D. F., Gasson, P. E. and Farmer, M. C. 1990. The wind blown tree survey: analysis of results. -- Arboricult. J. 14: 265-286. Dobbertin, M. and Seifert, H. 2000. Erste Ergebnisse des Teilprojektes: Erfassung der Bestandesdaten und Schaden auf dem reprasentativen 4x4-km Sanasilva-Netz. - Eidg. Forschungsanstalt WSL. Ellenberg, H. 1996. Vegetation Mitteleuropas mit den Alpen, 5th ed. - Ulmer. Emborg, J., Christensen, M. and Heilmann-Clausen,]. 1996. The structure of Suserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Landscape Res. 1: 311--· 333. Emborg, ]., Christensen, M. and Heilmann-Clausen, ]. 2000. The structural dynamics of Suserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Ecoi. Manage. 126: 173-189. Enevoldsen, K. 2000. Ny opg0relse: 3,6 millioner m 3 . - Skoven 32: 6--7. Everham III, E. M. and Brokaw, N. V L. 1996. Forest damage and recovery from catastrophic wind. - Bot. Rev. 62: 113-185. Falinski, J. B. 1978. Uprooted trees, their distribution and influence in the primeval forest biotype. - Vegetatio 38: 175-183. Foster, D. R. 1988. Species and stand response to catastrophic wind in central New England, USA - ]. EcoI. 76: 135-151. Gandil, C. 1932. Stormen den 8.-9. juli 1931-- og dens virkninger i danske skove. - Dansk Skovforenings Tidsskrift 17: 3550, in Danish. Gandil, C. 1934. Stormen den 8. februar 1934. - Dansk Skovforenings Tidsskrift 19: 329-373, in Danish. Gardiner, B. A. and Quine, C. P. 2000. Management offorests to reduce the risk of abiotic damage - a review with particular reference to the effects of strong winds. For. Ecoi. Manage. 135: 261-277. Hahn, K. and Thomsen, R.P. 2007. Ground £-lora in Suserup Skov: characterized by forest continuity and natural gap dynamics or edge-effect and introduced species? - &01. Bull. 52: 167~181.

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Hannon, G. E., Bradshaw, R. and Emborg, J. 2000. 6000 years of forest dynamics in Suserup Skov, a semi natural Danish woodland. - Global Ecoi. Biogeogr. 9: 101-114. Helles, F. 1983. Stormskade pa skov ~ en litterarurgennemgang. - Dansk Skovforenings Tidsskrift 68: 247-278, in Danish. Ida, H. 2000. Tredall gap disturbance in an old-growth beech forest in southwestern Japan by a catastrophic typhoon. - J. Veg. Sci. 11: 825-832. Jonsson, B. G. and Esseen, P 1990. Tree fall disturbance maintains high bryophyte diversity in a boreal spruce forest. - J. Ecoi. 78: 924-936. Kirby, K. J. et al. 1998. Preliminary estimates of fallen dead wood and standing dead trees in managed and unmanaged forests in Britain. - J. App!. Ecol. 35: 148-155. Konig, A, Mossmer, R. and Baumler, A 1995. Waldbauliche Dokumentation der flachigen Sturmschaden des Friihjahrs 1990 in Bayern und meteorologische Situation zur Schadenszeit. - Berichte aus der Bayerischen Landesanstalt fur Wald und Forstwirrschaft, N r. 2. Larsen, J. B. 1995. Ecological stability of forests and sustainable silviculture. - For. £col. Manage. 73: 85-96. Larsen, ]. B. 1997. Skovbruget ved en skiUevej - teknologisk rationalisering eller biologisk optimering. - In: Dansk skovbrug i 100 ar. Danske Forstkandidaters Forening, pp. 25-56, in Danish. Lutz, H. J. 1940. Disturbance of forest soil resulting from the uprooting oftrees. -- Yale Dniv. School ofFor. Bull. 45: 1-37. Lyford, W H. and MacLean, D. W 1966. Mound and pit micro relief in relation to soil disturbance and the distribution in New Brunswick, Canada. - Harvard For. Pap. 15: 1-18. Madsen, S. F. 1987. Vedmassefunktioner ved forskellige aHxgningsgr;£nser og n0jagrighedskrav for nogle yigtige danske skovtr;£arter. - Forstlige Fors0gsvaosen Danmark 350: 47-242, in Danish with English summary. Mason, W L. 2002. Are irregular stands more windfirm? - Forestry 75: 347-335. Millikin, C. S. and Bowden, R. D. 1996. Soil respiration in pits and mounds following an experimental forest blow down. Soil Sci. Soc. Am.]. 60: 1951-1953. Mueller, O. P. and Cline, M. G. 1959. Effects of mechanical soil barriers and soil wetness on rooting of trees and soil mixing by blow-down in central New York. Soil Sci. 88: 107-111. 0dum, S. 1980. De vildtvoksende trxer og buske. - In: N0rrevang, A and Lund0, J. (eds), Danmarks natur 6 - skovene, 3rd ed. Politikens Forlag, pp. 143-199, in Danish. Peterson, C. J. 2000. Damage and recovery of tree species after two different tornadoes in the same old growth forest: a comparison of infrequent wind disturbances. - For. Ecoi. Manage. 135: 237-252. Pomailler, J., Faille, A and Lemee, G. 1997. Storms drive successional dynamics in natural forests: a case study in Fontainebleau forest (France). - For. Ecol. Manage. 98: 1-15. Quine, C. et al. 1995. Forests and wind: management to minimise damage. For. Comm. Bull. 114. Quine, C. P., Humphrey, J. W and Ferris, R. 1999. Should the wind disturbance patterns observed in natural forests be mimicked in planted forests in the British uplands? - Forestry 72: 337-358. Redde, N. and von Ltipke, B. 2004. Investigation about risk of storm damage when harvesting single trees in old Norway spruce stands on deeply penetrable soils in the SoIling/Lower Saxony. - Forst und Holz 59: 270-277.

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Rohrig, E. 1991. Vegetation structure and forest succession. - In: Rohrig, E. and Ulrich, B. (eds), Ecosystems of the world (7): temperate deciduous forests. Elsevier, pp. 35-49. Runkle, J. R. 1985. Disturbance regimes in temperate forests. In: Pickett, S. T. A. and White, P. S. (eds), The ecology of natural dismrbance and patch dynamics. Academic Press, pp.17-34. Runkle, J. R. 1989. Synchrony of regeneration, gaps and latitudinal differences in tree species diversity. - Ecology 70: 546--547. Runkle, J. R. 1990. Gap dynamics in an Ohio Acer-Fagus forest and speculations on the geography of disturbance. - Can. J. For. Res. 20: 632-641. Samuelsson, J., Gustafsson, L. and Ingelog, T. 1994. Dying and dead trees - a review of their importance for biodiversity.-Swedish Environmental Protection Agency Report Series, Rep. 4306. Schnitzler, A. and Borlea, F. 1998. Lessons from natural forests as keys for sustainable management and improvement of naturalness in managed broadleaved forests. - For. Ecol. Manage. 109: 293-303.

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Stephens, E. P. 1956. The uprooting of trees: a forest process. In: Monthey, L. G. (ed.), Proceedings. Soil Sci. Soc. Am. 20: 113-116. Ulanova, N. G. 2000. The effects of windthrow on forest at different spatial scales. A review. - For. Ecol. Manage. 135: 155-167. Vejre, H. and Emborg, J. 1996. Interactions between vegetation and soil in a near-natural temperate deciduous forest. - For. Landscape Res. 1: 335-347. Webb, S. L. 1989. Contrasting windstorm consequences in two forests, Itasca State Park, Minnesota. - Ecology 70: 11671180. Webb, S. L. 1999. Disturbance by wind in temperate-zone forest. - In: Walker, L. R. (ed.), Ecosystems of disturbed ground. Elsevier, pp. 187-222. Whitmore, T. C. 1989. Canopy gaps and their two major groups of trees. - Ecology 70: 536-538. Wolf, A. et al. 2004. Storm damage and long-term mortality in a semi-natural temperate deciduous forest. For. Ecol. Manage. 188: 197-210.

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Ecological Bulletins 52: 81-102, 2007

Above and below ground gaps - the effects of a small canopy opening on throughfall, soil moisture and tree transpiration in Suserup Skov, Denmark Lise Dalsgaard

Dalsgaard, L. 2007. Above and below ground gaps - the effects of a small canopy opening on throughfall, soil moisture and tree transpiration in Suserup Skov, Denmark. EcoL Bull. 52: 81-102.

In the natural temperate deciduous forest the gap-phase is crucial for forest regeneration and succession. During a relatively shorr time span the forest microclimate is changed with higher global radiation, larger temperature fluctuations, and less demand for soil water and nutrients from trees. These changes depend on the size and structure of the gap. This study takes a closer look at the changes in the hydrological cycle in a small canopy gap (diameter < stand height) in Suserup Skov during the first and second growing season following the gap-establishment. Specifically the effects of gap formation on throughfall, soil moisture, forest floor evapotranspiration and individual tree transpiration for European beech Fagus sylvatica is described. Stemflow for European beech and common ash Fraxinus excelsior for exposed trees and for trees in the intact forest is shown. Further, a non-linear model is used to test the significance of tree size and position on the spatial variability of water use at the soil moisture measurement positions. Throughfall was significantly higher in the gap than in intact forest positions annually (17%) as well as in summer (19-30%) and spring (19%). Soil moisture in the gap was significantly higher than in intact forest positions during summer and autumn. In gap positions soil moisture remained near 90% offield capacity during the summer months compared to 60~}O% in the intact forest. Forest floor evapotranspiration did not differ between the intact forest and gap positions. Stemflow for European beech was higher than for common ash (2: 1) and for both species higher when bare than when in leaf (2: 1). Stemflow was highest for exposed trees when bare. On a stand level, stemflow was 2% ofprecipitation (in leaf), 6% (bare) and 12% (exposed trees when bare). The spatial variability in water use at the soil moisture measurement positions was correlated to tree basal area and to the distance between measurement points and the surrounding trees (~= 0.43, p
L Dalsgaard ([email protected]), Forest and Landscape Denmark, Univ. of Copenhagen, Horsholm Kongevej 11, DK-2970 Horsholm, Denmark.

Copyrighr © ECOLOGICAL BULLETINS. 2007

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The continuous emergence of relatively small canopy gaps is central to the understanding offorest succession (Runkle and Yetter 1987, Emborg et al. 2000). Resources become available to seedlings and to previously suppressed trees and especially the availability of light: has been the focus of many studies (Emborg 1998, Einhorn et al. 2004, Einhorn 2007). In gaps leaves and branches are removed above ground and roots are deactivated below ground. Such a disturbance affects not only the availability of light but also the continuous exchange of water and water vapour between the soil, the vegetation and the atmosphere (the hydrological cycle, Rutter 1975). Thus, a number of important processes in the hydrological cycle are affected such as throughfall, transpiration from plants, evaporation from soil and from plant surfaces (interception loss) and seepage below the root zone. Often with the general result that soil moisture in the gap remains high during the entire growing season (Bauhus and Bartsch 1995, Gray et al. 2002, Vilhar et al. 2005, Ritter and Vesterdal 2006). The variability in soil moisture is relevant for the understanding of the nutrient- and carbon dynamics (Epron et al. 1999, 2004, Granier et al. 2003, Ritter 2007) of heterogeneous forests as well as the description and prediction of below ground competition among trees (Ammer and Wagner 2002). The available soil moisture affects the growth of seedlings (Madsen 1994, 1995, Tognetti et al. 1994). Thus the success of forest regeneration in gaps established as a means by forest management depends upon knowledge on soil moisture distribution in time as well as in space. Here, results are presented to describe the effects of a gap on the throughfall of water, on the spatial and temporal distribution of soil moisture, on the evapotranspiration from the forest floor and on the transpiration of European beech trees Fagus sylvatica near the gap. Further, results are shown for stemflow ofEuropean beech and common ash Fraxinus excelsior and some effects of crown exposure on stemflow. This study does not present calculated drainage fluxes and the water balance can therefore not be described in full. However, it presents results that are relevant when drainage fluxes are to be calculated and a suitable water balance model is to be parameterized for the site. Drainage from a forest gap to ground water reservoirs may be only marginally different from that of the intact forest; however, a calculation of fluxes for the specific stand and soil conditions in Suserup Skov is necessary to reveal this. Results from this study represent a specific point in time and space and are not suitable for a generalization across gaps. They do, nonetheless, give insight into the hydrological cycle of a forest type not often described. The high spatial resolution ofthe measurements is unique and the combination oftree transpiration with studies in a canopy gap has not been presented earlier. The effect of a canopy gap on throughfall may be inferred from the observations on forest canopy interception. For European beech and oak Quercus sp. annual rainfall interception (% of above forest precipitation) was 33-

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40% in 35-yr-old stands (Thomsen et al. 2003), 25-28% for both a young and an old European beech stand and a mixed European beech-conifer forest (Granier et al. 2000a, Zirlewagen and von Wilpert 2001) and 15-36% (European beech) and 8-21 % (oak) for stands of different age (Peck and Mayer 1996). Canopy interception depends on canopy structure but also strongly on rainfall intensity and duration with numerous short storms of low intensity resulting in a higher interception than few long high intensity storms (Rutter 1975). The spatial distribution of rainfall in a gap may be affected by the crown structure of the trees, which determines the amount of drip points at the crown peripheries (Linskens 1951, in Geiger et al. 1995). BUt it may also be affected by the wind direction and turbulence (Slavik et al. 1957, in Geiger et al. 1995). The highest values observed in the latter study (> 100% of values outside the stand) were at the eastern edge (due to westerly winds) and at a few locations along the gap edges due to water dripping from the tree crowns. Values in the centre of the gap were 95-100% of values outside the stand. In the remaining locations rainfall approached the level observed in the stand. Gaps are dynamic in nature and the ground vegetation may grow fast during the first few years after the formation ofthe gap (Ritter et al. 2005). Thus, rain may fall directly on the soil (net-precipitation) immediately after gap formation. As the ground vegetation develops some of the rain is withheld as interception loss and unless rain collectors are placed at the ground level this loss is not included in the measurements. The amount of rain reaching the soil as stemflow tends to be species specific. In a review Levia and Frost (2003) collected evidence of the importance of bark texture. Smaller amounts of stemflow were found in species with rough or flaky bark than in species with smooth bark because of differences in water storage capacity. Branch inclination, angle and crown geometry as well as individual tree size and exposure were also found to be determinants with high inclination angles, large trees and exposed crowns giving high stemflow values. Annual stemflow in European beech (smooth bark) was 4% of precipitation (Neal et al. 1993) with less in the growing season than in the dormant season and 5% of precipitation in the growing season (Granier et al. 2000a). Annual stemflow was up to 20% of precipitation for European beech (Ladekarl 2001 and references therein). In contrast stemflow in oak (rough bark) was < 2% of precipitation (Nizinsky and Saugier 1988, in Ladekarl 2001). Common ash is expected to have less stemflow than European beech because of a coarser bark texture. While the formation of a canopy gap leads to increased light availability to previously overtopped vegetarian with a spatial distribution governed by solar inclination and altitude as well as stand structure (Canham et al. 1990, Ritter et al. 2005) the soil moisture response may be less predictable. Slavik et al. (1957, in Geiger et al. 1995) found, in a mixed oak-European beech forest, that soil moisture in the

ECOLOGICAL BULLETINS 52,2007

central part ofa small (diameter <20 m) gap remained high during the entire summer. Soil moisture in the topsoil of small gaps also remained high throughout the growing season in European beech (Bauhus and Bartsch 1995), tropical wet forest (Ostertag 1998) and coastal Douglas-fir Pseudotsuga menziesii (diameter 0.2-1 X stand height) (Gray et al. 2002). The latter study found that soil water content generally was higher in the deep soil layer (15-45 em) than in the topsoil, that intermediate size gaps (diameter near 0.5 X stand height) showed a more pronounced soil moisture response than small (diameter 0.2 X stand height) and large (diameter 1 X stand height) gaps and that soil moisture was lower at the northern than at the southern gap edge of large gaps due to direct radiation and high evapotranspiration. They further concluded that, although there was a general tendency for gap centers to show high soil moisture, radiation and variability in soil humus content created dry micro sites for seedlings also in the centre of gaps. Similarly, gap formation in a Nothofagus pumilio forest created both dry and moist conditions in the topsoil (Heinemann et al. 2000). Where understorey vegetation grows to dominate the gap a soil moisture response may not be observed at all (McGuire et al. 2001). Clearly, the growth and survival of seedlings and the distribution of other vegetation in a gap as well as the nutrient cycle and soil fauna may be affected by the soil moisture distribution (Ritter 2007, Bj0rnlund and Lekfeidt 2007, Hahn et al. 2007). The gap effect for soil moisture disappears with time. In a temperate coniferous forest after ca 4 yr (Gray et al. 2002) and after 1 yr in a tropical forest (Veenendaal et al. 1995). The duration of a gap effect for soil moisture is closely related to root distribution and root expansion (Brockway and Outcalt 1998, Ammer and Wagner 2002, Muller and Wagner 2003). However, root distribution is difficult to measure; therefore it is attractive to be able to predict root distribution from the vegetation. The relationship between root and single-tree distribution has been investigated for European beech (Nielsen and Mackenthun 1991) and Norway spruce Picea abies (Ammer and Wagner 2002). For both species fine root density decreased with distance to the tree in a nonlinear way and at some sites it increase with tree basal area. Such models have so far not been applied in mixed heterogeneous stands to describe the activity of roots (i.e. water extraction). The fact that root gaps do not last forever implies that some trees benefit from the high soil moisture found in gaps in their early stage. During the growing season the water content ofthe forest soil generally declines due to the combined effecrs of interception loss and transpiration. During dry periods, often in early autumn, the stand is subject to mild or severe water stress (Granier et al. 2000a, b). High soil moisture after gap formation may allow trees near the gap to sustain high transpiration rates in periods where nees in the stand experience beginning (or severe) water stress. Thus the release of trees following the formation of a canopy gap may not refer exclusively to the avail-

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ability oflight, but also to the access to soil water. In Scots pine Pinus sylvestris edge trees were observed to have higher transpiration rhan trees in the stand (CienciaIa et al. 2002). As photosynthesis and transpiration rates are proportional (Carovsky et al. 2002) this would imply, that the growth of trees near a canopy gap and the closure rate of gaps depends on the available soil water. In closed forests the evapotranspiration from the forest floor in the growing season is low - usually below 10% of stand evapotranspiration (Granier et al. 2000a, Wilson et al. 2000). However, the periodic contribution can be up to 20% of total stand evapotranspiration (Kelliher et al. 1992) and for a vegetated forest floor above 50% (Roberts et al. 1980). Evaporation near the forest floor was higher in the northern than the southern part of a canopy gap (Slavik et al. 1957, in Geiger et al. 1995), but measurements contrasting gap and intact forest conditions have not been presented. However, in references given above (Heinemann et aI. 2000, Gray et al. 2002) it is evident that the topsoil in gaps has been observed to become dry implying some evaporation in these gaps from the upper soil layers. A dry ropsoil (0-15 cm) does not contradict the existence ofdeeper soil layers with high soil moisture (as found by Gray et al. 2002), but it triggers the question if forest floor evaporation is higher in a gap than below the intact forest canopy. The basic hypothesis of this study is: 1) following the creation of a canopy gap, soil moisture in rhe gap is higher than below the intact forest canopy. Input and output of water were subject to individual investigations based on the following hypotheses: 2) throughfall in the canopy gap is higher than below the intact forest canopy. 3) Stemflow depends on species (European beech> common ash) and is higher for exposed trees than for trees in the closed stand. 4) Water uprake from the soil (water use) is related to the position and the size of trees near the gap; thus, the extent of a root gap can be predicted from tree size and position. 5) Evapotranspiration from the forest floor is higher in the gap than below the intact forest canopy. 6) Tree transpiration rates depend on tree position relative ro the canopy gap with the highest transpiration rates hmnd for trees near the canopy gap.

Methods Measurement site The site is in Suserup Skov, a 19.2 ha uneven-aged mixed deciduous forest (55°22 /N, 11 °34 /E), where a 20-m diameter gap was formed in the storm of December 1999 (Ritter et al. 2005, Heilmann-Clausen et al. 2007). The gap is very irregularly shaped. It was formed when a large old canopy tree lost most of its crown and a number of smaller trees were windthrown. Along the gap edges several

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small trees were released by the formation of the gap. The soil is a loamy till with pockets of sandy till (inceptisol) developed from moraine deposits (Vejre and Emborg 1996). The measurement plot was on a well-drained plateau in the central part of the forest. The groundwater level was below 1.2 m throughout the year based on the lack of gley-characteristics in the soil profile (Ritter and Vesterdal 2006). The plot was northeast of a lake (Tystrup S0) and 80 m from the northern forest edge bordering agricultural fields. Stand basal area at the measurement plot (based on measurements in a 6400 m 2 area around the gap) was 40.2 m 2 ha- 1• Total tree density (diameter> 4.5 em) was 733 stems ha- l . Four tree species were present near the gap; percentage of basal area is given below: European beech 56.1 %, common ash 28.1 %, wych elm Ulmus glabra 2.8% and pedunculate oak Quercus robur 13.1 %. Across all trees mean tree height was 13.3 m and stand top height was 28.4 m. The mean diameter was 18.5 em, 1st quartile for diameter was 6.8 em and 3rd quartile was 22.3 em. The stand is also characterized by a number of large old trees (European beech and pedunculate oak) reaching diameters near 150 em. Tree positions, tree heights and diameter were determined in January 2000, supplemented by measurements in 2001-2002 (Brunner, Oalsgaard, Einhorn and Ritter unpubl.). The oldest European beech trees have been dated to almost 300 yr and the structure now resembles that of a natural forest (Emborg et al. 1996,2000).

Meteorological measurements Precipitation (P; Pronamic, Rain-o-maric, area 0.02 m 2, resolution 0.2 mm), air temperature and relative air Immidity (Vaisala HMP45A), solar radiation (Li-Cor LI190SA Quantum Sensor) and wind speed (Vector Instruments A100L2, cup anemometer) was measured 2 m above the ground in a field 300 m from the stand edge. P was corrected for wetting (evaporation directly from the funnel surface) and for the influence ofturbulence near the funnel (Vejen et al. 2000). Corrections are based on on-site meteorological measurements in the height of the funnel (2 m) and assuming that the daily wetting is the same for 2 m as for the height used by the Danish Meteorological Inst. (1.5 m). Air temperature and relative air humidity at 2 m was also measured in the stand near the gap using the same type of instruments. Instruments were scanned every lOs and observations were averaged every 30 min. Air vapor pressure deficit (0) was calculated from measurements of air temperature and relative air humidity.

Measurement positions for throughfall and soil moisture Measurements were placed in an 8 X 8 point grid covering the gap with 6 m between positions in the north-south

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direction and 5 m between positions in the east-west direction. Fifty-nine of the 64 positions were equipped with instruments. The distances between positions as well as the total number stem from the need to coordinate measurements among researchers working at the site and in the same gap. Until 19 April 2001 all 59 positions were measured. After this day 28 of the 59 positions were measured (Fig. 5d, see caption). The positions were divided into three categories: intact forest (29/10): positions below the main canopy and 2 m from the stem of trees bordering the gap (in the direction away from the gap); gap (13/10): positions in open conditions and 2-3 m from the stem of trees bordering the gap (in the direction toward the gap); edge (17/8): remaining positions. The number of observations in each category is given in brackets (beforelafter 19 April 2001).

Throughfall and stemflow Throughfall (TF) was measured manually with a weeklymonthly resolution using plastic funnels (diameter 11.8 em) placed 1 m above the ground (and above the ground vegetation for all measurement positions). In the central part of the gap, throughfall may be equal to the precipitation. However, acknowledging that rain falling in a small canopy gap may be affected by the surrounding tall canopy the term "throughfall" was chosen. This allows for the same terminology for positions in the intact forest as well as in edge and gap positions. The water collected in the funnels was led into bottles buried in the ground. Measurements were corrected for wetting (Vejen et al. 2000). Stemflow (SF) was measured on 10 trees (five common ash 17-50 cm diameter and five European beech 14-57 em diameter). Two were at the edge of a small opening near the investigated canopy gap thus with exposed crowns. The remaining trees were in the stand near the investigated gap. None of the trees were near the soil moisture measurement positions. On each tree a profile silicon collar was spiralled twice around the stem 1.5 m above the ground. The water was led to a container (with a known volume) beside the tree and the amount of water in the container was measured manually once a week (May~Oc tober) or approximately once a month (November~April).

Soil moisture The volumetric soil water content (SWC, vol.%) was measured by Time Domain Reflectometry (Topp et al. 1980, Thomsen 1994) Crektronix 1502C/1502B). Measurements were at the positions described above. Probes were stationary and integrated over a 0.3,0.5 or 0.9 m soil profile and consisted of two 6 mm stainless steel rods. Measurements were manual and bi-weekly (May-October) or monthly (November-April). The soil water con-

ECOLOGICAL BUlLETINS 52, 2007

tent measured with TDR in vertical profiles was within 15% of the gravimetrically determined values (February 2001) scaled to a soil profile (n=3 for each of four horizons). For analyses of tree transpiration only measurements from below the intact forest canopy were used (depth 0.5 m, n;;::10). These can be expressed as the available soil water ((SWC-WP)/FC-WP), where WP is wilting point and Fe is field capacity. Field capacity was found as the mean of measurements from 25 January to 24 April (for some positions 19 April). During this period SWC measurements were stable and for the 0-0.9 m and 0-0.5 m probes within 5% of the mean value (FC) for each position except for one in 0-0.5 m (within 5.3% ofFC). In 00.3 m depth SWC was within 10% ofthe mean value (FC) except for one position (within 21.5% of FC). The mean value (and not the maximum) was used to avoid a very high FC due to recent rain or slow drainage of water from the soil. The mean in-situ FC was 229 mm (0-0.9 m), 134 mm (0-0.5 m) and 89 mm (0-0.3 m). Soil water retention was determined in the laboratory on soil samples from two soil profiles (n=4 or n=8 for each horizon) (Schonning 1985). Calculated fIeld capacity for the two soil profiles based on the water content at -0.01 MPa (pF 2) were 512% lower than the values measured in-situ: 202 mm (00.9 m), 127 mm (0-0.5 m) and 81 mm (0-0.3 m). Wilting point (WP) in 0-0.5 and 0-0.9 m was calculated from laboratory samples (-1.5 MPa, pF 4.2) to 4.4 and 4.3 vol.% respectively (22 and 39 mm). The two profiles were in the intact forest north-east and north-west of the gap. Due to the protected status of the forest as well as a lack of space in the gap area it was not possible to obtain soil water retention data from the gap or the edge.

Transpiration Sap flux density 0" g m- 2 S-I) was measured using the thermal dissipation technique (Granier 1985, 1987, Granier et al. 1996). Js was measured on 12 European beech trees from 15 June to 30 September 2000 (Dalsgaard unpub!.). The sample trees (diameters 0.11-0.70 m) were positioned north-west of the gap; some in the intact forest and some in the gap edge. Averages were logged every 30 min and Js was calculated using the calibration formula developed by Granier (I985). Probes (one pair per tree) were inserted radially into the northern side of the stem 2 m above the ground with a vertical distance of 0.2 m and protected from rain and from direct sunlight. Measurements were scaled from sensor to tree by using a model for the radial variation in sap flux density: relative], :; : 1.0075/ (l + (x 1 4.8896) 3.0836), where x is the depth (cm) and the relative Lis 1 at a given depth relative to Js measured in the outer 20 mm of the xylem (Dalsgaard unpub!.). The model was based on measurements from Suserup Skov and predicts a decreasing J$ with increasing xylem depth as also found by other authors (Kasmer et al. 1998, Lang 1999,

ECOLOGICAL BULlETINS 52, 2007

Granier et al. 2000a). Tree transpiration was the tree scaled sap flux density related to the crown projection area.

Forest Hoor evapotranspiration Evapotranspiration and soil evaporation from the forest floor was measured with smalllysimeters (depth 150 mm, diameter 85 mm) at two occasions: 14-15 August 2001 (1 d) and 29-3] August 2001 (2 d). At each occasion 16 lysimeters were placed in the intact forest and gap locations. Half of the lysimeters included small seedlings (mean seedling height at the two occasions was 26.4 and 27.0 em (gap) and 20.1 and 24.3 em (intact forest). The other half of the lysimeters included only soil and litter. Evaporation was determined as the difference in weight (g, two decimal points) in the morning on subsequent days. No rain occurred during the measurement periods.

Statistical analyses For throughfall (TF) differences among gap, edge and intact forest positions (Tukey-Kramer adjusted t-test, p<0.05, PROC GLM, SAS 8.2) were tested for spring (April-May)} summer Oune-September), autumn (October-November) and winter (December-March). Data were available from June 2000-January 2002 giving a total of seven periods. For each period throughfall was summed for each measurement position. Positions N, S} E or W of the gap centre were compared using the 45°, 135°, 225 0 and 315° angles as dividing lines between groups. Positions NE, ~ SE or SW of the gap centre were compared using the 90°, 180°, 270 0 and 360 0 angles as the dividing lines. Data were used from both the grid (59 positions) and transect (28 positions). The mean throughfall within each category was regressed on precipitation (bi-weekly to monthly measurements). The effects of category and season (defined as above) across all data was found by testing the significance of their interaction with P. For each season the effect ofthe interaction between P and category was tested. For each category the effect of the interaction between P and season was tested. The effect of year was found for measurements in summer (200012001) by testing the significance of the main effect as well as the interaction with P. Regressions (Y=slope x P) are presented for specific seasons and categories. PROC GLM} SAS 8.2 was used for all tests and regressions. Data were used from 28 positions measured in June 2000 through August 2001 (P was not measured after this date). For each tree stemflow (SF) was regressed on P and the significance of season was tested. Observations 1 November-3 May were categorized as bare (winter) and remaining observations as in leaf (summer). The flmnelling ratio (Herwitz 1986 in Levia and Frost 2003, Herwitz and Levia

85

1997) for individual trees F = V/BAP is given for selected periods (V is stemflow volume, BA is tree basal area). Subsets of the data were excluded from the analyses due to plugging or overflow from the containers. Further, for each season and for each of SF and SF/BA, the significance of tree basal area, species (ash, beech) and crown exposure (edge, stand) was tested in one model incorporating P as well as stemflow from all trees. PROC GLM, SAS 8.2 was used for all tests and regressions. Species specific models f(x SF/BA are used to predict the stand stemflow from P. The response (SF in L period-lor SF/BA in L m-2 period-I) was transformed when necessary to obtain homogeneity ofvariances. Transformations used were a log transformation: Y=ln(SF+l) and the Freeman-Tukey transformation:Y=(SFI BA)O.5 + (SF/BA+l)o.5 (Weisberg 1985). For soil moisture, differences among gap, edge and intact forest positions were tested (Tukey-Kramer-adjusted ttest, p<0.05, PROC GLM, SAS 8.2). Response variables were SWC in 0-0.3 m depth (SWC 30) and in 0-0.9 m depth (SWC90) and the relative SWC in the two depths (RSWC 30 and RSWC90 ), which is SWC as a fraction of field capacity. Data were used from both the grid (59 positions) and transect (28 positions). All responses were averaged over periods ranging from 1 to 4 months: spring: mid April-May, summer: June-September, autumn: OctoberDecember (autumn 2001 measured only in October), winter: January-mid April. Measurements were available from June 2000 to October 2001 giving a total of six periods. An effect of position relative to the gap centre was tested as described above for throughfall. To relate tree position and soil water dynamics periodic water use was calculated in 0-0.5 m depth (WU 50) and in 0-0.9 m depth (WU90)' Five summer periods in 2000 were identified where for each period P<1 mm. They were: 16-20 June, 3-7 July, 11-18 July, 25-28 July, and 4-8 August. T'he observed changes in soil water content were assumed to be caused primarily by water uptake by tree roots. For WU 50 the four periods were selected that had the highest SWC (period 1,2,3, and 5). SWC in 0-0.5 m depth was 14.8-19.4 vol.% in intact forest positions and 22.9-27.0 vol. % in gap position during these periods. For WU90 period 2, 3 and 4 were selected. For each position the changes during the relevant periods were summed (= water use in vol. %). A nonlinear model (Nielsen and Mackenthun 1991) relating water use at each position to tree position and basal area of the 20 closest trees was parameterized using PROC NLIN (SAS 8.2). water use =

i=20

a X BAd

i=l

1 + b x exp(c X dist i )

I

j

(1)

Where BA is stem basal area of tree. (m 2), dist is the distance (m) between the position and ~reei and a,J b, c and d are fitted parameters. Dead trees were not included and the old tree/stump in the centre of the gap (the gap maker, Fig. 2d) was also left out though a small parr of the crown still remained. A toral of 197 trees entered the model (for each

86

TOR position the 20 closest trees thus some trees more than once). 70% were European beech, 13% were common ash and the rest pedunculate oak (one old tree) and wych elm (numerous small trees). Possible differences in water use among tree species were investigated in the following two ways: 1) for each ofWU 50 and WU 90 , eq. 1 was allowed to have specific parameters for European beech and for the remaining species, thus, a total of 8 parameters; 2) for each position the basal area of each species (relative to the total basal area) for the closest 20, 10 or 5 trees was related to the studentized residuals found from eq. 1 (common parameters for all species). Differences between gap and intact forest positions on forest floor evapotranspiration was tested (Tukey-test, p < 0.05; PROC GLM SAS 8.2) for each of three observation periods and for the sum of the two observations on 29-31 August. The effect of tree size and position on tree transpiration was investigated by identifYing three groups of trees (Dalsgaard unpubl.): canopy trees (can: height> 20 m; n=6(5»), subcanopy trees below the intact canopy (subF: height < 20 m; n=3), subcanopy trees in the edge of the canopy gap (sub o : height < 20 m; n=3). Differences (t-test, PROC GLM SAS 8.2) in mean and maximum sap flow rates were tested in a monthly resolution Os-sum (kg water m-2 sapwood d- I ; and Js-max (kg water m- 2 sapwood halr hour-I». Differences in the daily transpiration rates were tested in a weekly resolution (Esum (mm d-- 1). The daily sap flux density for can and sub p relative to subo (in %) was analyzed in a multiple linear regression with daily values of global radiation, vapour pressure deficit and available soil water in 0-0.5 ffi.

Results Weather during the measurement period The summer of2000 was relatively cool with frequent rain episodes whereas the summer in 200 1 was warm. In 2000 mean air temperature (OC) measured on site for July, August and September were 15.4, 15.7 and 13.2. In 2001 the mean air temperature in July and August were 17.9 and 17.2. Precipitation was low in July for both years, but August was dry in 2000 and wet in 2001. Soil water content in 0-0.9 m in the intact forest reached a low of 11.5 vol. % (103.7 mm) in early September 2000 and 11.0 vol.% (99.1 mm) in early August 2001 (Fig. 1).

The spatial pattern of throughfalI Throughfall in the intact forest positions was significantly lower than in gap positions in summer and in spring (Table 1; 77-84% of throughfall in the gap), but edge posi-

ECOLOGICAL BULLETINS 52, 2007

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Fig. 1. Air temperature, precipitation and soil moisture in the intact forest (0~0.9 m) June 2000-0ctober 2001 in Suserup Skov. For technical reasons the measurement of precipitation stopped in September 2001. The lack of meteorological measurements in early spring 2001 is due to the maintenance and calibration of equipment. Error bars show ± one standard error of the mean.

tions were never different from the intact forest. Similarly, annual and total throughfall was lower in the edge and intact forest positions than in the gap. In autumn positions north of the gap centre received more throughfaH than positions east and south of the gap centre (114 vs 98 and 96 mm; 2000) or positions west of the gap centre (128 vs 105 mm; 2001). The interaction between category and orientation relative to the gap centre was never significant. Regression of throughfall on P showed that across years the interaction with both category (p
ECOLOGICAL BULLETINS 52, 2007

Stemflow Data showed a large variability in stemflow volumes (SF) and there were dear effects of season, species, BA, and crown exposure. The regressions of stemflow on precipitation for the individual trees gave r2-values of 0.51-0.79 for trees in leaf and 0.57-0.83 when bare. For all trees except one, season was significant (p<0.05) (Table 2). Funneling ratios were 0.9-3.3 and 8.6-18.9 for common ash and 5.1~8.4 and 15.4-47.0 for European beech (in leafand bare respectively, Table 2). During a summer period where measurements for the exposed crowns were missing (29 May-24 July 2001) funnelling ratios were 1.2-2.6 for common ash and 3.3~6.4 for European beech. Across all trees SF was predicted from P, BA, exposure and species (bare: p<0.0007 for all effects, r-value 0.74; in leaf: p
87

00 00

Table 1. Mean throughfall in the intact forest, edge and gap in Suserup Skov, Denmark, June 2000-January 2002. Different letters indicate significant (p<0.05) differences using the Tukey-Kramer adjustmentfor multiple comparisons. SE is the standard error of the mean. June 2000-April2001 all 59 positions in the grid were used and values in the square brackets are based on the 28 positions measured throughout all of seven periods. April 2001-January 2002 n;;:;:;28. Canopy interception (not including stemflow: ((P - throughfall)/P) for some of the periods is also shown. Throughfall mm (SE)

Canopy interception % (5£) Time period

Intact forest

Gap

Edge

June-September 2000

October-November 2001

A179.5 (6.3) [a171 .0 (5.6)] 27.7 (2.8)[25.4 (2.5)] A101.8 (2.5) [a99.5 (6.1)] 32.3 (7.6) [33.8 (4.7)] A176.9 (2.8) [a175.7 (6.4)] 20.7 (7.3) [20.5 (2.9)] A37.7 (1.2) 29.2 (2.6) A267.6 (12.0) 29.9 (3.8) A1 08.0 (5.8)

B213.2 (8.4) [b220.1 (8.2)] 7.0 (3.7) [4.0 (3.6)] A108.4 (5.8) [al12.2 (6.09)] 27.9 (3.9) [25.4 (4.0)] A175.0 (5.4) [a180.3 (3.6)] 22.7 (2.7) [79.7(2.0)J 644.9 (1.2) 22.3 (7. 7) B348.5 (12.8) 70.6(3.7) A121.6 (7.0)

A181.7 (6.8) [a178.3 (12.5)] 20.7 (3.0) [22.2 (5.5)] Al 07.8 (4.2) [a1 03.0 (6.5)] 28.3 (2.8) [31.5 (4.3)] A183.1 (4.5) [a179.1 (4.3)J 77.8 (2.3) [20.0 (2.2)] A39.5 (1.2) 28.9 (2.5) A273.1 (16.4) 30.3 (4.4) A114.4 (4.0)

December 2001-January 2002

175.7 (8.8)

163.6 (5.5)

181.4 (3.0)

Total integrated

A1035.1 (32.5) 27.S (2.4) A515.6 (15.2) 27.5 (2.2)

B1191.3 (27.7) 73.8 (2.0) 8603.2 (13.0) 75.2 (7.8)

A1 068.9 (32.1) 26.2 (3.0) A533.0 (19.4) 25.4 (3.0)

October-November 2000 1December 2000-19 April 2001 124 April-May 2001 lJune-September 2001

Annual: 27 June 2000-26 June 2001

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Precipitation (mm) Fig. 2. Throughfall relative to precipitation in gap, edge and intact forest position in Suserup Skov. Difference among categories were significant only during the summer. Error bars show ± one standard error of the mean.

ECOLOGICAL BULLETINS 52. 2007

89

60..---Edge and Intact forest .-

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2 - - Autumn: Y=0.679· P (r = 0.89) 2 Spring: Y=0.734 . P (r = 0,99) 2 Summer: Y=0.743 . P (r = 0.95) 2 - Winter: Y=0.797 . P (r = 0.99)

30

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Precipitation (mm)

Precipitation (mm) • • •

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2

Summer: Y=0.922 . P (r = 0.97) 2 Winter: Y=0.797 . P (r = 0.99) / 2 Spring: Y=0.799 . P (r = 0.99)

Fig. 3. Throughfall relative to precipitation for different seasons in Suserup Skov. Across seasons there was no significant difference between the edge and intact forest positions. In gap positions the regressions for winter and spring were almost identical and both are represented by the broken line. Error bars show ± one standard error of the mean.

stead of the species effect results were for the winter (rvalue 0.71): P (p
90

The spatial pattern of soil moisture Field capacity (FC) varied across positions, but for the 00.9 m depth there was no significant difference among categories and the mean FC was 229 mm (standard error of the mean: 0.5 mm) For 0-0.3 and 0-0.5 m FC in edge positions (93 and 141 mm) were significantly higher (p<0.05) than in the intact forest (86 and 130 mm) and FC in the gap was intermediate (92 and 136 mm). There wefe no indications that FC was higher close to tree stems thus any effect on FC of stemflow did not emerge. However, only in eight occasions was the soil moisture measurement within 1 m of tree stems. Differences among categories emerged during the summer and autumn (Fig. 5) with

ECOLOGICAL BULLETINS 52, 2007

85 CJ

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Table 2. Stemflow for individual trees predicted from precipitation. The level of significance (p-value) of season is shown as well as stem diameters and regressions for each tree when bare and when in leaf. Observed stemflow and funneling ratio (see text) are shown for selected periods. Trees #9 and #10 were at the edge of a small opening and their crowns were exposed.

#

diam. (em)

Common ash 1 24.2 2 49.7 5 16.9 6 28.3 10 38.2

in leaf Cregression (n) r2

Yt=0.045+0.034x (34) 0.51 Yt =0.082+0.085x (30) 0.63 Yt =0.028+0.035x (21) 0.56 Yt =0.152+0.065x (21) 0.63 Yt =0.044+0.085x (7) 0.63

12 September-31 October 2000. 10 November 2000-25 January 2001 . CThe response was transformed: Yt"'" In(stemflow+1). b

\D

cp
Stemflow Lx tree- 1 (funneling ratio) aj n leaf bbare P=134 mm P=193 mm

Fraxinus excelsior

European beech Fagus sylvatica 3 57.3 Yt :c:-0.045+0.19x-0.002x2 (30) 0.78 4 32.8 Yt :c:-0.045+0.148x-O.001 x2 (30) 0.79 8 14.3 Yt =0.190+0.040x (21) 0.57 9 36.3 a

bare regression (n) r2

y=-1.843+0.322x (12) 0.57 y=-14.732+ 1.336x (12) 0.62 y=-6.523+2.438x (8) 0.68

0.0001 0.1742 0.0008

5.3 (0.9) 69.3 (2.7) 6.4 (2.1) 28.2 (3.3) 48.3 (3.1)

y"",-40.71 0+6.268x (11) 0.77 y=-45.553+4.405x (12) 0.78 y=-l. 757+0.413x (12) 0.62 y"",-25.731 +5.928x (8) 0.83

0.0019 0.0035 0.0023

223.6 (6.5) 93.3 (8.4) 11.1 (5.1)

40.6 (9.4) 105.0 (8.6) 419.0 (18.9)

778.9 (15.6) 422.1 (25.9) 48.0 (15.4) 939.7 (47.0)

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Fig. 4. Stemflov,- relative to precipitation (L X m-2 tree basal area) for common ash Fraxinus excelsior and European beech Fagus sylvatica and total stand stemflow (mm) relative to precipitation in Suserup Skov, Denmark. Curves for exposed conditions scaled to the stand level use the same distribution of basal are to the two species as in the closed stand (see text). Data were obtained June 2000-Augu.st 2001 and each observation cover I-several precipitation events. Curves show the back-transf()rmed predictions using the Freeman-Tukey transformation ((stemflow)05 + (stemflow+l)°-5). R2-values for ash (predictions) were 0.59 (bare), 0.61 (bare exposed) and 0.59 (in leaf). For beech they were: 0.67 (bare) 0.76 (exposed) and 0.75 (in leaf).

gap positions showing higher soil moisture than positions in the edge and in the intact forest. For both 0-0.3 m and 0-0.9 m there was a dear soil moisture effect of the gap. In summer and autumn SWC was generally higher in gap positions, intermediate in edge positions and lowest in the intact forest (Table 3). Edge occasionally differed from gap and intact forest positions in summer and autumn, but not in all cases. In winter in-

92

tact forest SWC was slightly lower than in gap and edge positions. I spring intact forest and gap positions differed. RSWC showed the general result that edge positions were different from both gap and intact forest positions until autumn 2000. In 2001 edge was not different from the intact forest positions. Positions to the north were never significantly drier than other positions, neither for the entire measurement area nor for positions within the gap. Rather it was revealed that southern and southeastern positions in the measurement area were generally drier than other positions. This was most pronounced for the SWC and less pronounced for RSWC indicating that the relative values may express better the differences between the gap, edge and the intact forest.

For water use (WU), ~TU50 was 5.0-~15.3 vol.% (the equivalent of24.9-76.5 mm during 19 d) and WU90 was 1.8-6.7 vol.% (the equivalent of 16.2-60.3 mm during 14 d). Predicted and observed values ofwater use are shown in Fig. 6a, the regressions were both tested to be significant (p
Forest floor evapotranspiration Daily soil evaporation was lower than daily evapotranspiration including vegetation, but differences between intact forest and gap positions were not significant (Fig. 7). During the three measurement days, mean values for soil evaporation were 0.15-0.28 mm d- 1 and for evapotranspiration they were 0.7-0.9 mm d-- 1•

ECOLOGICAL BULLETINS 52, 2.007

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Distance from gap centre (m) Fig. 5. Smoothed values ofsoil water content at 0-0.5 m depth (SWC 50 , voL %) in and around a canopy gap in Suserup Skov during the summer of 2000. Inserts show measured vs predicted (smoothed) values with all axes from 0 to 30 vol.%; r2 values are given subsequently. (a): mean for July (n = 7; r= 0.91), (b): mean for August (n = 9; r2 = 0.93), (c): lowest observation on 1 September (r=0.92), (d): location of trees in and around the gap (gray circles). The size of the circles is scaled from tree diameter. The gap centre is at (0.0) m. At (-5.0) m a large grey circle show the position of the gap maker, which is still alive albeit with a very small crown. A thin black line indicates the edge of the gap. Triangles show positions where throughfall and soil moisture was measured until April 2001. Black triangles are positions measured after April 2001. For the contour plots, data are smoothed using a negative exponential weighting procedure (SigmaPlot 2000, SPSS, USA) with fixed bandwidth and a sampling proportion of 0.2 (ca 5 observations for each prediction; modified from Ritter et al. 2005).

Tree transpiration - effects of size and position of trees For the three groups oftrees the weekly value of mean daily transpiration were 0.2-0.9 mm (sub F), 0.3~0.8 mm (sub o ) and 0.4-1.3 mm (can). The minimum values were reached in mid September except for subo where minimum was

ECOLOCICAL BULLETINS 52, 200?

reached in late June. Maximum values were reached in mid June for all groups. Monthly values of JS~Sunl and Js--= were higher for subo than for subF in August ((p
93

Table 3. Mean soil water content in the intact forest, edge and canopy gap for Suserup Skov, Denmarklune 2000October 2001. Different letters indicate significant differences among categories (p
0-0.9 m Forest

Gap

Edge

June-September 2000 October-December 2000 January-19 April 2001 20 April-May 2001 June-September 2001 October 2001

A15.6 (alS.l) A16.9 (a16.5) 24.7 (a24.5) A22.2 A16.7 A20.9 1

B23.5 (b24.1) B24.6 (b25.3) 26.1 (b26.2) B24.6 B24.3 826.8 1

(19.4 (C19.2) c20.8 (C20.8) 25.9 (b26.0) AB23.7 A19.9 B25.2 1

Fraction of field capacity June-September 2000 October-December 2000 January-19 April 2001 20 April-May 2001 June-September 2001 October 2001

0-0.9 m AO.64 (aO.61) A0.70 (aO.67) 1.00 (1.00) AO.91 AO.68 AO.89 1

BO.90 (bO.92) BO.94 (bO.96) 1.00 (1.00) BO.94 80.93 Bl.02 1

(0.75 (aO.73) (0.79 (CO.79) 1.00 (1.00) ABO.91 AO.76 AO.95 1

0-0.3 m Forest

Gap

Edge

A17.7 1(a17.5) A22.4 (a22.0) A28.7 (a28.0) A23.6 1

B27.6 1(b28.6) B30.0 (b30.9) AB30.6 (b31 .2) B28.0 1

A19.9 A25.8 1

B29.2 832.5 1

c22.8 1(C24.1) fl27.2 (b27.8) 83"1.0 (b31.4) AB26.61 C24.5 AB29.51

0-0.3 AO.63 A0.78 ALOO AO.83 AO.71 AO.89

m (aO.63) BO.90 (bO.91) (aO.78 1) BO.98 (bO.98 1) (1.00) Al.00 (1.00) AO.89 80.93 Bl.03

c0.75 (CO.77) cO.88 (CO.89 1) Al .00 (1.00) AO.84 AO.78 AO.94

1The response variable was transformed. The mean value was back-transformed.

significant differences were predominantly found between can and sub p and values were consistently highest for the former (Table 4 and Fig. 8). Significant differences were found beginning in mid July 2000 until the end of the measurement period, thus not in the early summer. The evolution of the mean daily Js-sum (weekly resolution, Fig. 8) shows that in early summer subcanopy trees are equal regardless of position and canopy trees show the highest values. In late summer subcanopy trees near the gap show the highest values, canopy trees intermediate values and subcanopy trees below the forest canopy show the lowest E

EO) (/)

::::l

4

Ci5

115 3::

>-

C6 'U

r a

.....

~

E

Q) (/)

66- .6-

::::l

ID

t:.

6-

3

115 3:: .?-

2

0.6

E

02[

1:5 :0

t5 :0 Q)

0)

1 1.0 1.5 2.0 2.5 3.0 3.5 4.0 4.5 Measured mean daily water use (mm)

a.5m 2

0.4

'U

~

Ie

0.8

c

co Q)

-g a..

10J~

"(tj "0

c

('Ij Q)

E

E-

values. This development is seen also for E sum (Fig. 8, lower panel). In the multiple linear regression analysis on the relative daily flux density for both can and sub p global radiation (p<0.0012; p
0::

5m

0.0

--.-.., 0

2

4

6

8

Distance (m)

10

0.0

0.2

0.4

0.6

0.8

1.0

Tree basal area (m 2)

Fig. 6. Results from the prediction ofwater use in Suserup Skov. (a): Predicted and observed water use in 0-0.5 m depth (19 d, black symbols, thick line) and in 0-0.9 m depth (14 d, open symbols, thin line). For both depths r=0.43. Parameter values were: a = -6.0947, b = -2.3048, c = 0.1135, d = 0.3290 (0-0.5 m) and a = 2.2437, b = 0.7895, c = 0.2453, d = 0.2946 (0-0.9 m). The dotted line show a 1; 1 relationship, (b): predicted water use vs distance and two examples oftree basal area, (c): predicted water use vs tree basal area with two examples of distance.

94

ECOLOGICAL BULLETINS 52, 2007

o Gap:

r;a Forest: soil with litter

I!!1.l

gj

soil with litter Gap: soil, litter and plant

Forest: soil, litter and plant

1,6

E

~

1.4

c 0

.~

Mean Ta Mean 0 MaxO

3.6

157 4.8

8.9

10.1

19.9

14.6 3.7 9.5

0.ell

0.8

>

Q)

0

0.6

0

:;:::

(j) ~

0.4

2::-

0.2

E

.~

Week number

1.2

'0.. (/) c ~ (5

Table 4. Comparison (Hest) of mean daily Esurn (weekly mean) for tree groups in Suserup Skov, Denmark 15 June30 September 2000. P·values are indicated as p
0

0 14-15 Aug SWCO-30 em 14(8 211 (1.9) 30.8 (1.0)

29-30 Aug

28/8: 25.6 (1.4) 323 (0.8)

30-31 Aug

31(8: 225 (1.2) 299 (0.9)

Fig. 7. Evapotranspiration from the forest floor in gap and forest positions August 2001 in Suserup Skov. For 29-30 and 30-31 August observations were made on the same lysimeter and soil volume. Error bars show 1 standard error of the mean (n=4). The daily mean air temperature (Ta, °C) and the daily mean (D) and maximum (max D) vapour pressure deficit (hPa) are shown above bars. Soil water content (voL%) in 0~.3 m depth was measured on 14, 28 and 31 August. These data are shown below bars (upper: forest; lower: gap) including the standard error ofthe mean in parenthesis.

are lower than the remallllllg groups. In August there seems to be a clear differentiation among groups (sub o > can> sub F).

Discussion Spatial patterns Throughfall was higher in the gap than in the intact forest positions both annually and for spring and summer periods. In the growing season Slavik et al. (1957, in Geiger et al. 1995) found 90-100% ofreference precipitation in the gap and 70% in the intact forest, which corresponds well to that found in Suserup Skov. Neal et al. (1993) found significantly increasing throughfall in plots after windthrow (storm damage) but the size of the openings created were not given. Zirlewagen and von Wilpen (2001) found annual interception loss in gaps and crown openings to be 21 % of reference precipitation, which is higher than in Suserup Skov (15%). In the study mentioned above the height of the water collectors relative to the possible ground vegetation is not given thus a direct

ECOLOGICAL BULLETINS 52.2007

Esum (mm d- 1) 1: Mid June 2: Mid June 3: Late June 4: Early July 5: Mid July 6: Mid July 7: Late July 8: July/August 9: Early August 10: Mid August 11 : Late August 12: August/September 13: Early September 14: Mid September 15: Mid September 16: Late September

Comparison subo/can

subplcan

0.75/1.22** 0.76/1.25** ns ns 0.55/0.87* ns ns 0.50/0.73* ns ns ns ns ns

ns 0.87/1.25* ns 0.69/1.08* 0.50/0.87** 0.48/0.76* 0.45/0.76* 0.36/0.73** 0.50/0.88* 0.51/0.87* 0.53/0.94* 0.35/0.63* 0.28/0.54**

(-) (-)

(-) (-)

ns

0.25/0.55**1

(-) Due to non.homogeneity of variance results were not interpreted. 1 The response variable was log-transformed. comparison may be misleading. Assuming that they measured above the ground vegetation and at a similar height as in Suserup Skov the difference still does not seem unreasonable as some of these gaps were small corresponding to only one tree crown in size. When gaps are tormed branches and leaves in the canopy are removed and throughfall should logically increase, however, the creation of canopy openings also increases turbulence and hence interception losses (Neal et al. 1993). The resulting increase in throughfall thus depends on gap size (rain shadow from stand, Geiger et al. 1995) and turbulence as well as rainfall duration and -intensity (Rutter 1975). The interception loss in winter did not differ among positions. Except from the lack of leaves at positions in the intact forest, this is presumably caused by high turbulence increasing interception losses in gap positions. Further, rainfall patterns differed between summer and winter: high intensity rain storms occurred mostly in summer with peak intensities of 15-27 mm d- 1 in 2000 and 15-38 mm d- 1 in 2001, whereas peak values for winter observations were below 15 mm d- 1• Stemflow in the intact forest when bare was estimated at 6.0% of precipitation and 2.2% when in leaf This corresponds to measurements in European beech (Neal et al. 1993), but the values are lower than found by Granier et al. (2000a) in the growing season and in studies reviewed by Ladekarl (2001) for pure stands of European beech. Common ash has a more coarse textured bark than European beech and stemflow is therefore expected to be lower for

95

2000 1600 1200 800 400

0.0 160

180

200

220

260

240

Day number

1.6 •

1.2

g

SUb F

A

subo

6.

carl

0.8

LU'"

c:

eel Q.)

0.4

:2:

0.0

-L,--

160

~.-~--,.. - - ~ - - ~ ......•. - _ - - - . J

180

200

220

240

260

Day number

Fig. 8. Weekly values of the mean daily tree sap flux density (upper) and daily tree transpiration (lower) in European beech Fagus sylvatiet:l in Suserup Skov in the summer 2000. E,um is the transpiration for unit projected crown area. Error bars show ±one standard error of the mean. Inserts in the upper panel show daily sap flux density (as l}o of subo) vs available soil water below the intact forest (a) for can and (b) for subF ; see text (Dalsgaard. unpub!.).

the mixed stand than for a pure stand of European beech. For the same BA common ash had approximately half the stemflow ofEuropean beech. Differences in crown geometry between the two species as well as bark texture could contribute to the observed differences. Further, in a natural stand individual trees could be expected to have lower stemflow than in managed stands due to irregular stem shapes and the coarser texture of old and damaged trees (Levia and Frost 2003). Net-precipitation (throughfall 80% of P + stemflow 6% of P) during the winter was higher in the intact forest than the observed throughfall in the gap positions (78% of P). For gap positions without ground vegetation the netprecipitation equals throughfall, but for positions with dense ground vegetation (regenerating plants) net-precipitation was not determined. In edge positions stemflow may have been higher t.han in the intact forest thus also net-precipitation (throughfall 82% of P + stemflow 12% ofP). In Suserup Skov, throughfall in autumn was higher in the northern part of the measurement area presumably be-

96

cause of wind (from the lake, south of the measurement plot), however, this was not tested. Slavik et al. (I957, in Geiger et al. 1995) f9und a similar effect at the eastern / edge of a gap. SWC as well as RSWC were significantly higher in the gap than in intact forest positions throughout most of the year for both the upper soil layer (0-0.3 m) and for the soil down to a depth of 0.9 In expected to cover most of the rooting zone. During the winter there was no effect of the gap on RSWC and only small differences among categories for SWC. For most of the periods SWC in the southern and southeastern parts of the gap were significantly lower than remaining parts of the gap. As there was no differences in elevation among positions this indicated that soil texture may vary across the measurement area. During site installation a high stone content was observed in the southern part of the gap (unpubl., Rajzek pers. comm.). Comparisons among categories are probably best when based on the RSWC values. High throughfall at the northern gap edge (possibly caused by wind from the southern direction) as well as high stemflow on edge trees probably also contributed to these differences. Though this study showed large differences in stemHow for the two species and for trees of differing exposure, the resolution fiJr soil moisture measurement (monthly to bi-weekly measurements in an approximately 5 X 5 m grid) does not allow for a detailed study of the influence of sremHow on soil moisture. lIigher soil moisture in the gap than in intact forest positions have been found in numerous studies (Bauhus and Bartsch 1995, Ostertag 1998, Heinemann et al. 2000, Gray et al. 2002). The ratio ofgap diameter to stand height in Suserup Skov is ca 0.6. Gray et al. (2002) observed that gaps with ratios of 0.4-0.6 showed the highest response in soil moisture to gap formation compared to both smaller and larger gaps. Water use in 0-0.5 m depth was correlated with tree diameter and distance in spite of the high spatial heterogeneity in both soil and vegetation. The solution of Eq. 1 resulted in a model for water use that resembled that for fine root biomass (Nielsen and Mackenthun 1991); decreasing predicted water use with increasing distance. Ammer and Wagner (2005) used models with decreasing fine root biomass with distance (maximum reached at some distance from the stem) and Wang et al. (2002) found that fine roots were relatively evenly distributed and their densities not related to the distance to trees. Thus, the assumptions in the model used in the present study may not be optimal, but rather show a starting point based on the distribution of fine roots in European beech (Nielsen and Mackenthun 1991). The fact that the predicted water use does not lay near the 1: 1 line in Fig. 6a signalizes that the assumptions of the model are not fully valid. The site in Suserup Skov is complex in structure, which is probably the reason for the rather low r2 value. Trees have not been spaced evenly by forest management (thinning), thus the

ECOLOGICAL BULLETINS 52,2007

Suserup Skov 2000 100

... 80

21 June

sUb r

6.

sUbo

0

can

23 August

13 July

SWC 19 vol.%

SWC 14vol.%

SWC 20vol.%

E -9

40

(/)

J

20

0 1600 20

1400

"';-

1200

C';J

(/)

C?

15

1000

0....

..c 0

E (/)

Q)

800

10

600

0

E

2 0

LL

400

5

0.... 0....

200

a

0 06

12 Time

18

06

12 Time

18

06

12

18

Time

Fig. 9. Diurnal variation ofsap flux density Os' upper panel) for European beech Fagus sylllatica for three groups of trees in Suserup Skov in the summer 2000. Errors bars show ± one standard error of the mean. Soil water content (SWC) is indicated on the graphs and represents a 0-0.5 m soil profile below the forest canopy (n=olO). Air vapor pressure deficit (D) and photosynthetic global radiation (PPFD) are shown in the lower panel (Dalsgaard unpub!.).

roots may not be distributed symmetrically around the tree stems as assumed in the model. Roots of different species occupy different patches in the soil and European beech fine roots have been found to colonize nutrient rich patches more successfully than sessile oak Quercus petrea (Leuschner et al. 2001). In the unmanaged Suserup Skov decaying logs could contribute to spatial heterogeneity in soil nutrients. Common ash showed a plate root system and European beech a deeper growing heart root system (Rust and Savill 2000). In a mixed stand with European beech and Norway spruce European beech coarse roots primarily occupied the deep soil layers and Norway spruce primarily the upper soil layers (Schmid and Kazda 2001). To better predict the spatial variation ofwater use in mixed, unevenaged stands it is relevant to incorporate the effects of spatial

ECOLOGICAL BUl.LETINS 52. 2007

variability in soil nutrients as well as species-specific rooting patterns. The 19 d used for WU so and 14 d for WU90 were presumably characterized by vigorous root growth. The positions with the highest water use could have changed with time, this not being reflected in input variables. It was expected that when using WU90 , the regression of the predicted vs the observed water use would be closer to the 1: 1 line than for WU 50' especially for positions with high BA and high water use. However, this was not found. Evapotranspiration from soil and ground vegetation was not included in the model, but these were up to 0.9 mm d-] (up to 0.3 mm d~] for soil; present study, measurements in 2001). Thus, they clearly contributed to the measured water use. Though ground vegetation probably contributed less to water use in 2000 than in 2001 (plants were smaller)

97

the inclusion ofthis process is likely to improve the predictions of spatial variability of water use in the gap. In gap positions soil water content was near field capacity in the summer months, thus seepage ofwater beyond 0.5 em soil depth could also have contributed to the relatively poor model fit. Seepage during the summer can, however, be assumed to be very low at this site as it is not a sandy soil. The small rain episodes during the sample periods « 1 mm) were all lower than the water holding capacity of the canopy and of the litter layer of a temperate deciduous forest (2 mm, Wilson et al. 2000) and should not have affected the results. It is concluded that the model is still too coarse to predict the extent of root gaps. The species distribution near specific measurement positions influenced the residuals of the model thus with improvements it may be possible to detect significant species effects of rooting patterns and water use in mixed stands. In the small gap in Suserup Skov forest floor evapotranspiration did not differ between gap and intact forest positions. This is surprising knowing that more light penetrates to the floor in a gap than below the forest canopy (Ritter et al. 2005). However, the lysimeter measurements represent only a few days and these were not hot summer days. Also, this late in summer (mid-late August), the amount ofdirect radiation reaching the forest floor may be low. The smalilysimeters, chosen for the ease of installation, may not have enclosed all roots in the cases where plants were included. Evaporation may thus be underestimated. However, it is likely that uptake by roots within the lysimeter soil volume were able to meet the evaporative demand and thus compensated. For technical reasons it was unfortunately not possible to compare lysimeter measurements with changes in SWC measured by TOR. The forest floor evaporation has been shown to be driven mainly by large scale eddies penetrating the forest canopy thus being closely coupled to the vapor pressure in the ambient air (Baldocchi and Meyers 1991). This would explain the lack of differences between the intact forest and gap positions. More mea.<;urements ofsoil evaporation and forest floor evapotranspiration could be valuable to further test this hypothesis.

Fluxes Drainage of water beyond the rooting zone can be expected to be higher in gap than in the intact forest positions because ofa lower canopy interception and a lower transpiration. Higher drainage in gap positions was found by Zirlewagen and von Wilpert (2001) and by Vilhar et al. (2005), though in the latter study (growing season only) this difference was not pronounced. Rather, it was concluded that, in a natural forest with a heterogeneous stand and soil structure, drainage fluxes were not closely related to the position relative to the gap centre. A higher input from stemflow in the intact forest (and edge) than in the gap may counterbalance the differences caused by

98

throughfall and transpiration. Model examination of drainage fluxes in Suserup Skov is not completed. However, based on measurements the following can be expected: Soil moisture in gap positions remained near field capacity in summer. This indicates that drainage in autumn/winter will start earlier in gap than in intact forest positions where field capacity is reached as late as December or January at some positions. For the 2000 growing season it was estimated (Ritter et al. 2005), that lower transpiration in the gap was the major cause for the differences in soil moisture among gap and intact forest positions. The estimated amount of precipitation from mid June to September was 45 mm (the equivalent of 5 vol.% in a 0.9 m deep soil profile), whereas transpiration in the closed stand was ca 144 mm in the same period (Dalsgaard et al. unpub!.), a flux assumed to be almost lacking in the centre of the gap. A conservative estimate of forest floor evaporation of 0.2 mm d- 1 adds up to 13% ofstand evaporation in dry conditions in the same period. This is higher than closed European beech forest (Granier et al. 2000a), bur other studies in natural temperate deciduous forests have found that evaporation from the forest floor was 10-20%, thus a relatively large part of total evapotranspiration (Kelliher et al. 1992). The water-holding capacity of the litter layer was found to control the amount of forest floor evaporation (Wilson et al. 2000).

Effects and temporal trends In Suserup Skov, a higher transpiration for canopy than for subcanopy trees was found as also in other studies (Ladefaged 1963, Strelcova et al. 2002, Kastner et al. 1992), however, the differences among trees in different canopy position varied according to the amount of available soil water. Subcanopy trees near the gap benefited from the high soil moisture and maintained high transpiration throughout the summer. European beech has been reported both to be a drought sensitive species (Backes and Leuschner 2000, Aranda et al. 2000) and to exhibit a response in canopy conductance to low soil moisture similar to more drought tolerating species (Granier et a1. 2000a, b). Unfortunately it was not possible to investigate transpiration for different species in the present study. When available soil water in the intact forest approaches 40()lo of the potential it can be expected that tree transpiration is reduced (Granier et al. 2000a, b), whereas trees near the gap will maintain a higher rate of transpiration due to a higher soil moisture. In periods of water stress growth of suppressed trees are affected more negatively than dominant or open grown trees (Piutti and Cescatti 1997, Cescatti and Piutti 1998). In the beginning of the measurement period (mid June 2000) subcanopy trees below the canopy had higher or similar rates of sap flux density and transpiration than those near the gap. This was contrary to expectations because transpiration from trees at the edge of the

ECOLOGICAL BULLETINS 52,2007

gap was expected to be higher also early in the growing season because of more light reaching the crowns. Trees are able to displace their crowns toward gap centres and thereby forage for light (Mum and Bazzaz 2002). Based on results from Suserup Skov it is suggested that not only light determines the growth of trees in the edge of a canopy gap, but that the higher soil moisture availability in gaps significantly contributes to tree growth. Thus, that the spatial (and temporal) variation in available soil moisture has implications for forest succession and structure. Catovsky et al. (2002) found in closed forest stands that sap flow was a good measure of whole tree function across tree species including the overall carbon gain and stem growth. Soil nutrients have been found to be more abundant in gaps than in the adjacent intact forest (Ritter and Vesterdal 2006). In addition to higher soil moisture this may also improve the growing conditions of trees in the edge of canopy gaps. For how long do the effects of a canopy gap persist? Results from the analyses of relative soil water content (RSWC) showed that edge was a distinct category in 2000 only and in 2001 mostly was not to be distinguished from the intact forest category. Throughfall in the gap during summer was higher in 2000 than in 2001. Further, soil water content (0-0.3 m) along a transect from south to north through the gap showed that soil water content decreased from 2000 to 2001 in the northern, but not in the southern part (Ritter et al. 2005). It was observed in the field that regeneration grew rapidly especially in the northern part of the gap and tree density was higher in the northern than in the southern gap edge. Taken together this is an indication that only one year after gap formation edge trees and regenerating plants had already started to influence the gap area by root and crown growth and thereby water extraction from the soil as well as rain interception. Valverde and Silvertown (1997) found that gap closure rates are highest immediately after gap formation and that gap closure (based on hemispherical photography) is completed after ca 9 yr in temperate forests. Unfortunately the study in Suserup Skov does not allow the estimation of the time used for gap closure of either above or below ground gaps. However, the measured water use for each position fur 19 d (WU 90) in the summer 2000 had a minimum value of24.9 mm. That is > 1 mm d- 1• This is more than what could be expected from bare soil evaporation, thus roots must be active even in the central parts of the gap. Other studies have found that below ground gaps disappear quickly (1 and 4 yr after gap formation) (Veenendaal et al. 1995, Gray et al. 2002). Observations in Suserup Skov tend to support this result.

Conclusions In a small canopy gap (diameter < stand height) in Suserup Skov during the first and second growing season soil water

ECOLOCICAL BULLETINS 52,2007

content in both 0-0.3 and 0-0.9 m depth was significantly higher in gap positions than in the intact forest in spring, summer and autumn (hypothesis 1). For me relative soil water content differences were clear in summer and autumn. Soil moisture was near 90% of field capacity in the gap during the summer months compared to 60-70% in the intact forest. There was no evidence that positions north of the gap centre were drier than remaining plots due to more incoming radiation. For the relative soil water content, edge was a distinct category in summer and autumn 2000, but not in 2001 where edge was equal to the intact forest category. Annual throughfall (hypothesis 2) was 17% higher in the gap than in the intact forest (85 and 73% of P respectively). Throughfall was higher in the gap than in the intact forest in spring and summer, but not in autumn and winter. In the autumn precipitation was significantly higher north of the gap centre than in other positions. Throughfall in the gap was higher in the first than in the second summer after gap formation. Stemflow (hypothesis 3) was higher for European beech than for common ash (ca 2: 1 for unit basal area). For both species stemflow was higher when bare than when in leaf (2: 1 for unit basal area) and exposed trees (when bare) showed the highest stemflow volumes. On a stand level stemflow was 2% ofP in summer, 6% in winter and 12% in winter for exposed trees. Water use (hypothesis 4) during 19 d (0-0.5 m depth) or 14 d (0-0.9 m depth) was correlated (r = 0.43) to tree basal area and distance using a non-linear model previously used to predict spatial variability in root biomass. It was not possible to parameterize species specific models. But there was a tendency for residuals to depend on the species dominance at the measurement positions. Forest floor evapotranspiration (hypothesis 5) did not differ between gap and intact forest positions. This was contrary to the expectation. Individual tree transpiration (hypothesis 6) showed that high soil moisture in the gap enabled released subcanopy trees ofEuropean beech to sustain high transpiration rates throughout the growing season (2000), whereas transpiration rates of canopy and suppressed subcanopy trees of European beech were limited by low soil moisture. The formation of a canopy gap clearly affected the hydrological cycle but it is suggested that these changes are very short lived. Soil moisture in edge positions approached that of the intact forest in the second growing season and throughfall in the gap decreased (relative to P). The sustained transpiration in edge trees during the summer also indicate that these trees may grow vigorously. Thus, processes influencing soil moisture can affect gap dynamics through the facilitation ofgap closure. The effect ofgap formation on seepage water (ifany) should be quantified using a suitable process based model. Working in a semi-natural forest like Suserup Skov presents obvious technical and methodological problems. Variability in investigated objects (soil, trees and classes of canopy cover) is large because each measurement position

99

and each tree has its own history of disturbance) damage and competition. This variability obscures the mean values) but must also be regarded as an important part of the results. Results reported here are from the two first growing seasons after formation of one small canopy gap. More gaps should be investigated to test the generality of these results. To increase our knowledge on the interaction between above and below ground processes monitoring should best continue until both above and below ground gaps are closed. Acknowledgements - Andreas Harder, Xhevat Haliti, Valeria Vranova and Kirsten ScheIde helped with field measurements. Christian Norgaard Nielsen gave ideas for the analysis of species effects on the variation in water use. Further, I am thankful to Annemarie Bastrup-Birk, J. Bo Larsen and Karsten Raulund Rasmussen for helpful discussions and comments.

References Ammer, C. and Wagner, S. 2002. Problems and options in modeling fine-root biomass of single mature Norway spruce trees at given points from stand data. - Can. J. For. Res. 32: 581-590. Ammer, C. and Wagner, S. 2005. An approach for modeling the mean fine-root biomass ofNorway spruce stands. - Trees 19: 145-153. Aranda, I., Gil, L. and Pardos, J. A. 2000. Water relations and gas exchange in Fagus sylvatica L. and Quercus petrea (Mattuschka) Liebl. in a mixed stand at their southern limit of distribution in Europe. - Trees 14: 344--352. Backes, K. and Leuschner, C. 2000. Leaf water relations of competitive Fagus sylvatica and Quercus petrea trees during 4 years differing in soil drought. - Can. J. For. Res. 30: 335-346. Baldocchi, D. D. and Meyers, T. P. 1991. Trace gas exchange above the floor ofa deciduous forest 1. Evaporation and CO 2 efflux. - J. Geophys. Res. 96: 7271-7285. Bauhus, J. and Bartsch, N. 1995. Mechanisms for carbon and nutrient release and retention in beech forest gaps. 1. Microclimate, water balance and seepage water chemistry. - Plant Soil 168-169: 579-584. Bj0rnlund, L. and Lekfeldt, J. D. 2007. Nematode assemblages and their responses to soil disturbance differ between microsites in Suserup Skov, a semi-natural forest. - Ecol. Bull. 52: 123-131. Brockway, D. G. and Outcalt, K. W. 1998. Gap-phase regeneration in longleaf pine wiregrass ecosystems. - For. Ecol. Manage.106: 125- 139. Canham, C. D. et aL 1990. Light regimes beneath closed canopies and tree-fall gaps in temperate and tropical forest. - Can. J. For. Res. 20: 620-631. Catovsky, S., Holbrook, S. and Bazzaz, F. A. 2002. Coupling whole-tree transpiration and canopy photosynthesis in coniferous and broad-leaved tree species. - Can. J. For. Res. 32: c

295~309.

Cescatti, A. and Piutti, E. 1998. Silvicultural alternatives, competition regime and sensitivity to climate in a European beech forest. - For. Ecol. Manage. 102: 213-223. Cienciala, E. et aL 2002. The effect of a north-facing forest edge on tree water use in a boreal Scots pine stand. Can. J. For. Res. 32: 693-702.

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Einhorn, K. S. 2007. Growth and photosynthesis of ash Fraxinus excelsior and beech Fagus sylvatica seedlings in response to a light gradient following natural gap formation. - £col. Bull. 52: 147-165. Einhorn, K. S., Rosenquist, E. and Leverenz, J. 2004. Photoinhibition in seedlings of Fraxinus and fagus under natural light conditions: implications for forest regeneration? - Oecologia 140: 241-251. Emborg, J. 1998. Understorey light conditions and regeneration with respect to the structural dynamics ofa near-natural temperate deciduous forest in Denmark. - For. £coL Manage. 106: 83-95. Emborg, J., Christensen, M. and Heilmann-Clausen, J. 1996. The structure of Suserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Landscape Res. 1: 311333. Emborg, J., Christensen, M. and Heilmann-Clausen, J. 2000. The structural dynamics of Suserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Ecol. Manage. 126: 173-189. Epron, D. et al. 1999. Soil CO 2 efflux in a beech forest: dependence on soil temperature and soil water content. - Ann. For. Sci. 56: 221-226. Epron, D., Ngao, J. and Granier, A. 2004. Interannual variation of soil respiration in a beech forest ecosystem over a six-year study. -Ann. For. Sci. 61: 499-505. Geiger, R., Aran, R. H. and Todhunter, P. 1995. The climate near the ground, 5th ed. - Friedr. Vieweg and Sohn, W'iesbaden, Germany. Granier, A. 1985. Une nouvelle methode pour la mesure du flux de seve brute dans Ie tronc des arbres. - Ann. Sci. For. 42: 193-200. Granier, A. 1987. Evaluation of transpiration in a Douglas-fir stand by means of sap flow measurements. - Tree Physiol. 3: 309-320. Granier, A. et al. 1996. Transpiration of trees and forest stands: short and long-term monitoring using sapflow methods. Global Change BioI. 2: 265-274. Granier, A., Biron, P. and Lemoine, D. 2000a. Waterbalance, transpiration and canopy conductance in two beech stands. - Agricult. For. Meteorol. 100: 291--308. Granier, A., Loustau, D. and Breda, N. 2000b. A generic model of forest canopy conductance dependent on climate, soil water availability and leaf area index. - Ann. For. Sci. 57: 755765. Granier) A. et al. 2003. Deciduous forests: carbon and water fluxes, balances and ecophysiological determinants. - In: Valentini, R. (ed.), Fluxes ofcarbon, water and energy ofEuropean forests. Ecol. Stud. 163: 55-70. Gray, A. N., Spies, T. A. and Easter, M. J. 2002. Microclimate and soil moisture responses to gap formation in coastal Douglas-fir forests. Can. ]. For. Res. 32: 332-343. Hahn, K., Madsen, P. and Lindholt, S. 2007. Gap regeneration in four natural gaps in Suserup Skov - a mixed deciduous forest reserve in Denmark. - Eco1. Bull. 133-145. Heilmann-Clausen, J. et al. 2007. The history and present conditions of Suserup Skov - a nemoral, deciduous forest reserve in a cultural landscape. - Eco1. Bull. 52: 7-17. Heinemann, K, Kitzberger, T. and Veblen, T. T 2000. Influence of gap microheterogeneity on the regeneration of Nothofagus pumillo in a xeric old-growth forest of northwestern Patagonia, Argentina. Can. J. For. Res. 30: 25~31.

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Herwirz, S. R. 1986. Infiltrations-excess caused by stemflow in a cyclone-prone tropical rainforest. - Earth Surf. Proc. Lindf.

1]: 401-412. Herwitz, S. R. and Levia Jr, D. F. 1997. Mid-winter stemflow drainage from Bigtooth aspen (Populus grandidentata Michx.) in central Massachusetts. - Hydrol. Proc. 11: 169-

175. Kelliher, F. M. et al. 1992. Evaporation, xylem sap flow, and tree transpiration in a New Zealand broad-leaved forest. Agricult. For. Meteorol. 62: 53-73. Kastner, B. et al. 1992. Transpiration and canopy conductance in a pristine broad-leaved forest of Nothofagus: an analysis of xylem sap flow and eddy correlation measurements. Oecologia 91: 350-359. Kastner, B., Granier, A. and Cermak, J. 1998. Sapflow measurements in forest stands: methods and uncertainties. Ann. Sci. For. 55: 13-27. Ladefoged, K. 1963. Transpiration of forest trees in dosed stands. Physiol. Plant. 16: 378-414. Ladekarl, U. L 2001. Soil moisture, evapotranspiration and groundwater recharge in forest and heathland. - Ph.D. thesis, Vol. 11, Aarhus Geoscience, Dept of Earth Sciences, Univ. of Aarhus, Denmark. Lang, S. 1999. Okophysiologische und anatomische Untersuchungen zum Saftfluss in verschiedenen Splintholzbereichen von Fagus sylvatiea 1. - Ph.D. thesis, Fakultat fur Bio- und Geowissenschaften der Univ. Karlsruhe. Leuschner, C. et al. 2001. Root competition between beech and oak: a hypothesis. Oecologia 126: 276-284. LeviaJr, D. E and Frost, E. E. 2003. A review and evaluation of stemflow literature in the hydrologic and biogeochemical cycles of forested and aricultural ecosystems. - J. Hydro!. 274:

1-29. Linskens, H. F. 1951. Niederschlagsmessungen unter verschiedenen Baumkronentypen im belaubten u. unbelaubten Zustand. - Ber. D. Bot. G. 64: 15-221. Madsen, P. 1994. Growth and survival of Fagus sylvatiea seedlings in relation to light intensity and soil water content. - Scand. ]. For. Res. 9: 316-322. Madsen, P. 1995. Effects of soil water content, fertilization, light, weed competition and seedbed type on natural regeneration of beech (Fagus sylvatica). - For. Ecol. Manage. 72: 251-264. McGuire, J. P. et al. 2001. Gaps in a gappy forest: plant resources, longleaf pine regeneration, and understory response to tree removal in longleaf pine savannas. - Can. J. For. Res. 31:

765-778. Muller, K. H. and Wagner, S. 2003. Fine root dynamics in gaps of Norway spruce stands in the German Ore Mountains. Forestry 76: 149-158. Muth, C. and Bazzaz, E A. 2002. Tree canopy displacement at forest gap edges. Can. J. For. Res. 32: 247-254. Neal, C. et al. 1993. Relationships between precipitation, stemflow and throughfall for a lowland beech plantation, Black Wood, Hampshire, southern England: findings on interception at a forest edge and the effects of storm damage. - J. Hydrol. 146: 221-233. Nielsen, C. N. and Mackentun, G. 1991. Die horiwntale Variation der Feinwurzelintensitat in Waldb()den in Abhangkeit von der Bestockungsdichte. ~ AUg. Forst- Jagdztg. 162: 112-119. Nizinsky, J. J. and Saugier, B. 1988. Mesures et modelisations del'interception nette dans une futaie de chenes. - Acta Eco1., Ecol. Plant. 9: 311-329.

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Ostertag, R. 1998. Belowground effects ofcanopy gaps in a tropical wet forest. - Ecology 79: 1294-1304. Peck, A. and Mayer, H. 1996. Einfluss von Bestandesparametern auf die Verdunstung von Waldern. - Fors£v.'. Cbl. 115: 1-9. Piutti, E. and Cescatti, A. 1997. A quantitative analysis of the interactions between climatic response and intra specific competition in European beech. - Can. J. For. Res. 27: 277-284. Ritter, E. 2007. Nitrate in soil solution and nitrogen availability in litter and soil after gap formation in the semi-natural Suserup Skov and two managed beech Fagus sylvatica forests in Denmark. - Eco1. Bull. 52: 103-111. Ritter, E. and Vesterdal, L. 2006. Gap formation in Danish beech (Fagus sylvatiea) forests of low management intensity: soil moisture and nitrate in soil solution. Eur. J. For. Res. 125:

139--150. Ritter, E., Dalsgaard, L. and Einhorn, K. S. 2005. Light, temperature and soil moisture regimes following gap formation in a semi-natural beech-dominated forest in Denmark. For. Eco1. Manage. 206: 15-33. Roberts, J. et al. 1980. Seasonal changes in leaf area, stomatal and canopy conducrances and transpiration from bracken below a forest canopy. - J. Appl. Ecol. 17: 409~22. Runkle, J. R. and Yetter, T. 1987. Treefalls revisited: gap dynamics in the southern Appalachians. -- Ecology 68: 417~24. Rust, S. and Savill, P. S. 2000. The root systems of Fraxinus excelsior and Fagus sylvatica and their competitive relationships. Forestry 73: 499-508. Rutter, A. J. 1975. The hydrological cycle in vegetation. Veg. Atmosphere 1: 111-154. Schmid, 1. and Kazda, M. 2001. Vertical distribution and radial growth of coarse roots in pure and mixed stands of Fagus sylvatica and Pieea abies. - Can. J. For. Res. 31: 539-548. Schcmning, P. 1985. Equipment for drainage of soil samples. Tidsskrift for Planteavls Specialserie 1762: 3-25, in Danish. SlaVIk, B., Slavikova, J. and Jenfk, J. 1957. Okologie der gruppenweisen Verjungung eines Mischbestandes. - Rozpravy Tschechoslow. Akad. 67: 2, in Czech with German summary. Strelcova, K., Matejka, F. and Mindas, J. 2002. Estimation of beech tree transpiration in relation to their social status in forest stand. - J. For. Sci. 48: 130-140. Thomsen, A. 1994. Program AUTOTDR for making automated TDR measurements of soil water content. User's guide, ver. 01, January 1994. - SP report no. 38, Ministry of Agriculture, Danish Inst. of Plant and Soil Science, Denmark. Thomsen, A. et al. 2003. Vandkredsl0b i skove. - For. Landscape Res. 33: 97-112, in Danish. Tognetti, R., Michelozzi, M. and Borghetti, M. 1994. Response to light of shade-grown beech seedlings subjected to different watering regimes. -Tree Physiol. 14: 751-7 58. Topp, G. C, Davis,]. 1. and Annan, A. P. 1980. Electromagnetic determination ofsoil water content: measurements in coaxial transmission lines. - Water Resour. Res. 16: 574-582. Valverde, T. and Silvertown, J. 1997. Canopy closure rate and forest structure. - Ecology 78: 1555--1562. Veenendal, E. M. et al. 1995. Differences in plant and soil water relations in and around a forest gap in West Mrica during the dry season may influence seedling establishment and survival. - J. Eco1. 83: 83-90. Vejen, E, Madsen, H. and Allerup, P. 2000. Korrektion for fejlkilder pa miling af nedb0r. - Danmarb Meteorologiske Inse, Teknisk Rapport 00-20, in Danish.

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Vejre, H. and Emborg, J. 1996. Interactions between vegetation and soil in a near-namral temperate deciduous forest. - For. Landscape Res. 1: 335-347. Vilhar, U. et al. 2005. Gap evapotranspiration and drainage fluxes in a managed and a virgin dinaric silver fir-beech forest in Slovenia: a modeling study. - Em. J. For. Res. 124: 165-175. Wang, X. L. et ai. 2002. Root structure of western hemlock and western redcedar in single- and mixed-species stands. - Can. J. For. Res. 32: 997-1004.

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Weisberg, S. 1985. Applied linear regression, 2nd ed. - Wiley. Wilson, K. B., Hanson, P. J. and Baldocchi, D. D. 2000. Factors controlling evaporation and energy partitioning beneath a deciduous forest over an annual cycle. - Agricult. For. Meteoral. 102: 83-103. Zirlewagen, D. and von Wilpen, K. 2001. Modeling water and ionfluxes in a highly structured, mixed-species stand. - For. Ecol. Manage. 143: 27-37.

ECOLOGICAL BULLETINS 52, 2007

Ecological Bulletins 52: 103-111, 2007

Nitrate in soil solution and nitrogen availability in litter and soil after gap formation in the semi-natural Suserup Skovand two managed beech Fagus sylvatica forests in Denmark Eva Ritter

Ritter, E. 2007. Nitrate in soil solution and nitrogen availability in litter and soil after gap formation in the semi~natural Suserup Skov and rwo managed beech Fagus sylvatica forests in Denmark. - Ecol. Bull. 52: 103-111.

This paper is a review of different gap studies carried out in the semi-natural Suserup Skov and rwo managed beech Fagus sylvatica forests in Denmark (gap diameters 18~33 m). The effect of gap formation on N release from litter decomposition and soil mineralization and nitrification, N03-N concentrations in soil solution, and losses ofN03-N with seepage water investigated in the different studies showed that differences between the effects observed in Suserup Skov and the managed forests were generally small. Gap formation changed N turnover processes in litter and soil only moderately, but caused a significant increase in concentrations and losses ofN0 3-N in soil solution in the gaps. While the relative increase was similar at all sites, absolute NO,-N concentrations and losses were dearly higher in the semi-natural forest than in the two managed forests. This indicates that the N cycle of an unmanaged forest ecosystem is not necessarily dosed. Overall, the effect of gap formation on the processes investigated was less pronounced than expected. Root distribution, regeneration, forest structure, and soil-related factors were suggested to modifY the impact of the canopy opening.

E Ritter ([email protected]), The Agricultural Univ. ofIceland, Hvanneyri, lS-311 Borgarnes, Iceland

Disturbances, whether natural or human induced, smallscale or large-scale, are known to alter nitrogen (N) cycling in forest ecosystems by changing e.g. microclimate, hydrology, and microbial activity (Gessel et aL 1973, Krause 1982, Mooney and Godran 1983). A typical small-scale disturbance in temperate forest ecosystems is the formation of a gap. It occurs when single trees or small tree groups are injured or killed, or parts of living trees in the upper canopy layer are removed. Below-ground responses are referred to as root gaps, indicating that fine root density in gaps differs from that of the dosed forest (Wilczynski and Pickett 1993, Brockway and Outcalt 1998).

Copyright © ECOLOGICAL BULLETINS, 2007

A gap reduces the interception of radiation and precipitation by the canopy (Geiger et al. 1995). Together with reduced water uptake by tree roots this results in higher soil moisture levels in gaps compared to the closed forest (Wright et al. 1998, Dalsgaard 2007). Increased water availability concurrent with reduced nutrient uptake by roots in the gap may increase drainage fluxes and thus export of nutrients in soil solution. Soil temperature is altered after gap formation since it among other factors depends on irradiance and the water content of the soil. These microclimatic changes and the influence of plant roots may have consequences for microbiological processes

103

like decomposition and mineralization and hence nutrient availability (Cassman and Munns 1980, Cheng and Bledsoe 2004). It is generally assumed that N turnover processes increase after tree felling, especially after clear-cutting, result~ ing in known negative effects like increased leaching of nitrate (N0 3-). Studies of different harvesting systems have indicated that a less intensive removal of the forest cover can have a moderating effect on the N turnover in forest ecosystems (Prescott 1997). Nature based forest management seeks therefore to keep disturbances caused by harvesting to a minimum to avoid extreme changes in the physical environment and the biogeochemical cycling. The aim is to mimic small-scale disturbances observed in natural forest ecosystems (Attiwill 1994), and gap formation is suggested as one possible silvicultural tool. However, studies on changes in the internal N cycle after natural disturbances in temperate forest ecosystems not subject to human intervention are scarce. Most studies are carried out in managed forests, investigating the impact of different management practices on N mineralization rates and N availability. In the temperate region ofwestern Europe, this lack of studies in natural forests is partly due to the limited number of old-growth and non-intervention forests, and partly to a greater interest in the regulation of managed forest ecosystems to improve their productivity. However, the increasing awareness of the need for sustainability in forestry calls for better knowledge about ecological processes and natural dynamics in forest ecosystems.

The importance ofstudies in undisturbed forests as a reference for sustainable forestry has therefore to be emphasised (Hackl et al. 2004). In this review the results of different case studies on the effect ofgap formation on processes in the N cycle of forest ecosystems are discussed and related to each other. The case studies took place in a semi-natural forest (Suserup Skov) and two stands in traditionally managed forests. The aim is to indicate the possible range ofeffects ofgap formation in forests of different management intensities, taking into account that a direct comparison between the different study sites is not possible. The results of the studies presented in this review are published in Ritter (2005), Ritter and Bj0rnlund (2005), Ritter et al. (2005a), and Ritter and Vesterdal (2006).

Materials and methods Study sites The studies were carried out in three European beech fa-

gus sylvatica forests of two different structures and management intensities located on central Zealand, Denmark (Table 1) One forest was Suserup Skov (55°22'N, 11°34'£) which is a non-intervention, heterogeneous forest reserve. This site is more closely described in Heilmann-Clausen et al. (2007). The other two forests were traditionally managed forest stands (55°31 'N, 11 °54 'E) which were homo-

Table 1. Description of the forest structure, the gaps, and the study periods of the different investigations carried out at the three study sites. Suserup Skov

Ravnsholte Skov

Hejede Overdrev

Management system

Semi-natural

Forest structu re

Highly heterogeneous 31 m December 1999 Natural (storm) 1 18 m

Traditionally managed Homogeneous

Traditionally managed Homogeneous

1: north-south 1: west-east

27 m January 2001 Felling 2 small gap: 19 m large gap: 27m small gap: 0.7 large gap: 1.0 1: north-south 1: west-east*

28m January 2001 Felling 2 small gap: 20 m large gap: 33 m small gap: 0.7 large gap: 1.2 1: north-south

Nov. 2001-Nov. 2002 Feb. 200l-Jan. 2002 July 200().....()ct. 2002 July 2000-0ct. 2002

Nov. 2001~Nov. 2002 Apr. 200l~May 2002 May 200l-Apr. 2003 Sep. 200l-Apr. 2003

Not measured Not measured July 2001-Apr. 2003 Oct. 2001-Apr. 2003

Average canopy height Time of gap formation Way of gap formation No. of gaps Gap diameter Gap diameter to canopy height ratio No. and direction of transects Investigations and study periods Litter decomposition N mineralization N03-N in soil solution N03-N leaching

0.6

* In Ravnsholte Skov, only sampling of soil solution for N03-N investigation was carried out along both transects. All other investigations were restricted to the north-south transect.

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ECOLOGICAL BULLETINS 52. 200/

geneous in rerms of structure and age class: a 75-yr old stand (3.7 hal in Ravnsholre Skov (a forest of ca 200 hal and a 80-yr-old stand (3.9 hal in Hejede Overdrev (a forest of ca 275 hal. All three sires are locared on nutrienr-rich soil developed from glacial till.

cover contained patches ofgrass (mainly D«hampsUlfkxuosa) and vasious sedge speties (c,= spp.). In the small gap, Rubus idMus developed sooo afrer gap formation. All tbre<: gap sites were fenced to avoid disturbances by visitors of the forest or browsing by detS.

The gaps

Experimental design

Gap diameters of the five gaps included in the study varied from 18 to 33 m (Table I). The gap in Suserup Skov was created narurally during a severe storm on 3 December 1999 when a large beech rree losr mosr of irs crown and a number of smaller beech trees were uproored. The irregularly formed gap was characterized by a high regeneration potential ofash Fraxinus ",,,/sior (Fig. 1). Due to the protected StatUS of me forest, none of the fallen trees were removed &om the site. In cach of the twO managed foresrs, twO almost circular gaps (a small and a large one) were created by felling in January 200 I. Trees were removed from the gaps, thereby trying to avoid soil disturbance. Advanced but scattered regeneration of sycamore maple A"r psrodoplatanus occurred in Ravnsholte Skov already before gap formation. In the large gap in Hejede Overdrev, ground vegetation

lnvescigacions discussed in this review include N release from litter decomposition (total nitrogen (N», soil mineralization and nitrification rates (inorganic nitrogen (Nmlo ) and nitrate-nitrogen (NO,-N») in 0-10 em depth of mineral soil as well as NO,-N concentrations in soil solution below the rooting wne (90 cm depth) carried out in Suserup Skov and Ravnsholre Skov. In Hejede Overdsev, only soil solution fot analysis of NO,-N concenrrations was sampled. Losses ofNO,-N with seepage warer were calculated for all three sites using the water balance model WATBAL (Starr 1999). The application ofthe model on conditions met in the gaps is described in Ritter et a1. (2005a) and Rittet and Vesterdal (2006). Measurements were carried out once a month until 16-35 monrhs afrer gap formation - depending on processes and study sites (Table I). Sample plors were locared

Fig. 1. The gap in Suserup Skov in summer 2000 with early regeneracion ofash Fraxinus txct/sior. Gap formation took place during a severe smrm in December 1999.

ECOLOGICAL BUllETINS 52, 2007

105

mg N g-I under dosed canopy (Ritter 2005). There was no significant difference between the small and the large gap in this managed forest.

along transects running through the approximate centre of each gap, with a maximum extension into the surrounding forest of 19-42 m from the centre of the gap. The distance between sample plots was 3~5 m in gaps, but somewhat larger under closed canopy. In Suserup Skov and Ravnsholte Skov a north-south and a west-east transect were established. However, litter and soil investigations in Ravnsholre Skov wefe only carried out along the north-south transect. Similarly, soil solution in Hejede Overdrev was only collected along a north-south transect. Statistical analysis of some processes was carried out separately fc)r periods defined by the developmental status of the tree leaves. For simplicity, these periods are referred to as growing season (trees in full leaf, June-October) and dormant season (trees without leaves or not yet fully developed leaves, November-May). Gap effects were based on the assumption that pre-gap conditions were represented by sample plots below the closed canopy, because conditions of the variables studied before gap formation were unknown. For a detailed description of the experimental set up and the analyses see also Ritter (2005), Ritter and Bj0rnlund (2005), Ritter et al. (2005a), and Ritter and Vesterdal (2006).

Nitrogen mineralization Spatial and temporal variations in mineralization and nitrification rates were high. In some months, immobilization occurred at the same time as N release in different sample plots. Overall, mineralization was only moderately stimulated at all study sites. Nitrification and mineralization rates in the two gaps in Ravnsholte Skov tended to be increased during the growing season. The difference between the large and the small gap illustrated in Fig. 3 was not significant. In average 28 kg N0 3-N ha-- 1 and 40 kg N min ha- I were released in the gaps, but only 18 kg N0 3-N hal and 20 kg N min ha- I under closed canopy (Ritter 2005). However, a gap effect was not significant and even less during the dormant season. In Suserup Skov, the amount of mineralized N was ofsimilar magnitude during the growing season as in the managed forest being ca 30 kg N rnin ha- I both in the gap and under closed canopy. Nitrification was higher with almost 50 kg NOJ-N ha- 1 in the gap and slightly less under closed canopy (Fig. 3). No strong effect of gap formation was found in either season (Ritter and Bj0rnlund 2005).

Results Nitrogen availability in litter

Nitrate concentrations in soil solution Nitrogen release from litter material was not affected by gap formation, but net release was different between the semi-natural and the managed forests. In Suserup Skov, a very small annual N release of 0.3 mg N g-lleaflitter yr- 1 was observed (average of all plots) (Ritter and Bj0rnlund 2005). In contrast, N was immobilized in Ravnsholte Skov (Fig. 2), in average 2.4 mg N g-l litter in the gaps and 3.0

1 year of decomposition

Concentrations were generally higher in gaps than under closed canopy, and the relative differences between gap and forest was similar at all sites. :However, NO)-N concentrations in the semi-natural forest were much-higher than in the managed forests. Average monthly concentrations in Suserup Skov were highest for the dormant season 20001

2 years of decomposition

2 ,..-------------------,------------, _ 'i:.' Q)

under closed canopy in the gap

--;---r~~.=FJ-------+-

~ '0)

a r--.---

Z

g -1 Q)

~ ~ ~

z

-2 -3

-4

L-

-,-

Suserup

106

---,

Ravnsholte small gap

---,-

Ravnsholte large gap

--J.

~------l

Suserup

Fig. 2. Release ofN from beech foliar litter at the semi-natural Suserup Skov and the managed Ravnsholte Skov. Negative values indicate immobilization. The high standard deviation in the gap in Suserup Skov in the first year of decomposition is due to one single sample plot with a release of 3.6 mg N gl litter, while immobilization occurred in the other gap plots.

ECOLOGICAL BULLETINS 52, 1007

Suserup Forest

Suserup Forest

'5:-, 60 _ -

closed canopy (n;;; 7) c::==J gap (n "" 5)

-

c::==J

closed canopy (n = 7) gap (n = 5)

'('0

.r:

E 40

I~

z

"0 (l)

~ 20 :t= Z

o 60

_

..c

Ravnsholte, small gap

'>.,

closed canopy (n = 4) gap (n = 3)

z

ill

"0

().) i;::

20

~ 20

c ~

1_

z

I

01------

60

..c

_

'

I

01------

Ravnsholte, large gap

'>.,

Ravnsholte, large gap

closed canopy (n = 4) gap (n'" 3)

'>.,

60

'('0

-

closed canopy (n"" 4) gap (n "" 3)

..c

~

"2 ro
closed canopy (n = 4) gap (n'" 3)

0)

"0

Z

===:J

::s 40

40

,Dl

'('0

_

..c

CJ)

m (jj

60

'('0

.Y'.

Z

01-----

-,-J---'----,,---

Ravnsholte, small gap

..... >, "7('0

II

I--~---

0)

::s 40

40

Z "0

,Dl

().)

20

'§ 20

:t=

c ~

Z

o '--~--growing

season

dormant

season

growing season

dormant season

Fig. 3. Average of accumulation of mineralized N (NH 4-N+N03-N) (left:) and accumulated nitrified N (N(\-N) (right) in 0-10 em of mineral soil under dosed canopy and in the gap during growing seasons and dormant seasons, respectively in Suserup Skov (seminatural forest), and the small gap and the large gap in Ravnsholte Skov (managed forest). Error bars are 1 standard error.

2001 with 34 mg N0 3-N 1-1 in the gap centre (without plots located along the gap edge) and 17 mg NO,,-N 1-1 under dosed canopy. They decreased slightly with time after gap formation. During the growing season 2002, an average of 14 mg NO,C)-N 1-1 and 5 mg N0 3-N I-I was measured in the gap centre and under dosed canopy, respectively (Ritter and Vesterdal 20(6) . In the two managed forests, monthly average N0 3-N concentrations of the whole study period and all four gaps were 7.2 mg N0 3-N 1-1 compared to 2.2 mg N0 3-N 1-1 under dosed canopy (Ritter et al. 2005a). Overall N0 3-N levels were lowest in the gap where ground vegetation was almost absent, the large gap in Hejede Overdrev (Ritter et al. 2005a). There was no effect of gap size among the gaps in the managed forests.

ECOLOGICAL BULLETINS 52,2007

Nitrate losses with soil solution Leaching loss ofN0 3-N was increased in all gaps. The difference between gap and closed forest was most pronounced in the gaps of the managed forests. In contrast, the total loss of N0,C)-N was highest in the semi-natural forest and presumably only little aHected by gap formation. In Suserup Skov, N0 3-N losses from the gap area decreased from 38 kg N0 3-N in the dormant season 2000/ 2001 to 30 kg N0 3-N ha- 1 in the dormant season 20011 2002 (the first two winters after gap formation). The highest losses during growing seasons (24 kg N0 3-N ha- 1) were measured in 2001, a year with a wet late summer. No losses occurred in the following third growing season after gap

107

formation (Ritter and Vesterdal 2006). Overall, total losses from the gap were about 4-fold or 63 kg N03-N ha- I higher than under the closed canopy in the first two years after gap formation (Ritter and Vesterdal 2006) . This difference had disappeared in the third year Oanuary-October) (Fig. 4). In the four gaps in the two managed forests, average N0 3-N losses from the gaps ranged from 1.1 kg N0 3-N ha- I (growing season 2002) to 2.2 kg NC\-N ha- I (dormant season 200112002) (Ritter et al. 2005a). For the whole study period, losses were 3- to 13-fold or up to 30 kg N0 3-N ha- I higher in the four gaps than in their surrounding forests and thus significantly increased (Fig. 5). There was no effect of gap size, but site specific differences were indicated by up to 2.5 times lower N0 3-N losses per ha from one of the large gaps compared to the three other gaps (Ritter et al. 2005a).

Discussion Litter decomposition The relatively short time span of these two studies seems to be too short to draw any general conclusion about the effect of gap formation on processes in the litter layer. Also Bauhus (1996) reported no effect ofgap formation on forest floor mass and N concentrations after only 21 months, while effects were observed in studies investigating forest floor parameters for a longer period of time. Eight years after gap formation, a significant effect on forest floor mass was reported by Bauhus et al. (2004). In the Suserup Skov, overall a small net N release from litter occurred concurrent with a decrease in C:N ratios after both one and two years of decomposition (Ritter and Bj0rnlund 2005). Berg and Ekbohm (1983) reported N immobilization and a

100

'"8

80

'C

Suserup (semi-natural) r-----~~.- - --.-----..... -.~- - - -----------.. ---.

I _ closed canopy ~ [=----:.J gap

Q)

0-

'co ..c ZI

60

subsequent decrease in C:N ratios after one year ofdecomposition of fresh beech litter material with relatively low N concentrations as seen in the gaps of the managed Ravnsholte Skov (immobilization). This net immobilization may in the following year change to net release of N, as reported by Berg and Staaf (1981). They found that the absolute amount ofN may increase to a critical level before a net release of N (mineralization) starts. This indicates that changes in forest floor properties may occur in later years, depending on degree and rate of the closure of the canopy gap.

Nitrogen mineralization Gap studies have shown both increased and decreased N mineralization rates in gaps, as well as spatial differences throughout a gap (Mladenoff 1987, Bauhus and Barthel 1995, Bauhus 1996). It seems that changes in N mineralization are site specific and micro-environmental effects have to be considered closely in the discussion ofN availability in gaps. While Christ et al. (1997) reported increased mineralization rates in those parts of a gap where soil temperature or soil moisture were increased, Bauhus and Bartsch (1995) found no influence of soil temperature on mineralization rates. Also in the present studies, mineralization and nitrification did not show a clear response to soil temperatures or the continuously high soil water content in the gaps (Ritter 2005, Ritter and Bj0rnlund 2005). However, the tendency of increased mineralization rates in the gaps in Ravnsholte Skov during the growing season imply overall better conditions for microorganisms than under closed canopy. The generally small difference between gap and closed forest and the high variation in mineralization rates among sample plots may indicate that N mineralization was affected by factors on a smaller scale, independent of gap formation. An impact of roots in the gap, e.g. on substrate quality and C availability, cannot be excluded. There may have been sample plots not influenced by remaining or expanding living roots in places without regeneration or next to uprooted trees. Furthermore, populations ofdecomposers, soil texture and thickness of the organic layer varied among plots, especially in Suserup Skov (Ritter and Bj0rnlund 2005) .

40 I(")

oZ

0>

..:.::

-~II1

Nitrate in soil solution - concentrations and losses ___J

1st+2nd 3rd year after gap formation Fig. 4. Total losses ofNOJ-N in Suserup Skov. Losses are illustrated as the sum of the first two years and of the third year after gap formation, respectively.

Similar high N0 3-N concentrations as in the present studies were found in mixed and pure stands of European beech, Norway spruce Picea abies, and silver fir Abies alba by von Wilpert et al. (1996) and Bartsch et a1. (1999), and also the tendency ofincreased N0 3-N losses from the gaps is consistent with other gap studies (Bartsch 2000). Never-

Ravnsholte (managed)

Hejede Overdrev (managed)

50 _

40

gap

30

.... I

I-I I I

co 20

I !

o

Z ~

I

I

I

i

!:

Iii

-JJ -LlLL---!~~_-----L-_ I

0

closed canopy ----" gap

I

Z

10

r::

I

..c

1C")

_

closed canopy

large gap

small

gap

large gap

small

gap

Fig. 5. Total losses of N0 3-N from the small and the large gaps, respectively, in the managed stands in Ravl1sholte Skov and Hejede Overdrev. Losses are illustrated as the sum of the total model period of 20 months.

the1ess, N0 3-N concentrations in Suserup Skov were high compared to other Danish forest sites not managed for wood production. A study on N0 3-N concentrations below the rooting zone reponed 0.7 mg N0 3-N I-I for such forest sites (Callesen et al. 1999). .High N0 3-N concentrations below the rooting zone are considered as an indicator for excess N0 3-N production (Gundersen 1998) and may occur when N mineralization rates exceed N consumption by plants (Smethurst and Nambiar 1990, Hobra et al. 2001). However, in the present studies N mineralization was not significantly stimulated in the gaps. There is also little evidence that N deposition had caused increased N0 3 -N levels in gaps. Wet N deposition at the study sites (ca 15-20 kg N ha yr- 1) was in the medium range of European ecosystems (Gundersen et al. 1998), and the measured input of N with precipitation was not higher in gaps than under closed canopy (Ritter et al. 2005a, Ritter and Vesterdal 2006). The nevertheless significant increase in N0 3 -N must therefore derive from other sources. Removal of the canopy cover increases water fluxes out of the rooting zone, but decreases N uptake by plant roots (Bosch and Hewlett 1982, Hornbeck et al. 1997). Leaching of N0 3- may decrease again as soon as available N is utilised by developing understorey vegetation and microbial activity (Barg and Edmonds 1999, Bartsch et al. 1999). However, in the present studies N0 3-N losses were lowest in the gap with least ground vegetation cover (Ritter et al. 2005a). This could be due to the more exposed location of this gap which may have inhibited N turnover processes, as indicated by the mor layer at this site. Furthermore, in Suserup Skov N0 3-N concentrations and losses were high both in the gap and under closed canopy

ECOLOGICAL BULLETINS 52. 2007

despite a vigorously growing regeneration in the gap and the remaining living roots of the old beech tree which had created the gap. The advanced ash regeneration may, however, explain the slight decrease in N0 3-N in the gap in the third growing season after gap formation. At that time, regeneration had reached a height of ca 1.5 m (Ritter et al. 2005b), and N demand of young trees is high until they reach canopy closure (Miller 1990). This indicates that a rapid closure of the gap (above and belowground) either by ground vegetation, regeneration or lateral growth of the surrounding trees should be achieved in order to avoid long-lasting losses ofN0 3-N. In this context, gap size can become a relevant fact~r. Although no effect of gap size was found on N03-N losses in the two managed forests in the first years after gap formation, it can be assumed that the small gaps are closed earlier than the large ones (Valverde and Silvertown 1997) and that N0 3-N loss thus stop earlier as well. It is furthermore suggested that the status of Suserup Skov as a long-term non-intervention forest reserve may have resulted in a high storage of N in living biomass and soil. Long rotation periods were shown to reduce the output of nutrients with export of biomass in managed forests (Huttl and Schaaf 1995). Suserup Skov had the longest period of undisturbed growth and no removal of biomass by human intervention of all sites investigated. This assumption is supported by the results of a study in a traditionally managed forest in the vicinity of Suserup Skov, hence a forest receiving comparable amounts of N input by throughfall, in which N0 3-N concentrations below the rooting zone were still < 1 mg 1-] (Beier et al. 2001). Thus, it seems that the internal N cycle afan ecosystem is important for the N balance after disturbances.

109

Conclusion The effect ofgap formation on processes in the N cycle was much less pronounced than expected, both in the seminatural and the managed forests. There was not much difference between gaps and closed forests except in soil solution N0 3-N. Large variation on a small spatial scale may have reduced the difference. Nitrogen turnover in litter and soil was only moderately stimulated, more so in the managed than in the semi-natural forest. While the relative increase in NOi-N concentrations in gaps was similar in all forests investigated, Suserup Skov had the highest nitrate concentrations and losses in tOtal. This was independent of gap formation. It indicates that the N cycle of this long-term non-intervention forest is not necessarily more closed than in traditionally managed forests. Generally, differences between changes in processes in the N cycle in the semi-natural and the managed forests were small, and the knowledge obtained from natural forest ecosystems may thus be regarded as being useful in nature-based forest management. The results emphasise, however, that forest sites have to be considered individually since regeneration potential and the internal N cycle of the forest ecosystems appear to be important for the overall changes in the N cycle. Furthermore, for a successful application of gap regeneration to forest management, not only the effect ofgap formation has to be understood profoundly, but also the role ofgap closure, including below-ground root gaps as well as above-ground canopy gaps.

References AttiwiIl, P. M. 1994. The disturbance of forest ecosystems: the ecological basis for conservative management. - For. Eco!. Manage. 63: 247-300. Barg, A. K and Edmonds, R. L. 1999. Influence of partial cuttingon site microclimate, soil nitrogen dynamics, and microbial biomass in Douglas-fir stands in western Washington. Can.]. For. Res. 29: 705-713. Bartsch, N. 2000. Element release in beech ("fagus sylvatica L.) forest gaps. - Water Air Soil Pollut. 122: 3--16. Bartsch, N., Bauhus, ]. and Vor, T 1999. Auswirkungen von Auflichtung und Kalkung auf das Sickerwasser in einem Buchenbestand (Fagus sylvatica L.) im SoIling. - Forstarchiv 70: 218-223. Bal1hus,]. 1996. C and N mineralization in an acid forest soil along a gap-stand gradient. - Soil Bioi. Biochem. 28: 923932. Bauhus, ]. and Barthel, R. 1995. Mechanisms for carbon and nutrient release and retention in beech f()rest gaps: II. The role of soil microbial biomass. - Plant Soil 168-169: 585592. Bauhus, ]. and Bartsch, N. 1995. Mechanisms for carbon and nutrient release and retention in beech forest gaps. 1. Microclimate, water balance and seepage water chemistry. Plant Soil 168-169: 579--584.

110

Bauhus, ]. et al. 2004. The effects of gaps and liming on forest floor decomposition and soil C and N dynamics in a Fagus sylvatica forest. - Can. ]. For. Res. 34: 509-518. Beie;, C. et al. 2001. Fluxes ofNO,-, NH/, NO, NO j, and NjO in an old Danish beech forest. - Water Air Soil PoIlut. 1: 187~195.

Berg, B. and Staaf, H. 1981. Leaching, accumulation and release of nitrogen in decomposing forest litter. - Ecol. Bull. 33: 163--178. Berg, B. and Ekbohm, G. 1983. Nitrogen immobilization in decomposing needle litter at variable carbon:nitrogen ratios. Ecology 64: 63-67. Bosch, ]. M. and Hewlett, ]. D. 1982. A review of catchment experiments to determine the effect of vegetation changes on water yield and evapo-transpiration. - ]. Hydro!. 55: 323. Brockway, D. G. and Outcalt, K. W 1998. Gap-phase regeneration in longleaf pine wiregrass ecosystems. - For. Eco1. Manage. 106: 125-139. Callesen, I. et al. 1999. Nitrate concentrations in soil water below Danish forests. For. Ecol. Manage. 114: 71-82. Cassman, K. G. and Munns, D. N. 1980. Nitrogen mineralization as affected by soil moisture, temperature, and depth. -Soil Sci. Soc. Am. J. 44: 1233-1237. Cheng, X. M. and Bledsoe, C. S. 2004. Competition for inorganic and organic N by blue oak ( Qercus douglasit) seedlings, annual grass, and soil microorganisms in a pot study. - Soil Bioi. Biochem. 36: 135-144. Christ, M.]. et al. 1997. Microclimate control of microbial C. N, and P pools in Spodosol Oa horizons. Can.]. For. Res. 27: 1914-1921. Dalsgaard, L. 2007. Above and below ground gaps - the effects of a small canopy opening on throughfall, soil moisture and tree transpiration in Suserup Skov, Denmark. - Eco1. Bull. 52: 81-102. Geiger, R., Aran, R. H. and Todhunter, P 1995. The climate near the ground, 5th cd. - Friedrich Vieweg und Sohn, Germany. Gessel, S. P, Cole, D. Wand Steinbrenner, E. C. 1973. Nitrogen balances in forest ecosystems of the Pacific Northwest. - Soil BioI. Biochem. 5: 19-34. Gundersen, P 1998. Effects of enhanced nitrogen deposition in a spruce forest at Klosterhede, Denmark, examined by moderate NH,.N0 3 addition. - For. Eco!. Manage. 101: 251-268. Gundersen, P et aL 1998. Impact of nitrogen deposition on nitrogen cycling in forests: a synthesis of NITREX data. - For. Ecoi. Manage. 101: 37-55. Hackl, E., Bachmann, G. and Zechmeister-Boltenstern, S. 2004. Microbial nitrogen turnover in soils under different types of natural forest. - For. Eco1. Manage. 188: 108-112. Heilmann-Clausen, J. et aL 2007. The history and present conditions of Suserup Skov - a nemoral, deciduous forest reserve in a Cl1ltl1rallandscape. - Ecol. Bull. 52: 7-17. Hobra, S. et al. 2001. Mechanism of nitrate loss from a forested catchment following a small-scale, natural disturbance. ~ Can.]. For. Res. 31: 1326--1335. Hornbeck, J. W, Martin, C. Wand Eagar, C. 1997. Summary ofwater yield experiments at Hubbard Brook Experimental Forest, New Hampshire. - Can. ]. For. Res. 27: 20432053. Hi..ird, R. F. and Schaaf, W 1995. Nutrient supply of f()rest soils in relation to management and site histolY. - Plant Soil 168169: 31-41.

ECOLOGICAL BUllETINS 52, 2007

Krause, H. H. 1982. Nitrate formation and movement before and after clear-cutting of a monitored watershed in central New Brunswick, Canada. - Can. J. For. Res. 12: 922-930. Miller, H. G. 1990. Management of water and nutrient relations in European forests. - For. Ecol. Manage. 30: 425-436. Mladenoff, D. J. 1987. Dynamics of nittogen mineralization and nitrification in hemlock and hardwood treefall gaps. - Ecology68: 1171-1180. Mooney, H. A. and Godran, M. (eds) 1983. Disturbances and ecosystems. - Ecol. Stud. 44, Springer. Prescott, C. E. 1997. Effects of dearcutting and alternative silvicultural systems on rates of decomposition and nitrogen mineralization in a coastal montane coniferous forest. - For. Ecol. Manage. 95: 253-260. Ritter, E. 2005. Litter decomposition and nitrogen mineralization in newly formed gaps in a Danish beech (FaguJ' sylvatica L.) forest. - Soil BioI. Bioehem. 37: 1237-1247. Ritter, E. and Bj0rnlund, 1. 2005. Nitrogen availability and nematode populations in soil and litter after gap formation in a semi-natural beech-dominated forest. - Appl. Soil Eeol. 28: 175-189. Riner, E. and Vesterdal, 1. 2006. Gap formation in Danish beech (Fagus sylvatica) fNests of low management intensity: soil moisture and nitrate in soil solution. - Eur. J. For. Res. 125: 139-150. Ritter, E., Starr, M. and Vesterdal, L. 2005a. Losses of nitrate from gaps of different sizes in a managed beech (Fagus sylvatica) forest. - Can. J. For. Res. 35: 308-319.

ECOLOGICAL BULLETINS 52, 2007

Ritter, E., Dalsgaard, L. and Einhorn, K. S. 2005b. Light, temperature and soil moisture regimes following gap formation in a semi-natural beech-dominated forest in Denmark. - For. Ecol. Manage. 206: 15-33. Smethurst, P. J. and Nambiar, E. K. S. 1990. Distribution of carbon and nutrients and fluxes of mineral nitrogen after clearfelling a Pinus radiata plantation. Can. J. For. Res. 20: 1490-1497. Starr, M. 1999. WATBAL: a model for estimating monthlywater balance components, including soil water fluxes. - In: Kleemola, S. and Forsius, M. (eds), 8th Annual Report 1999, UN ECE ICP Integrated Monitoring. Finnish Environment Inst., Helsinki, Finland, pp. 31-35. Valverde, T. and Silvertown, J. 1997. Canopy closure rate and forest structure. - f.',cology 78: 1555-1562. von Wilpert, K., Kohler, K. and Zirlewagen, D. 1996. Die Differenzierung des Stofihaushalts von Waldokosystemen durch die waldbauliche Behandlung auf einem Gneisstandort des Mittleren Sehwarzwaldes. - Mitt. Forstlichen Versuchs- und Forschungsanstalt Baden-Wiirttemberg, Heft 197. Wilczynski, C. J. and Pickett, S. T. A. 1993. Fine root biomass within experimental canopy gaps: evidence for a below ground gap. - J. Veg. Sci. 4: 571-574. Wright, E. F., Coates, K. D. and Bartemucci, P. 1998. Regeneration from seed of six tree species in the interior cedar-hemlock forests of British Columbia as affected by substrate and canopy gap position. - Can. J. For. Res. 28: 1352-1364.

111

112

ECOLOGICAL BULLETINS

2007

Ecological Bulletins 52: 113-121,2007

The carbon pools in a Danish semi-natural forest Lars Vesterdal and Morten Christensen

Vesterdal, L and Christensen, M. 2007. The carbon pools in a Danish semi-natural forest. Ecol. Bull. 52: 113--121.

There is currently little knowledge of the potential for carbon (C) storage in temperate beech forests. Beech forest reserves subject to little or no human intervention may serve as benchmark forests to determine this potential. We estimated the C stock and the distribution of the C stock between tree bioma.<;s, dead wood, forest floor and mineral soil in a part ofSuserup Skov where all phases of the natural forest cycle were represented. The total C stock of the forest was 382 Mg ha- l . The largest proportion of C (225 Mg ha- 1) was in woody biomass > 3 em. Dead wood, which is a unique pool of C in such a forest reserve, contributed 21 Mg ha~l or 6% to the total estock, wherea.<; rorest floor C stock'> including smaller woody debris contributed only 4.5 Mg ha~l or approximately 1% to the total C stock. The forest floor C content was relatively insignificam in this forest as rates of decomposition are high, but the mineral soil contained the secondlargest amount ofC to 1 m depth (132 Mg ha- 1). The total C stock ofSuserup Skov is considerably higher than in mature managed beech forests. This suggests that there is a potential for increasing C stock'> in conventionally managed beech-dominated forests of the region, possibly by adoption ofnatural forest structures and focused management of dead wood in the managed beech forests.

L. vesterdal ([email protected]), Forest and Landscape Denmark, Univ. ofCopenhagen, HfJrsholm Kongevej 11, DK-2970 H@rsholm, Denmark. ~ M Christensen, Forest and Landscape Denmark, Univ. ofCopenhagen, Rolighedsvej 23, DK-1958 Frederiksberg Den-

c:

mark.

Forests store carbon (C) in vegetation, dead wood, forest floors and mineral soils. The Kyoto Protocol has in particular raised the question to which extent we are able to increase the C stock of forests by changing the management. The most recent estimate of the C stock in woody biomass of Danish forests was 57 Mg C ha- I (Larsen and Johannsen 2002). As the main parts of Danish forests are regenerated by clear-cutting, this figure is an average covering clear-cut areas, young stands and mature stands. In managed forests, signifIcant C pools are also found in soils including the forest floor that blankets the mineral soil, but dead wood amounts are very limited (Green and Peterken 1997) and thus contribute little to the total C stock.

Copyright © ECOLOGICAL BULLETINS, 2007

During the last decades, forestry in several European countries has initiated a change in management ofdeciduous forests toward nature-based or continuous cover forestry (Pommerening and Murphy 2(04). This management form is inspired by natural forests where disturbance occurs down to the single tree level, i.e. there is almost continuous crown cover over time. There is currently little knowledge of the influence of this change in management on C stocks. Possibly, more C could be stored as a result of this change in management, as the traditional clearcutting system is known to have low C stocks in the regeneration period with no canopy cover (Liski et al. 2001). An important characteristic in nature-based forestry is the more con-

113

tinuous canopy cover or at least the smaller and less longlasting openings in the forest canopy~ This means that in the long-term there is a higher average biomass C stock per ha in such forests compared to traditional dear-cutting/ replanting systems. Nature-based forest management possibly also preserves more C in soils compared to the dearcutting system, where the soil C stock may decrease in the period following dear-cUtting and replanting (Covington 1981, Heinsdorf 2002, Peltoniemi et al. 2004). Soils may also be prone to fewer disturbances, thereby conserving larger C stocks than in traditionally managed forests. Compared to traditionally managed forests, reserves in natural forest are not exploited with respect to wood. A greater amount of biomass C is therefore left on site, which also sustains a larger pool of C in dead wood (Green and Peterken 1997, Fridman and Walheim 2000, Hahn and Christensen 2004). In Pacific Northwest, Harmon et al. (1990) reported that conversion of old-growth forests to plantations would result in a significant release of C to the atmosphere due to lower C stocks in plantation forests. Fleming and Freedman (1998) similarly found that a landscape managed as a shifting mosaic of plantations on a 60yr rotation would store only ca 22% as much aboveground C as a landscape covered in old-growth natural forests with gap-phase disturbance dynamics. They attributed this to lower biomass levels and to the paucity of snags and coarse woody debris in the managed forests. In a meta analysis of effects of land-use change on soil C, Guo and Gifford (2002) found indications that the soil C stock may be reduced by 13% following conversion from native forests to plantation forestry. In managed forests with a mixture of even-aged stands of different age classes, average total C stocks are usually lower, as the biomass C stock is obviously at a low level in recently dearcut or reforested areas. For forests in the German state Rheinland-Pfalz, Schone and Schulte (1999) reponed ecosystem C stocks for different major tree species from 197 to 236 Mg ha- 1 with the largest part of the C stock in soils (ca 60%). In order to address the possible effect on C storage of conversion to nature-based management, it is relevant to know the potential for C storage in different European forest ecosystems when there is no or little human intervention. Hooker and Compton (2003) recently stressed the need for such benchmark old-growth forests to determine potential biomass recovery after abandonment. The few small remaining areas ofsemi-natural or unmanaged natural forest types may serve as such benchmark forests with respect to various ecosystem properties. The C stock of a forest in structural steady state, i.e. a forest comprising areas of all phases in the forest cycle (Watt 1947) could serve as a benchmark of potential C stocks when there is no management involved. The objective of this study was to provide such a reference for C stocks in beech-dominated Danish forests and to assess the partitioning of C in different components of the forest ecosystem. Suserup Skov represents the cool-

114

temperate nemoral beech-dominated forest type. As such it may provide valuable information on potential C stocks in beech-dominated forests of the region. Carbon pools in living woody biomass, dead wood, and soils were estimated in a part of Suserup Skov, which was previously reported to be within the structural steady state characteristic of natural forests (Emborg et al. 2000).

Materials and methods Suserup Skov (19.2 ha), located on central Zealand (55°22 'N, 11 °34'E), is one of the few semi-natural forests left in Denmark. Carbon stocks were estimated for a part ofSuserup Skov (10.7 ha) reported to have the longest histolY as non-intervention forest and thus also with the structural features of a natural forest (Emborg et al. 2000). It is a mixed deciduous foreSt with a stand basal area of 40 m 2 ha- 1 . European beech Fagus sylvatica and common ash Fraxinus excelsior dominate (56.1 and 28.1 % of basal area, respectively), bUt also several pedunculate oak Quercus robur and wych elm Ulmus glabra are present. The soil is nutrient-rich and developed from glacial deposits. The C horizon is calcareous and contains ca 20% clay. Smaller patches of sandy till occur within the dominating loamy till material (Vejre and Emborg 1996). The soil was classified as an Inceptic Hapludalf according to Anon. (1992). For more information about the forest in general and the studied part, see Emborg et al. (1996) and HeilmannClausen et al. (2007). The climate is cool-temperate with a mean annual temperature of 8.1 °C and a mean annual precipitation of ca 650 mm, the majority ofwhich falls in late summer and autumn.

Volume and C content of woody biomass The volume of living trees was measured May-August 2002. All trees> 30 cm DBH (diameter at breast height, 1.3 m) were measured within the 10.7 ha plot. Small trees between 3 and 30 cm DBH were measured in three representative 1-ha sample plots. Tree heights were estimated using species-specific diameter-height regressions from Suserup Skov (Emborg et al' 1996). Volume of merchantable biomass was calculated by diameter class based on basal area, height and a form factor derived from the Danish standard volume functions for beech (Madsen 1987; for details see Emborg et al. 1996). For broadleaved trees, merchantable wood includes the stem and branches. Carbon contents of total (above- and belowground) woody biomass was calculated by the methods used in Danish National Inventory Repons under United Nations Framework Convention on Climate Change (Illerup et al. 20(5). These methods include tree species specific basic wood densities (in average 0.56 t dw m~3 fresh volume for

ECOLOGICAL BULLETINS 52, 2007

broadleaved trees), an expansion factors to estimate total below- and aboveground biomass from merchantable biomass (1.2), and wood C concentration (0.5 g C gl dw). As no national data are available for broadleaved tree species to support development of expansion factors, the applied expansion factor is based on studies on biomass distribution in Sweden, and Belgium (Nihlgard and Lindgren 1977, Vande Walle et al. 2001). It is assumed that the distribution of tree biomass in these countries is comparable to biomass distribution in Denmark.

Volume and C content of dead wood The volume of dead wood was measured December 2001 using line-intersect sampling (Warren and Olsen 1964, Kirby et a1. 1998). A total of fifteen 50 m transects were laid out from random starting points and in random directions. Thc number of fallen dead wood pieces (> 5 cm diameter) intcrsecting the line was counted. Diameter was measured in cm where dead wood pieces intersected the line, and the species was identified. Dead wood intersections were assigned to diameter classes and the mean crosssectional area for that class was calculated. Thc total volume of fallen dead wood (m3 ha-- 1) in each diameter class then equals the length for that class multiplied with the cross-sectional area, i.e.

where V is the total volume of fallen dead wood of diameter class d (the diameter being measured at the intersect

with the transect line), n is the number of intersections for dead wood pieces of diameter d, and t is total length of transects in metres (Kirby et al. 1998). The conversion factor of 104 is needed to change the results to volume (m3) per hectare rather than per m 2 . For the forest area as a whole the volume per hectare is the sum ofthe volumes for each diameter class. The volume of standing dead wood (snags) was estimated from an area of 10 m width along the same transects. Snag volume was calculated from information on height and diameter. The decay class of dead wood was determined using a key for a six-class scale Clahle 1). Each piece of dead wood was assigned to a decay class by testing hardness combined with a visual estimation of outline and bark. Sampling ofdead wood for C analysis was done in September 2000. Wood samples were taken from the surface towards the centre of the logs using drilling equipment. For all downed logs six samples were taken from different angles, except for the down facing part. From snags higher than 2 m, six samples were drilled from six different directions and in different heights ranging from 0.5 to 1.5 m above the ground. All samples were ground and samples from each log and snag were pooled into a composite sample. Carbon concentration was determined by the Dumas method (Matejovic 1993) using a Leco CNS-2000 analyzer. Wood composite samples (l00-200 mg) were oxidized to CO 2 at 1350°C. The amount of CO 2 was measured using an infrared detection method. For estimation ofbasic wood density ofdead wood, one piece of representative wood (ca 3 x 3 x 3 em) was taken from each log and snag. The collection was done during rather moist winter conditions (February 2002), which in-

Table 1. Characteristics of the six decay classes used for dead wood. Twigs and branches

Softness

Surface

Shape

Intact or missing only in small patches, > 50%

Present

Hard or knife penetrates 1-2 mm

Covered by bark, outline intact

Circle

2

Missing or < 50%

Only branches >3 cm present

Hard or kn ife penetrates
Smooth, outline intact

Circle

3

Missing

Missing

Begin to be soft, knife penetrates 1-5 cm

Smooth or crevices present, outline intact

Circle

4

Missing

Missing

Soft, kn ife penetrates

> 5 cm

Large crevices, small pieces missing, outline intact

Circle or elliptic

Decay Bark class ---~~_

... _-

5

Missing

Missing

Soft, knife penetrates > 5 cm

Large pieces missing, outline partly deformed

Flat elliptic

6

Missing

Missing

Soft, partly reduced to mould, only core of wood

Outline hard to define

Flat elliptic covered by soil

ECOLOGiCAL BULLETINS 52, 2007

115

dicates that wood moisture was close to the maximum "natural" level at sampling. Volumes were measured on wet samples (after at least 2 h in water) in water and dry weights were measured after drying at 105°C for at least 24 h until the weight was stable. Carbon content of dead wood was finally calculated by multiplying volume, density and C concentration for each diameter class. The reported C content of dead wood for the forest is the sum of C contents of each diameter class.

Forest floor C content Forest floors were defined as the organic layer consisting of shed leaves, twigs and branches above the mineral soil, i.e. equivalent to 0 horizons. Forest floors were mull-like and mainly consisted of recently shed leaves and twigs, i.e. there was no distinct humus layer. Forest floors were sampled on an area basis by using a 25 X 25 em wooden frame. Sampling was done carefully in order to avoid contamination with mineral material as far as possible. Six subsampIes were randomly collected in March 2000 around the soil pit (see below). Subsamples were dried at 60°C, and the material was weighed (± 1 g). The six subsamples were ground and pooled to one sample for C analysis by dry combustion (Dumas method) in a Leco CNS-2000 as described for dead wood. Forest floor C stocks were estimated by multiplying C concentrations by dry mass per ha.

Mineral soil C content

density determination were sieved (2 mm) and dried to constant weight at 105°C. Data on three other soil pits within the studied area of Suserup Skov were reported by Vejre and Emborg (1996). Information on bulk density was not available in this study, and bulk densities by genetic horizon were thus estimated using a pedotransfer function based on similar Danish soil types (Alfisols) (Callesen et aI. 2003, Vejre et a1. 2003). Of the four soil profiles, two represented the undulating northern part of the forest and the other two represented the more level area close to the lake (see map in Heilmann-Clausen et al. 2007). For all four soil profiles, mineral soil C content for the fraction ~ 2mm were neglected (McNabb et aI. 1986), and soil organic C (SOC) stocks in [Mg ha- 1] were estimated by genetic horizon i via

where Pi is the bulk density of the < 2 mm fraction in g cm 3 , 8i ,2mm is the relative volume of the fraction ~ 2 mm (%), d i denotes the thickness of layer i in em, and C j denotes the C concentration oflayer i. Carbon stocks of horizons were then summed to a depth of 1 m. Information on stone contents were not available and mineral soil C stocks may therefore be slightly overestimated in some of the four soil profiles.

Results

Data from four soil pits were included in the study. One soil pit was dug in March 2000 at a plateau in the northeastern part of the forest area. The soil pit was described and subsequently soil was sampled by genetic horizon for C analysis and bulk density determination (2 samples). Soil samples for C analysis were air dried and sieved (2 mm). Samples were then ground in an agate mortar and analyzed for total C by dry combustion as for dead wood and forest floors. The two samples per horizon for bulk

Biomass C content The merchantable woody biomass amounted 670 m 3 ha- 1, and by use of the various to conversion factors the C stock of both above- and belowground woody biomass was estimated at 225 Mg C ha-[ C!able 2). Beech contributed most to the biomass C stock followed by ash and oak as a direct consequence of the species distribution of mer-

Table 2. The distribution of biomass C among the most dominant tree species. Merchantable wood is stem and branch wood whereas biomass C includes both above-and belowground C. Merchantable wood (m 3 ha- 1)

C stock (Mg ha- 1 )

144 35 34

Other species

429 105 99 22 10 5

2

64 16 15 3 1 1

Total

670

225

100

Fagus sylvatica Fraxinus excelsior Quercus rabur Ulmus glabra Tilia platyphy/los

116

7 3

Relative C distribution (%)

ECOLOGICAL BULLETINS 52, 2007

Table 3. Measured variables and calculated C stocks for dead wood decay classes. Decay class

Volume (m 3 ha~l)

1 2 3

33.5 (20) 16.7 (10) 37.6 (22)

4 5 6

58.9 (35) 19.2 (12) 2.2 (1)

Total

Basic density (g cm-3 )

C concentration (mgg""l)

C stock (Mg ha- 1 )

0.42 0.32 0.23

474 471 467

6.7 (32) 2.5 (12) 4.0 (20)

0.21 0.17 0.10

466 473 470

5.8 (28) 1.5 (7) 0.1 «1) 20.5

168.0

Note: numbers in brackets are percentage of total.

chantable wood. The total amount of C in woody biomass is equivalent to 825 Mg CO 2 ha~l.

found for each 10 em layer below 50 em where C concentrations were 3.8 mg g-I on average.

Dead wood C content

Total C stock

The total volume of dead wood was 168 m 3 ha- 1 resulting in a total C stock of dead wood of 21 Mg ha- I (Table 3). Dead wood C amounted to 9.3% of the C stock estimated for total woody biomass. The main part of the dead wood volume was beech (74%) followed by oak (21 %). Decay class 4 contributed most to the total volume of dead wood (35%), whereas decay class 1 contributed most to the total C stock ofdead wood (32%) Cfable 3). The younger decay classes contributed relatively more to total C stock than to total volume as density of dead wood decreased with increasing age and decay class. Carbon concentration was constant across decay classes.

The sum of C pools in woody biomass, dead wood, forest floor and mineral soil amounts to 382 Mg ha- I (Table 4). Woody biomass accounts for the main part of the stored C in Suserup. More than half of the total C is stored in woody biomass. Mineral soil is the second-most important ecosystem compartment with about one third of total C. Dead wood accounts for just 6% of total C and forest floors are quite insignificant for C stock assessment in this specific natural forest ecosystem.

Discussion The C pools of Suserup Skov

Forest floor and mineral soil C content Soil C is found in both forest floor and the mineral soil. In Suserup Skov the forest floor is thin and mainly consists of litter from the last litterfall event. Decomposition is fast and only 4.5 Mg C ha- 1 is stored in this part of the soil profile (Fig. 1). In this forest ecosystem, the mineral soil is by far the most important soil compartment for C storage with an average C content of 132 Mg ha-~I . Mean values for mineral soil C content based on the four soil pits are given in Fig. 2. The C content decreases relatively gradually which is common for nutrient-rich till soils in Denmark (Fig. 2a). Most C is located within the top 30 em of the mineral soil, which in most cases corresponds to the A-horizon. The C concentration in 0-30 em ranged from 16 to 23 mg g-I resulting in soil C contents of ca 70 Mg C ha- I or 53% of the C stock to 1 m (Fig. 2b). About 100 Mg C ha- I (75% of total C content) is found within the upper 50 em of the mineral soil. Only low C contents of 6 Mg C ha- I were

ECOLOGICAL BULLETINS 52. 2007

The results provide an estimate of the C stock and its distribution in the nemoral beech-dominated natural forest type of eastern Denmark. The C stock reported is representative only of Suserup Skov, but nevertheless the results give an impression of the potential C stock for a semi-natural beech-dominated forest subject to structural steady state conditions (Emborg et al. 2000). Biomass C stocks (225 Mg ha- I) were relatively high in Suserup Skov. For Germany, biomass C stocks in managed 200-yr-old beech forests were reported to be around 150 Mg C ha- 1 (Dieter and Elsasser 2002). In a study of British semi-natural woodlands, Patenaude et al. (2003) found that two non-intervention stands dominated by ash and field maple (70-80 yr) contained only 133 and 115 Mg C ha- I, respectively. The volume of living merchantable wood in Suserup (670 m 3 ha~l) is also high compared to most non-intervention hxest reserves in northern Europe. A study of 18 reserves in north European lowland and central European submontane areas with beech dominated

117

Fig. t. One ofthe fouf soil profiles excavated at Suscrup. Note th~ dark A horizon indicating a high C concentration and me shallow forest floof. d~p.

Carbon content, Mg ha-1 20 0 10 30

a)

E () Ol

0

Carbon content, Mg ha-1 0 40 80 120 160

b) 40

0

0

20

20

40

.s::. .....

a.

forest shows an average volume of 53B m' ha- ' (Christensen et aI. 2005). A study of 9 forest reserves in the southern Baltic region reported an average volume of 479 m' ha- ' (Hahn and Christensen 2004). The highest wood volumes in Europe are fOund in montane mixed beech forest in eastern and central Europe (Hahn and Christensen 2004, Christensen et aI. 2005). Forest biomass varies tremendously within Europe depending on tree species, soil type) climatic conditions and managemem. In Suserup Skov there is no active management and the high merchantable biomass stocks, and in turn biomass C stocks, can be attributed to the very favourable growth conditions. Beech and ash in Suserup Skov attain large heights and volumes for Danish conditions. The soil at Suserup is very rich in nutrients, and water supply on the south-ficing slope is also very fivourable to tree growth. The high biomass C stock in Suserup compared to C stocks in some British semi-natural forests (Patenaude et aI. 2003) can also be attributed [0 the long period of non-intervention which has enabled uccs to grow to their maximum si7..e. In Suserup Skov, trees are also present for a longer time alter they attain their maximum size compared to managed forests, where harvesting shortcuts the natural fOrest cycle. Managed beech forests in Denmark contain much less C in the biomass than the beech-dominated forest at Suserup. The most recent forestry census estimated that beech srands on average contained 77 Mg C ha- I (Larsen and Johannsen 2002). This is for the main part due to the shifting mosaic of stands in managed forests where large areas can have quite low biomass volumes, e.g. old srands undergoing natural regeneration or young srands with low biomass levels. Compared to managed beech forests, natural fOrests with small-scale gap disturbance dynamics seems to

E ()

40

.s::. .....

60

a. Ol

0

60

80

80

100

100

Fig. 2. (a) Carbon content in mineral soil and (b) cumulative amounts of C by each lOan laye.r down to 100 em. Error bars are standard. errors of me mean.

liB

ECOLOGICAL BUlLETlf-lS ~2. 2007

Table 4. The distribution of C among the studied ecosystem compartments.

C stock (Mg ha- 1 ) Above- and belowground biomass (d>3 cm) Dead wood (d>5cm) Forest floor Mineral soil to 1 m

225 21 4.5 132

Total

382

be able to store more biomass and thus C on average over time as also reported by Harmon et al. (1990) and Fleming and Freedman (1998). Our results are in line with a British study of five semi-natural stands in a forest reserve, which suggested that managed broadleaved forests with little understorey present store less C (Patenaude et al. 2003). However, it is necessary to temper conclusions regarding effects of management by the fact that Suserup Skov only serves as a case study on C storage in a natural forest. Productivity is high in Suserup Skov as judged from tree height, and regeneration potential is very high. The biomass C stock of this forest would therefore also be higher than the average for Danish forests if it had the same ageclass distribution as Danish beech forests. Thus, we refrain from extrapolating the C stocks ofSuserup Skov to Danish beech forests in general. Apart from the high biomass C stock, the main difference in C pools between Suserup Skov and managed Danish forests is the presence of dead wood with a diameter above 5 em. This pool of C is virtually absent from Danish forests where very little dead wood has been left following thinning and harvesting operations. There is little information on dead wood in Danish forests, but in Belgium, Vande Walle et al. (2001) found only 0.3 and 0.8 Mg C hal in dead wood> 5 cm diameter in a managed oakbeech and a managed ash stand, respectively. In the UK, Green and Peterken (1997) reported that dead wood volumes in managed forests were no more than 30% of the dead wood volumes in unmanaged forests and usually very much lower. It is therefore of special interest to quantifY the contribution of this organic matter pool to the C stock of natural forests. The volume of dead wood in Suserup is comparable to the amounts found in other non-intervention reserves in European beech-dominated forest (Hahn and Christensen 2004, Christensen et al. 2005). Christensen et al. (2005) analysed data from 86 forest reserves and found a mean volume of 130 m 3 ha- 1• The C stock of the dead wood component at Suserup was quite similar to the amount reported (28 Mg ha- 1) from an unmanaged beech forest in Hungary (6dor and Standovar 2003), but much higher than the amount (2 Mg C ha- l) reported from 70-80-yr-old semi-natural British woodlands (Patenaude et al. 2003). According to provisional benchmarks for dead wood in British forests (Kirby et al. 1998), Suse-

ECOl.OCICAL BULLETINS 52. 2007

Relative distribution (%)

59 6 1 34 100

rup Skov has a high level ofdead wood (>40 01 3 ha-- 1). Such high levels of dead wood are characterized as uncommon and found in forests likely to be long (>70 yr) unmanaged and/or to have been affected by major disturbance. These properties of British forests with high levels of dead wood are well in line with the management history of Suserup Skov (Heilmann-Clausen et al. 2007). The forest floor C stock (4.5 Mg ha- 1) was relatively small at this site which can be attributed to the mull-like humus form developed on this nutrient-rich mineral soil. Decomposition is rapid (Ritter and Bj0rnll.lnd 2005), and forest floor accumulation ofC is correspondingly low. The C stock of the forest floor was comparable to C stocks found in beech stands at similar soil types in Denmark whereas beech stands can accumulate three times as much C in forest floors at poor, sandy soil types (Vesterdal and Raulund-Rasmussen 1998). The mineral soil stored a relatively large amount of C to 1 m depth at Suserup (132 Mg hal). Vejre et al. (2003) reported a mean value for well-drained Danish forest soils of 125 Mg C ha- 1, but the mean value for the dominant soil type at Suserup (Alfisols) was only 88 lv1g C hal. The soils at Suserup Skov are quite representative of Danish Alfisols with respect to particle size distribution and pedological development, so this is not the primary cause for the higher C content. Although the C content in some of the profiles may have been overestimated slightly because of larger stones not accounted for, the C content at Suserup is well above the average for the soil type. The high input of organic matter to soils because oflimited harvesting has been stressed as a factor contributing to maintenance of soil organic C at Suserup (Vejre and Emborg 1996).

The total C stock and relative contributions of various C pools The total C stock estimated for this part of Suserup Skov amounted to 382 Mg ha- 1, which is a fairly high amount compared to 80-yr-old deciduous stands in Belgium (ca 325 Mg ha-\ Vande Walle et aL 2001). In Suserup Skov, biomass contributed the most to the C stock, followed by mineral soil, dead wood and forest floor. Although the C

119

stock of dead wood wa.<; relatively small it made up 6% of the total C stock and was more important in this forest ecosystem than forest floor C. This is in line with results from natural North American coniferous forests, where the dead wood pool accounted for between 2 and 17% of the total C stock (Kueppers et al. 2004). Comparable contributions of the dead wood component were reported for natural Nothoftgus forests in both New Zealand (70/0, Hart et al. 2004) and in Argentine (11 %, Weber 1999). The relative contribution of dead wood and soil pools obviously depends on soil type, forest type, age and developmental stage of the forest stand. The relative contribution ofsoils to the total C pool was much larger in a British semi-natural deciduous forest (ca 70%) due to much higher mineral soil C stock<; (335 Mg ha- 1 to 50 cm depth) and lower dead wood and biomass C pools in these 70-80-yrold forests (Patenaude et al. 2003). For Pacific Northwest coniferous forests, Sun et al. (2004) reported that the relative contribution ofnecromass C pools (mineral soil, forest floor and dead wood C) decreased as a negative exponential function of stand age to a value of around 35% for stands aged 150-200 yr. In Suserup, these necromass pools made up 41 % oftotal C which is fairly consistent with the findings of Sun et aI. (2004). This study has contributed with a rough estimate ofthe C stock and C stock distribution in a natural beech-dominated fOrest in Denmark. The study was not based on a specific inventory of C stocks and needed to rely on standard mensuration methods for quantification of biomass C stocks as destructive sampling is not possible in the forest reserve. The C stock in soils must be regarded with caution, as it is only based on four soil pits, but also the biomass C stock has high uncertainty due to the use of a standard biomass expansion factor for broadleaves used in Danish UNFCCC reporting (Illerup et al. 2005). There are currently no available expansion functions to estimate belowground biomass more accurately under Danish conditions. Regeneration trees with a diameter < 3 cm and ground vegetation were not included, but ground vegetation generally contributes little to the total C stock (Weber 1999, Vande Walle et al. 2001, Patenaude et al. 2003). In spite of these shortcomings, the study has indicated the large potential for C storage in such beech-dominated forest reserves on nutrient-rich till soils. The high C stock in semi-natural forests also suggest that more C could be stored by conversion from the traditional forest management system based on clearcutting and replanting to continuous cover forestry with focus on the maintenance of the dead wood component.

Acknowledgements - We extend our thanks to Katrine Hahn, Jaris Bigler, Ed Mountford, Jacob Heilmann-Clausen, Anne Maren Madsen, Eva Ritter and Finn V J0rgensen for assistance with field work.

120

References Anon. 1992. Keys to soil taxonomy, 5th ed. - SMSS technical monograph no. 19. Pocahontas Press, Blacksburg, VA, USA. Callesen, 1. et al. 2003. Soil carbon stores in Nordic upland forest soils - relationships with climate and site variables. - Global Change BioI. 9: 358--370. Christensen, M. et al. 2005. Dead wood in European beech (Fagus sylvatica) forest reserves. - For. Ecol. Manage. 210: 267282. Covington, W W 1981. Changes in forest floor organic matter and nutrient content following dear cutting in northern hardwoods. - Ecology 62: 41-48. Dieter, M. and Elsasser, P. 2002. Carbon stocks and carbon stock changes in the tree biomass of Germany's forests. - Forstw. Cbl. 121: 195-210. Emborg, ]., Christensen, M. and Heilmann-Clausen, J. 1996. The structure of Suserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Landscape Res. 1: 311333. Emborg, ]., Christensen, M. and Heilmann-Clausen, J. 2000. The structural dynamics of Suserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Ecol. Manage. 126: 173-189. Fleming, T. L. a:qd Freedman, B. 1998. Conversion of natural, mixed-species'forests to conifer plantations: implications for dead organic matter and carbon storage. - Ecoscience 5: 213-221. Fridman, J. and Walheim, M. 2000. Amount, structure, and dynamics of dead wood on managed forestland in Sweden. For. Ecol. Manage. 131: 23-36. Green, P. and Peterken, G. E 1997. Variation in the amount of dead wood in the woodlands ofthe Lower Wye Valley, UK in relation to the intensity of management. - For. Eeo!. Manage. 98: 229-238. Guo, L. B. and Gifford, R. M. 2002. Soil carbon stocks and land use change: a meta analysis. - Global Change BioI. 8: 345360. Hahn, K. and Christensen, M. 2004. Dead wood in European forest reserves - a reference for forest management. - In: Marchetti, M. (ed.), Monitoring and indicators offorest biodiversity in Europe - from ideas to operationality. EFI Proc. 51, pp. 181-191. Harmon, M. E., Ferrell, W K. and Franklin,]. F. 1990. Effects on carbon storage of conversion of old-growth forests to young forests. - Science 247: 699-702. Hart, I~ B. S. et al. 2004. Biomass and macronutrients (aboveand below-ground) in a New Zealand beech (Nothofagus) forest ecosystem: implications for carbon storage and sustainable forest management. - For. Eco!. Manage. 174: 281294. Heilmann-Clausen, J. et al. 2007. The history and present conditions of Suserup Skov a nemoral, deciduous forest reserve in a cultural landscape. Ecol. Bull. 52: 7-17. Heinsdorf, D. 2002. Einfluss der Bewirtschafi:ung auf den KohlenstoHhaushalt von Forstokosystemen on Nordostdeutschen Tiefland. - Beitr. Forstwirtsch. u. Landsch. ako!. 36: 168-174. Hooker, T. D. and Compton, J. E. 2003. Forest ecosystem carbon and nitrogen accumulation during the first century after agricultural abandonment. - Ecol. App!. 13: 299-313.

ECOLOGICAL BULLETINS 52, 2007

Illerup,]. B. et al. 2005. Denmark's National Inventory Report 2005. Submitted under the United Nations Framework Convention on Climate Change 199~2003. - Ministry of Environment, Denmark, National Environmental Research Institute, . Kirby, K. J. et al. 1998. Preliminary estimates of fallen dead wood and standing dead trees in managed and unmanaged forests in Britain. - J. App!. EcoL 35: 148-155. Kueppers, L. M. et al. 2004. Dead wood biomass and turnover time, measured by radiocarbon, along a subalpine elevation gradient. - Oecologia 141: 641-651. Larsen, P. H. and Johannsen, V. K. 2002. Skove og plantager 2000. - Statistics Denmark, Skov and Landskab, Danish Forest and Nature Agency. Liski, J. et al. 2001. Which rotation length is favourable to carbon sequestration? - Can. J. For. Res. 31: 2004-2013. Madsen, S. F. 1987. Vedmassefunktioner ved forskellige afl~gn inggr~nser og n0jagtighedskrav for nogle vigtige danske skovtr~arter. - Det Forstlige Fors0gsv~sen i Danmark 41: 47242, in Danish. Matejovic, 1. 1993. Determination ofcarbon, hydrogen, and nitrogen in soils by automated elemental analysis (dry combustion method). - Comm. Soil Sci. Plant Anal. 24: 2213-2222. McNabb, D. H., Cromack, K. and Fredriksen, R. L. 1986. Variability of nitrogen and carbon in surface soils of six forest types in the Oregon Cascades. Soil Sci. Soc. Am. J. 50: 1037-1041. Nihlgard, B. and Lindgren, L. 1977. Plant biomass, primary production and bioelements of three mature beech forests in south Sweden. - Oikos 28: 95~ 104. 6dor, P. and Standovir, T 2003. Changes ofphysical and chemical properties ofdead wood during decay. - Nat-man WP7 report, . Patenaude, G. L et al. 2003. The carbon pool in a British seminatural woodland. - Forestry 76: 109-119.

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Peltoniemi, M. et al. 2004. Changes in soil carbon with stand age an evaluation of a modelling method with empirical data. Global Change BioI. 10: 2078-2091. Pommerening, A. and Murphy, S. T. 2004. A review of the history, definitions and methods ofcontinuous cover forestry with special attention to afforestation and restocking. - Forestry 77: 27-44. Ritter, E. and Bj0rnlund, L. 2005. Nitrogen availability and nematode populations in soil and litter after gap formation in a semi-natural beech-dominated forest. - Appl. Soil Ecol. 28: 175-189. Schone, D. and Schulte, A. 1999. Forstwirtschaft nach Kyoto: Ansatze zur Quantifizierung und betrieblichen Nutzung von Kohlenstoffsenken. - Forstarchiv 70: 167-176. Sun, O. J. et al. 2004. Dynamics of carbon stocks in soils and detritus across chronosequences of different forest types in the Pacific Northwest, USA. Global Change BioI. 10: 1470-1481. Vande Walle, I. et al. 2001. The abovc- and be1owground carbon pools of two mixed deciduous forest stands located in EastFlanders (Belgium). -Ann. For. Sci. 58: 507-517. Vejrc, H. and Emborg,]. 1996. Interactions between vegetation and soil in a near-natual temperate deciduous forest. - For. Landscape Res. 1: 335-347. Vejre, H. et al. 2003. Carbon and nitrogen in Danish forest soils - contents and distribution determined by soil order. - Soil Sci. Soc. Am.]. 67: 335-343. Vesterdal, L. and Raulund-Rasmussen, K. 1998. Forest floor chemistry under seven tree species along a soil fertility gradient. - Can. J. For. Res. 28: 1636-1647. Warren, W. G. and Olsen, P. F. 1964. A line intersect technique for assessing logging waste. For. Sci. 10: 267-276. Watt, A. S. 1947. Pattern, process and natural disturbance in vegetation. - Bot. Rev. 45: 229-299. Weber, M. 1999. KohlenstoffVordite cines Nothofagus-Primarwaldes auf Feuerland. - Forstw. CbI. 118: 156-166.

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Ecological Bulletins 52: 123-131, 2007

Nematode assemblages and their responses to soil disturbance differ between microsites in Suserup Skov, a semi-natural forest Lisa Bj0rnlund and Jonas D. Lekfeldt

Bjornlund, L. and Lekfeldt, J. D. 2007. Nematode assemblages and their responses to soil disturbance differ between microsites in Suserup Skov, a semi-natural forest. - Ecol. Bull. 52: 123-131.

Effects of a controlled disturbance (sieving and drying of soil) on free-living nematode assemblages in Suserup Skov forest soil were srudied at two microsites with different soil conditions and tree stand age. Results confirmed that nematode assemblages are site specific on a small scale in this forest, most likely as a result ofvariation in soil properties. Responses to the disturbance were similar with regard to distribution ofnematode feeding gtoupS at both sites suggesting that the microflora was uniformly affected at both sites. However, effects on total number of nematodes and on summed maturity index differed between the two microsites in Suserup Skov. The findings of this and three previous studies in Suserup Skov are summarized to present an overview of how soil nematode assemblages reflect environmental conditions in this semi-natural forest.

1. Bj(Jrnlund ([email protected]), Dept ofEcology, Univ. ofCopenhagen, Thorvaldsemvej 40, DK-1870 Frederiksberg C Denmark. - J D. LekJefdt, Dept Terrestrial Ecology, Biological

Inst., Univ. ofCopenhagen, 0ster Farimagsgade 2D, DK-1353 Copenhagen K Denmark.

Why study nematodes in the semi-natural forest Suserup Skov? 1. Nematodes are numerous. Densities of nematodes in forest soil and litter usually reach 10-100 g-l soil or millions per square meter of the forest floor (Nielsen 1949, Yeates 1972, Wright and Coleman 2000, Sohlenius and Bostrom 2001). Therefore only small soil samples are needed to obtain sufficient individuals for analysis and minimum perturbation is imposed on the soil system during sampling. This is attractive when sensitive and unmanaged ecosystems are studied. 2. Nematodes are very diverse. At least 12000 species have been described and a distinct part of the terrestrial species pool may be present in natural forests that offer a more complex and patchy habitat for nematodes than do

Copyright t"J ECOLOGICAl BULLETINS, 2007

the relatively homogeneous and usually species poor arable land (Hanel 2001, Ettema and Yeates 2003). 3. Nematodes occupy several trophic levels within soil food webs and can be assigned according to food preferences into at least five feeding groups: bacterial feeders, fungal feeders, plant feeders, omnivores and predators (Yeates et al. 1993). Microbivorous nematodes may modulate the structure of bacterial (Griffiths et al. 1999, Djigal et al. 2004) and fungal communities (Bakhtiar et al. 2001) and, likewise, plant feeders may affect plant production. Furthermore, bacterial feeding nematodes contribute to nutrient turnover, e.g. nitrogen mineralization (Ingham et al. 1985, Verhoef and Brussard 1990) in a direct manner by excretion and indirectly by grazing on bacteria which, in turn, stimulate bacterial activity (Freckman 1988).

123

4. Nematodes are adapted to different life strategies ranging from the fast growing, opportunistic colonizers (rstrategists) to the slower growing and perturbation sensitive persisters, (K-strategists). Accordingly, Bongers (1990) assigned a cp-value between one and five to each nematode family. Based on this, the maturity index (M!) can be calculated as the weighted means of the cp-values for microbial feeding nematodes (Bongers 1990). This was later modified by "Yeates (1994) who included the herbivorous nematodes in the summed maturity index (LM!). It is theoretically possible to gain important insight into various aspects of soil function through analysis of nematode population dynamics based on feeding and life-strategy guilds (Bongers and Ferris 1999). This approach rests on the assumption that food availability governs nematode densities and "bottom-up" control of both plant parasitic nematodes (De Deyn et al. 2004) and microbivorous nematodes (Rantalainen et al. 2004) is often reported. With all these appealing aspects in mind it is not surprising that nematode analysis are often employed in studies on arable (Garcia-Alvares et al. 2004), heathlands (Schmidt et al. 2000) as well as forest (Wright and Coleman 2000) systems to evaluate effects of various environmental influences on the soil biota. However, interpretation of field data on nematodes or other soil dwelling organisms is rarely an easy task due to the confounding effects of variable environmental factors that need to be taken into account. Disturbance effects are generally specific to ecosystems (Neher et al. 2005). Wright and Coleman (2000) recommended performing more long-term cross-site studies to achieve insight into the complex interrelations of determining factors. Conversely, Ettema and Wardle (2002) argue that the heterogeneity within natural sites should be considered a key to understanding the structure and function of soil biodiversity rather than an obstacle that introduce noise and hamper reliable quantification of soil populations. They recommend the application of geostatistics, especially the use of semivariograms that may reveal how variability between soil samples depends on horizontal distance in the field. In this study, we want to add to the understanding of the influence of soil heterogeneity on soil biota by investigating the link between the susceptibility of the nematode community to an anthropogenic perturbation (sieving and drying) and small scale spatial variation in the seminatural forest Suserup Skov. Furthermore, we study if migration could be an important aspect of resilience of nematode communities. The knowledge gained in this and three previous studies of nematodes in Suserup Skov, conducted 1999-2003, are summarized in an attempt to give an overview of how environmental impacts appear to influence the nematode communities at this site. Finally, we discuss the relevance of using nematode community analysis as a tool for monitoring soil health in natural ecosystems.

124

Materials and methods Experimental design For site description ofSuserup Skov and the study area, see Heilmann-Clausen et al. (2007) and Ritter and Bj0rnlund (2005). Two microsites of 16 m 2 each were chosen. Microsites were positioned east (1) and west (2), respectively, of a large gap formed in 1999 in the central parts of the forest. The microsites were separated by 75 m and differed with respect to soil conditions and the structure of the forest stand. At microsite 1, the texture was loamy sand with a pH of 5.3--6.8. The forest stand consisted of large beech trees with some smaller elm in the understorey and could be assigned to "late biostatic phase" indicating that the forest was in a late succession state ofthe forest cycle (Emborg et al. 2000). At microsite 2, the soil was a sandy loam with a pH range of3.1-4.4. Here, the forest consisted mainly of younger beech trees mixed with a few ash trees and some regeneration of elm. This plot was assigned to an earlier succession state termed "aggradation to early biostatic". The only ground vegetation that was observed was Anemone nemorosa in early spring at both microsites and this was most developed at microsite 2. Within each microsite, 8 plots each sized 1 m 2 were established and each of the fouf treatments described below were assigned randomly to two plots of each microsite.

Treatments and sampling Four treatments were applied to two plots at each of the two microsites in a 2 X 2 factorial design. Treatments were with or without physical perturbation (sieving and drying) of the soil, combined with (plastic tube: 4.5 X 15 cm) or without (litterbag: mesh size 2 mm) a physical barrier to prevent or allow migration of nematodes, respectively. On 13 March 2002,6 soil cores were taken with a plastic tube (4.5 X 15 cm) from each of the 8 plots at both microsites, a total of 96 samples that were treated and analyzed separately throughout the experiment. Nematode extraction by a modified Baerman method was initiated for 16 soil cores, one for each plot, on day O. Extractions were terminated after 48 h. Nematodes were counted and heat-fixed in formaldehyde (80°C, 6%). A 2 cm layer of heat-treated gravel (105°C, 12 h) was filled into each hole made in the forest floor to prevent vertical migration of nematodes. T'he 40 unperturbed soil cores were returned immediately to their original positions within the plots. In the laboratory, the remaining 40 individual samples were separately sieved by hand through a 2 mm sieve and mixed. The sieved soil samples were left: to air dry on filter paper trays at 20°C for 96 h. This had previously reduced the number of nematodes by 98% and the water content to 3% in a pilot experiment (data not shown). On day 5,

ECOLOGICAL BULLfflNS 52, 2007

each sieved and dried sample was returned to the hole in the forest floor from where it had been collected. On four occasions (day 5, 9, 21, 43) 16 samples, one from each plot, were again sampled and the nematode density recorded. Four additional samples, two for each microsite were collected on day 2 L Nematodes from these samples were also extracted and counted to compare the abundances of

40

35

nematodes found in the experiment to that of the forest floor within the microsites. By the end of the experiment, one sample per plot remained as back-up and was not analyzed. On average 32 (day 0 and 5) or 42 (day 43) individuals per sample were identified to family (Bongers 1994), assigned to feeding group (Yeates et al. 1993) and colonizer-persister scale (Bongers 1990, 1999).

10

5

o

C~_~

o

._ •• , ••

~ ~ ~

10

~

~

20

30

~~_--l

40

50

Day

Data analysis Numbers of nematodes were log transformed to obtain equal variances. Densities before and after the perturbation (day 0 and 5) at the two microsites were compared by a two-way ANOVA to examine short term effects of the treatment. A similar procedure was used to compare nematode densities in undisturbed samples to the background density of nematodes on day 21. To evaluate the recovery, nematode densities from the 5 to 43 d period were tested by a GLM procedure (SAS 6.12) including microsite (lor 2), perturbation (with or without), migration potential (samples in plastic tube or litterbag) and sampling day (5, 9, 21 and 43) into the model. Likewise, Maturity index and feeding groups of nematodes on day 0,5 and 43 were tested in a GLM procedure. Finally, the overall composition ofnematode assemblages in the samples were analysed by a principal component analysis (PCA) (CANOCO 4, Center for Biometry Wageningen, Microcomputer Power, Ithaca NY).

Results Nematode density Overall, nematode densities ranged between 4 and 77 g-l soil. The average number of nematodes was consistently 2-4 fold higher at microsite 2 than at microsite 1 throughout the study period (ANOVA site; p = 0.0001) (Fig. 1). Perturbation reduced nematode densities by 25-70% of initial size (Fig. 1) and water content was reduced from 37% to between 6 and 12% (w/dw). Samples enclosed in litterbags and in plastic tubes had similar nematode densities across all samplings from day 5 to 43. Therefore, migration was not important for recovery during 43 d following disturbance and pooled data from samples in tubes and litterbags are presented in Fig. 1. The additional field samples collected on day 21 were not significantly different

ECOLOGICAL BUU.FJlNS 52, 2007

Day

Fig. 1. Number of nematodes recorded in soil two microsites in Suserup Skov. Solid lines represent data from control samples while dotted lines represent data from disturbed samples. Error bars represent ± 1 SE.

from the undisturbed samples coUected on this day. This demonstrates that nematode densities of the control samples had not been affected by the inevitable root damage inflicted upon the samples at the set-up of the experiment. Comparisons of samples from day 0 with samples from day 5 showed that nematode density decreased significantly by 50~75% at microsite 1 (p < 0.05, Tukey) while a nonsignificant decrease of 30-50% was seen at microsite 2 in response to the disturbance (Fig. 1). This indicates that nematode density at microsite 1 was less resistant than at the microsite 2. The effect of the perturbation on nematode numbers from day 5 to 43 was similar at both localities (perturbation; p = 0.0001) as there was no significant interaction between site and perturbation. Hence there was no statistical evidence for a difference in recovery of nematode densities between sites. However, from inspection of Fig. 1 it appears that recovery of nematode density was underway in the disturbed samples from microsite 1, while this seemed not to be the case at the microsite 2. Nematode numbers increased over time but only at microsite 1 (ANOVA: p = 0.0422).

125

Composition of nematode assemblages There was a complete separation of samples from the two microsites in the PCA-diagram (Fig. 2A) in which the first and second axis explained 19.5 % and 12.9 % of the variation, respectively. This suggests a difference in the taxonomic composition of the nematode communities at the two sites. We note that for example Cephalobidae and Wilsonema spp. were more frequent at microsite 2 whereas Alaimidae and Teratocephalidae occurred more frequent at microsite 1 (Table 1). Furthermore, data-points from disturbed and undisturbed samples from both sites were distinct on day 43 (Fig. 2B) suggesting that disturbance affected community composition at both sites.

Nematode feeding groups responded similarly to the disturbance at both sites (Fig. 3). Short term effects were evident on relative decrease of fungal feeders (disturbance, p = 0.017) at both microsites, almost entirely due to a decline in Diphterophoridae (Table 1). The relative abundance of bacterial feeders was higher in perturbed samples at day 43 (perturbation x sampling, p = 0.04) (Fig. 3). Rhabditidae dominated the perturbed samples from microsite 2 (53%) whereas Cephalobidae were the most prevalent bacterial feeders in perturbed samples from microsite 1 (20.7%) at day 43 (Table 1). The initial value of the summed Maturity index (LMI) was higher at microsite 1 (2.36) than at microsite 2 (2.06) (p = 0.003, Tukey) (Fig. 4) indicating that the soil system at microsite 1 was in a more mature state at the beginning of the experiment. I,MI was affected negatively by the perturbation at microsite 1 (site X perturbation, p = 0.0024), and the effect increased over time (site X sampling, p = 0.033).

51)

•

I)

Discussion

o

Site effects on nematodes of Suserup Skov

5D

• B

o

c

Fig. 2. Principal component analysis (PCA) of the nematode community composition. Closed symbols represent samples from microsite 1 while open symbols represent samples from microsite 2. A: data from day 0, 5 and 43. B: data from day 43. Symbols with a "C" correspond to the control samples while symbols with a "D" correspond to the disturbed samples.

126

The two microsites, separated by only 75 m, exhibited clear differences in community composition and density ofnematodes. In line with previous results, Alaimidae were more prevalent in the near neutral soil compared to the acidic soil (Bj0rnlund et al. 2002, Ritter and Bj0rnlund 2005). Hence, we conclude that soil conditions such as pH and texture are important determinants of the taxonomic composition of nematode assemblages at particular microsites in Suserup Skov. This agrees with De Goede and Bongers (1994) who concluded that the influence of soil conditions is stronger than that ofvegetation type on nematode assemblages. Accordingly, aboveground events, such as vegetation cover and fire frequency, had less influence than disturbance of soil on the nematode community (Matlack 2001). An earlier study compared effects of site heterogeneity and litter quality on decomposer organisms in litter (Bj0rnlund and Christensen 2005) and taken together with the present results they suggest the importance ofheterogeneity between microsites for the taxonomic composition of nematodes in both decomposing litter and soil. Furthermore, site effects on the relative abundance of dominant taxa in litter were independent oflitter type (ash or beech) in Suserup Skov, at least during the first four months ofdecomposition. As was expected, however, litter type governed the decomposition rate and density of decomposer organisms (Bj0rnlund and Christensen 2005). Densities of nematodes and other decomposer organisms assessed (bacteria, fungi, protozoa) in ash litter were several fold higher than those in beech litter during the first four months of decomposition. However, proportions of fast-

t::COLOGICAL

l~ULLFT[NS

2007

Table 1. Relative abundance (%It feeding group (SA: bacterivores, FU: fungivores, PL: plant feeders, OM: omnivores, PR: predators) and colonizer-persister score (cp) of nematode families from two microsites (site 1 and 2) in Suserup Skov immediately (short term effect) or 43 d after soil samples were subjected to sieving/drying or not (Dist., Cont.). Short-term effect Site 1 Site 2 Cont. Dist. Dist. Cant. Families

Feeding

cp

Alaimidae Anguinidae Aphalenchoididae Aporcelaimidae Cephalobidae Criconematidae Desmodoridae Diphtherophoridae Diplogasteridae Diplopeltidae Dolichoridae Halaphanolaimidae Hoplolaimidae Hypodontolaimidae Leptolaimidae Leptonchidae Monhysteridae Mononchidae Onchulidae Panagrolaimidae Paratylenchidae Plectidae Prismatolaimidae Qudsianematidae Rhabditidae Teratocephalidae Trichodoridae Tyledoridae Tylenchidae Wilsonema nd

SA PUFU FU PRiOM SA PL SA FU SA SA PL SA PL SA SA FU SA PR OM SA PL SA SA FU SA SA PL PL PL SA

4 2 2 5 2 3 3

4.8

6.5

'11.8

3

13.8 0.5 0.5

4.1 0.8

1 3 3 3 3 3 2 4 2 4 4 3

0.5

1.1

0.6 2.6 4.3 0.5 0.6

1

2 2 4 1 3 4 2 2 2

1.7 0.8

4.7 4.9 0.5 11,9

6.8 0.5 11.7 22.0 0.5 0.5

5.1 0.9 0.8 0.9 0.8 0.9

0.7

6.6

6.2 0.8

20.7

6.6 2.5

1.7 4.2

0.7 2.2 1.5

1.1

9.6 1.5

7.3

1.1

D.8

0.5 6.2 0.5

8.6 23.3 4.8 0.5

Disturbance effects on nematodes of Suserup Considering that nematode assemblages differed considerably between microsites, it was surprising that the respons-

4.9

2.5

21.0 20A 0.8 1.7

Skov

ECOLOCICAL BULLPI'INS 52, 2007

11.9

16.1 3.5

growing bacterial feeding Rhabditidae were similar in ash and beech litter placed at the same microsites, but varied between microsites of different elevation and forest phases within Suserup Skov (Bj0rnlund and Christensen 2005). The opposite was observed in a Danish agricultural fIeld (10027'E, 55°18 /N) litterbag study as nematode taxa responded to the type oflitter (vetch or rye) but not to standing crop (Georgieva et al. 2005). However, spatial heterogenity is not as pronounced in farmlands as in forests and, therefore, less likely to influence nematode assemblages (Ettema and Yeates 2003).

0.8 0.8 0.8

7.2 1.5 0.8

1.1

1.7 2.5 0.8 15.4

2.2 2.9

0.5 0.4 1.5 6.3 1.0 15.2 2.0

0.9 6.0 0.8

Day 43 Site 1 Site 2 Dist. Cont. Dist. Cant.

6.6 3.9

0.6

1.7 4.0

6.3 7.4 14.5

1.1 0.6 5.0 0.6

5.0 3.3

12.9 4.4 0.8 4.8 18.3

53.0 4.2

5.8

1.3

24.8 22.6 7.5

6.8 16.8

1.3

3.2 0.8

9.6

1.5 2.3

0.6 1.1

1.6

4.5

0.8 10.9

1.7 1.2 5.3 1SA 3.0

8.5 2.3 0.8 6.5 37.1 2.3

10.2 9.6 7.3 1.2

es to sieving and drying were quite similar for all feeding groups. If feeding group distribution indeed reflected the availability of food sources for nematodes in soil it would be logical to assume that the perturbation would have a similar impact on the microflora at both sites. Thus, the relative decrease in fungal feeders in response to the perturbation may reflect that fungal mycelium was disrupted and killed by the sieving and drying of soil. This, as well as the death of other soil organism and plant roots, may have been followed by a pulse of nutrient release upon rewetting that induced growth of bacteria which supported the increase in bacterial feeders by day 43. I-Iencc indirect effects of the disturbance linked to changes in food availability were probably similar between microsites. Likewise, Sohlenius and Bostrom (200 1) found that changes in the abundance and proportions of fungal and bacterial feeders followed a regular pattern over time though large and unpredictable fluctuations in species composition occurred

127

4%

1%

T-

O)

36%

+-'

U5

56%

1%

Cf)

4%

..q >.

2%

en

1%

0

C\I 0) +-'

Ci5

50%

55%

Fig. 3. Data for the distribution of the different nematode feeding groups: predators and omnivores (white), plant feeders (light grey), fungivores (dark grey), bacterivores (black). The upper parr of the figure shows the short term effect of the disturbance while the lower parr shows the efFect at day 43.

128

ECOLOGICAL BULLETINS 52, 2007

3 Site 1

Site 2

Site 2

Site 1

2

o Short-term effect

Day 43

Fig. 4. Average IMI from the two microsites directly after the disturbance (short term) and after 43 d. Open bars represent control samples while dosed bars represent disturbed samples. Error bars represent ± 1 SE.

when two annual time series were compared in a Swedish pine forest. Interestingly, results for total number of nematodes and the shift in proportions of taxa indicate differences in the direct effects of the disturbances between sites. Because the decline in nematode numbers was most pronounced at microsite 1 and there was a shift toward the extreme rstrategists Rhabditidae in response to the disturbance, we assume that the nematode assemblages at microsite 1 were more susceptible to the disturbance. This is consistent with the summed Maturity index CLMI) for nematodes being significantly higher at microsite 1 than at microsite 2 on day 0 as well as the observed decline in I,MI at microsite 1 in perturbed samples day 43, partly explained by the relative increase in Rhabditidae. Since microsite 1 was in an area of the forest in «late biostatic phase" whereas microsite 2 was in «aggradation to early biostatic phase", the maturity stams of the nematode assemblages agreed well with that of the forest stands. Previously, two other types of disturbances were studied, forest management and natural gap formation (Bjornlund et al. 2002, Ritter and Bjornlund 2005). Effects of forest management on nematode assemblages were investigated by comparing three pairs of managed and unmanaged forests including Suserup Skov and a nearby managed forest. This revealed that all managed forests exhibited a

ECOLOGICAL BULLETINS 52.2007

lower prevalence of bacterial feeding nematodes than did unmanaged forests. Furthermore, the maturity index was significantly higher in the two unmanaged forest that had been left untouched the longest time (> 100 yr) than in the adjacent managed forests. A high input of dead wood to the soil is characteristic. of unmanaged forests and dead wood harbour many rare species of fungi (HeilmannClausen and Christensen 2004) and insects (Schiegg 2000). Generally, the inside of decaying logs in Suserup Skov remains moist even in midsummer. Perhaps partly decayed dead wood incorporated into the soil provided a stable habitat for the development ofnematode communities. However, such explanations remain purely hypothetical at this stage. As opposed to the anthropogenic influence of management or sieving!drying, a naturally occurring disturbance event in unmanaged forest would be formation of a gap in the canopy, e.g. due to wind throw or breakdown of old trees. During the severe 1999 winter storm such a gap was formed in Suserup Skov. Nematode numbers decreased in density within the gap for two years and recovered in the third year after the gap was formed (Ritter and Bjornlund 2005). Spatially, this recovery mirrored the upcoming regeneration of young ash trees along the north-south transect of the gap, which may suggest that root exudates from living plants in part controlled nematode biomass,

129

perhaps providing microbial food resources. Neher et al. (2005) found higher diversity and proportions of plant parasites in a young forest in North America harvested within the three previous years than in a 75 yr old mature forest although total abundances were similar overall when composite samples were compared. The nematode numbers in littcr responded to the formation of gaps in an opposite manner to nematode numbers in soil since an increase in litter nematode numbers occurred within the gap (Ritter and Bj0rnlund 2005). Presumably, this was linked to improved microclimatic conditions. The water content of the soil remained close to field capacity throughout the year in the gap whereas moisture content dropped to ca 60% under closed canopy during the growth seasons (Ritter et al. 2005:1.

Putting the pieces of the puzzle together The general trends in how the nematode community reflected variation in environmental impacts in this and the three previous studies are: 1) taxonomic constellation of nematodes were governed by soil parameters such as pH and texture. 2) Nematode density appeared to be controlled by carbon turnover - as indicated by responses of nematode numbers to resource quality in the litter layer and to formation of a forest gap followed by seedling regeneration. Decrease and increase in nematode density reflected similar changes expected in root exudation. 3) Functional groups of nematodes in soil (life strategy and feeding groups) were affected by forest management and soil drying/sieving. Functional groups related more to site soil heterogeneity than to litter type. 4) All aspects studied i.e. density, taxonomic composition, feeding pattern and life strategy, were affected by sieving and drying of soil. However, with the exception of feeding pattern the impact of the disturbance depended on conditions at the microsite, i.e. on the heterogeneity encountered within Suserup Skov. These conclusions confirm that nematode communities do reflect many important aspects of soil structure and function. It would in our opinion be relevant to include nematode analysis in a soil health indicator scheme for survey of selected sites of particular ecological interest over time. However, since heterogeneity has a vast but not random influence on nematode communities we would recommend surveys to be focused within microsites of a few square meters as between site comparisons are likely to be seriously confounded by a large number ofsite specific factors. Acknowledgements ~ We would like to thank the reviewers and Katrine Hahn for helpful comments on the manuscript.

130

References Bakhtiar, Y. et aI. 2001. Interactions between two arbuscular mycorrhizal fungi and fungivorous nemarodes and control of the nematode with fenamifos. - AppI. Soil EcoI. 17: 107-117. Bj0rnlund, L. and Christensen, S. 2005. How does litter quality and site heterogeneity interact on decomposer food webs of a semi-natural forest? - Soil BioI. Biochem. 37: 203~213. Bj0rnlund, L. et a1. 2002. Nematode communities of natural and managed beech forests - a pilot survey. - Pedobiologia 46: 53-62. Bongers, T. 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. - Oecologia 83: 14-19. Bongers, T. 1994. De Nematoden van Nederland, 2nd ed. Pirola, Schaad, Holland. Bongers, T. 1999. The Maturity index, the evolution of nematode life history traits, adaptive radiation and cp-scaling. ~ Plant Soil 212: 13-22. Bongers, T. and Ferris, H. 1999. Nematode community structure as a bioindicator in environmental monitoring. - Trends EcoI. EvoL 14: 224-228. De Deyn, G. B. et a!. 2004. Plant community development is affected by nutrients and soil biota. - J. Eco!. 92: 824-834. De Goede, R. and Bongers, T. 1994. Nematode community structure in relation to soil and vegetation characteristics. App!. Soil Eco!. 1: 29-44. Djigal, D. et aI. 2004. The influence of bacterial-feeding nema·· todes (Cephalobidae) on soil microbial communities during maize growth. - Soil Bio!. Biochem. 36: 323-331. Emborg, J., Christensen, M. and Heilmann-Clausen, J. 2000. The structural dynamics ofSuserup Skov, a near natural temperate deciduous forest in Denmark. - For. Eco!. Manage. 126: 173-189. Ettema, C. H. and Wardle, D. A. 2002. Spatial soil ecology. Trends Ecol. EvoI. 17: 177-183. Ettema, C. H. and Yeates, G. W. 2003. Nested spatial biodiversity patterns of nematode genera in a New Zealand forest and pasture soil. - Soil BioI. Biochem. 35: 339-342. Freckman, D. W 1988. Bacrerivorous nematodes and organic matter decomposition. - Agriculr. Ecosyst. Environ. 24: 195-217. Garcia-Alvares, A. et al. 2004. Effect ofagricultural management on soil nematode trophic structure in a Mediterranean cereal system. - AppI. Soil Ecol. 27: 197-210. Georgieva, S. et a1. 2005. Early decomposer assemblages of soil organisms in Iitterbags with vetch and rye roots. - Soil BioI. Biochem. 37: 1145-1155. Griffiths, B. S. et aI. 1999. Changes in microbial structure in the presence of microbial-feeding nematodes and protozoa. Pedobiologia 43: 297-304. Hanel, L. 2001. Succession of soil nematodes in pine forests on coal-mining sands near Cottbus, Germany. - App!. Soil Eco!. 16: 23-34. Heilmann-Clausen, J. and Christensen, M. 2004. Does size matter? On the importance of various dead wood fractions for fungal diversity in Danish beech forests. -_. For. Eco!. Manage. 201: 105-119. Heilmann-Clausen,]. et al. 2007. The history and present conditions of Suserup Skov - a nemoral, deciduous forest reserve in a cultural landscape. - Ecol. Bull. 52: 7-17.

ECOLOGICAL HliLLETINS 52, 20m

Ingham, R. E. et al. 1985. Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. - EcoL Monogr. 55. 119-140. Matlack, G. L. 2001. Factors determining the distribution of soil nematodes in a commercial forest landscape. - For. Ecol. Manage. 146: 129~143. Neher, D. A. et al. 2005. Ecosystem type affects interpretation of soil nematode community measures. - Appl. Soil Ecol. 30: 47-64. Nielsen, C. O. 1949. Studies on the soil microfauna II. The soil inhabiting nematodes. - Natura Jutlandica 2: 1-132. Ramalainen, M. L. et al. 2004. Influence of resource quality on the composition of soil decomposer community in fragmented and continuous habitat. - Soil BioI. Biochem. 36: 1983-1996. Ritter, E. and Bj0rnlund, L. 2005. Nitrogen availability and nematode populations in soil and litter after gap formation in a semi-natural beech-dominated forest. - Appl. Soil Ecol. 28: 175-189. Ritter, E. et al. 2005. Light, temperature and soil moisture regimes f()llowing gap formation in a semi-natural beechdominated forest in Denmark. - For. Ecol. Manage. 206: 15-33.

ECOLOGICAL BULLETINS 52.2007

Schiegg, K. 2000. Effects of dead wood volume and connectivity on saproxylic insect species diversity. - Ecoscience 7: 290298. Schmidt, I. K. et al. 2000. Long-term manipulation of the microbes and microfauna oftwo subarctic heaths by addition of fungicide, bactericide, carbon and fenilizer. - Soil BioI. Biochern. 32: 707-720. Sohlenius, B. and Bostrom, S. 2001. Annual and long-term fluctuations of the nematode fauna in a Swedish Scots pine forest soil. - Pedobiologia 45: 408-429. Verhoef, H. A. and Brussard, L. 1990. Decomposition and nitrogen mineralisation in natural and agro ecosystems: the contribution of soil animals..~ Biogeochemistry 11: 175-211. Wright, C.]. and Coleman, D. C. 2000. Cross-site comparison of soil microbial biomass, soil nutrient status, and nematode trophic groups. - Pedobiologia 44: 2-23. Yeates, G. W. 1972. Nematoda of a Danish beech forest. I. Methods and general analysis. Gikos 23: 178-189. Yeates, G. W 1994. Modification and qualification of the nematode maturity index. - Pedobiologia 38: 97-101. Yeates, G. Wet al. 1993. Feeding habits in soil nematode families and genera ~~ an outline for soil ecologists. ~ J. Nematol. 25: 315-331.

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132

ECOLOGICAL BULLFJ'INS 52, 200?

Ecological Bulletins 52: 133-145,2007

Gap regeneration in four natural gaps in Suserup Skov - a mixed deciduous forest reserve in Denmark Katrine Hahn, Palle Madsen and Sara Lindholt

Hahn, K., Madsen, P. and Lindholt, S. 2007. Gap regeneration in four natural gaps in Suserup Skov - a mixed deciduous forest reserve in Denmark. - Eco!. Bull. 52: 133-

145.

Gap regeneration in natural or semi-natural forests is often suggested as a reference for sustainable forest management. To increase the knowledge about gap regeneration, a study of gap formation and regeneration was carried out in four small gaps (200-300 m 2) in the semi-natural deciduous forest Suserup Skov, Denmark 1997-2002. The aim was to improve the understanding of regeneration processes and patterns in natural unmanaged forests, and to use this knowledge as a reference to support similar studies and develop guidelines for management of deciduous forests. There was a good correlation between gap structure, light, and soil moisture but the regeneration response to gap formation was less predictable than expected. This probably reflects the relatively small gaps employed in this study and the highly variable conditions in both time and space of a forest with natural disturbance dynamics. The study also demonstrates the low predictability of regeneration success at the small-scale and in the short term. This is in contrast to common textbook and model descriptions of gap-regeneration that often leave the reader with the impression that spontaneous gap-regeneration is a reliable silvicultural practice.

K Hahn ([email protected]); Forest and Landscape Denmark Univ. of Copenhagen, Roiighedsvej 23, DK-1958 Frederiksberg C, Denmark. - P. Madsen, Forest and Landscape Denmark, UnhJ. ofCopenhagen, Kvak MolieVfj 31, DK-7100 Tlejle, Denmark. - S. Lindholt, Buderupholm Statsskovdistrikt, Mosskovhus, M¢ldrupvej 28, DK-9520 Sk¢rping, Denmark.

The reliability and economic feasibility of beech forest regeneration - natural regeneration in particular - has, for long, been strongly debated in Danish forest management. During the 18th and 19th centuries beech regeneration was mainly by a combination of sporadic coppice and unplanned spontaneous natural regeneration typically following foraging by domestic pigs (pannage). Late 19th and 20th century regeneration developed into well-planned, intensive and reliable methods. Artificial regeneration (direct seeding or planting) became more common as nursery practice and provenance selection was developed Oakobsen 1990, Fritzb0ger 1994). Intensive natural regeneration methods, typically shelterwood regeneration supported by

Copyright © ECOLOGICAL BULLETINS, 2007

soil preparation, liming, weeding, rodent control, and deer fencing etc. were also used. However, increased interest in plantation forestry based on conifers caused a marked decline in beech regeneration from about 1930 to 1990. Within the last two decades, beech has become more popular in both public and private forests, especially in a nature-based context (Hahn et al. 2005) including the maintenance of continuous forest cover, natural regeneration, natural differentiation, and a mixture of different tree species and age groups. Because gap formation is a natural process in most European temperate deciduous forests (Koop and Hilgen 1987, Wagner 1999, Tabaku and Meyer 1999, Emborg et

133

al. 2000), this regeneration approach is highly relevant in a nature-based silviculture context. In the literature, gapregeneration is suggested as a way to foster mixed-species and structurally diverse forests (Watt 1925, Peltier et al. 1997, Emborg 1998, Schutz 2002). Silviculture is the means to achieve the owner's forestry goals, and many owners (both private and public) believe that a naturebased approach offers a better alternative than classical silviculture or plantation forestry. This may include better recognition of biodiversity, environment or wildlife aims in addition to the wood production aims of more traditional silviculture. In nature-based silviculture the silviculturist takes advantage of and mimics the natural processes, species compositions and forest structures of the various forest ecosystems - i.e. by using site adapted tree species and forest structures as well as natural differentiation and regeneration. In a practical context, however, there is a significant lack of knowledge on how to regenerate beech forests in a nature-based way. The present conversion to nature-based forest management (Larsen 2005) highlights the need for development and documentation ofmore well-defined silvicultural methods. Successful and reliable natural regeneration is a key issue in such forestry, thus making an interesting link back to the ideology of the 1781 Royal Forest Decree, which states that the forester should "follow and support Nature in her performance" (Anon. 1781). Natural, non-intervention forests are important reference sites for nature-based forestry, but in Denmark only a few forests have been left unmanaged for> 50 yr. Suserup Skov, which has been a non-intervention forest reserve since 1925 (Fritzb0ger and Emborg 1996), is one of the very few examples of such old beech-dominated forests in Denmark (Emborg et al. 2000). We studied the gap-regeneration dynamics in Suserup Skov to improve the understanding of regeneration processes and patterns in natural unmanaged forests, and ultimately to use this knowledge as a reference for similar studies and for management guidelines. The hypotheses of the study were: 1) regeneration ofbeech and ash shows higher stock density and faster height growth in the gap centres than outside the gaps. 2) Significant effects oflight and soil moisture availability can predict variations in regeneration stock density and height growth.

al. 20(0). Beech Fagus sylvatica, ash Fraxinus excelsior, pedunculate oak Quercus robur and wych elm Ulmus glabra presently dominate the stand, partly reflecting topography, soil conditions and past management activities (pre-1925). The stand structure is characterised by small-scale mosaic with distinct gap regeneration, a high proportion of old trees, and a high level of dead wood (Emborg et al. 2000, Christensen et al. 2005, Ritter et al. 2005, Nielsen and Hahn 2007). The study was based on four small gaps (Gap 1-4) formed by natural breakdown of one or more trees Cfable 1, Fig. 2). The selection of gaps in winter 1997-1998 was based on the presence ofcanopy gaps with no regard to the occurrence of natural regeneration. Gap boundaries (vertical crown projections of canopy trees) were registered twice on a detailed forest map with individual stem positions; at the beginning of the study-period (pre-1999) and after the December 1999-hurricane, which severely hit southern Denmark (Fodgaard and Hansen 2005) (Fig. 3). A grid system of plots with a central north-south base line (120 m) and four parallel sidelines (42 m each; two east and two west of the central base line) were laid out in Gaps 1-3 in spring 1997 to monitor regeneration establishment in the gap as well as in the surrounding dosed forest (Fig. 3). For Gap 4, a similar grid system was established in September 1997 immediately before the gap was formed at a site where we expected a gap to appear in near future due to the presence of a large, fungal-infested Fomes fomentarius beech tree. The grid system in each of Gaps 14 included 91 plots, totalling 364 plots, with a spacing of 3 x6m. Leaf area index (LAl) of the canopy was determined by the Li-Cor LAI-2000 Plant Canopy Analyzer (Welles and Norman 1991) in the years 1997-2002. Simultaneous

Materials and methods Sampling was performed 1997-2002 in the near-natural deciduous forest Suserup Skov (19 ha) in eastern Denmark (55°22'N, 11 °34'E) (Fig. 1). The climate is cool-temperate, sub-Atlantic with an annual mean temperature of 8.1°C and annual precipitation of 644 mm. The soil varies from sandy to loamy and clayey tills, all developed from glacial deposits (Vejre and Emborg 1996). The forest has been continuously forested for at least 6000 yr (Hannon et

134

Fig. 1. Location of Suserup Skov in Denmark.

ECOLOGICAL BULLETINS 52,2007

Table 1. Description of the four gaps in the study; year of gap formation, number of gap makers, cause of gap formation, and gap size (m 2 ). Gap

Year

Cause

Gap makers

'I 2

1997 1995-1997 1997 1997-1998

Senescence Dutch elm disease, expanded in 1999-hurricane Senescence, expanded in 1999-hurricane Single-tree death (snag)

2 beech trees Elm cohort 1 large beech 1 large beech

3 4

measurements of the gap fraction on five concentric rings were taken with the two cross-calibrated sensors in unif()rmly overcast conditions. The above-canopy sensor was placed on open land adjacent to the forest and the belowcanopy sensor was used for measurements 1 m above all plots. A 90 degree cover cap was mounted on both sensors to exclude the northern quadrant canopy of the sensor by orientating the sensors southwards. Hereby, the canopy density ofthe three quadrants; east, south, and west, which influence both direct and diffuse forest floor light, was given priority in the quantification of the light conditions in each plot; see also Madsen and Larsen (1997). Relative light intensity (RLI, the photosynthetic photon flux densities (PPFD, mmol m 2 S-1) in the 400-700 nm waveband) were estimated using the relationships between LAI and RLI in a comparable beech forest in eastern Denmark (Madsen and Larsen 1997).

Size (m 2) pre-1999

Size (m 2 ) after 1999

272

167 782

283 431

300

656 602

Volumetric soil moisture content was measured at all plots along the base line during a dry spell in the vegetation periods of 1998, 1999 and 2002 (Gaps 1-4). All three years were rather wet with above-average summer precipitation, in which dry spells did not occur until late in the summer (Cappelen and J0rgensen 1999, 2000, 2003). Measurements were carried out with a cable tester (Tektronix 1502C) for two sets of probes at each plot at 0-30 em depth using time domain reflectometry (TD R), and data were converted to volumetric soil moisture content by the calibration of Topp et al. (1980) embedded in the software AUTOTDR by Thomsen (1994). Information on other soil characteristics including thickness of litter layer (O-horiwn) and soil texture (clay, silt and sand %), pH, and carbon content (all in the upper 10 em of the A-horizon) was gathered for 69 plots along the base lines in Gaps 1-3 (2000) and analysed in the soil laboratory.

I

o

50

I 100 m

Fig. 2. Position ofthe sampling plots (dark circles) within and around the four gaps. Forest boundaries (forest and wood pastures to the north, east and west; lake to the south) are indicated with black lines, small footpaths within the forest are indicated with grey lines; Gaps 1-4 are marked with numbers.

ECOLOGICAL BULLETlNS 52, 2007

135

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Fig. 3. Diagrammatic representation of the shape of each gap, pre-1999 (stippled black) and after the 1999-hurricane (full line black). Gaps 1-4 are depicted from left to right. The open circles indicate sampling plots; the black circle indicates the sampling plot considered to be closest to the gap's centre.

Regeneration was recorded for all plots within and around all four gaps. We used circular plots of 0.3 m 2 in 1997-2000 and semi-circular plots of 3.5 m 2 in 20012002. Recordings of species, density and height were carried out by the end of the growth season (October-November) each year in the sampling period. Regeneration was defined as all young trees (seedlings and saplings) < 6 m height in the 0.3 m 2 plots, whereas only regeneration taller th..m 0.5 m was recorded in the 3.5 m 2 plots. Plot size and sampling height were changed because a large proportion among the smaller plots had no seedlings. Limits in resources, however, forced us to record only the taller (>0.5 m) seedlings in those larger plots. Regeneration density was calculated for each plot and species as young trees per m 2 • Height of tallest young tree was recorded for each species in each ploL Seed-fall and dispersal was not monitored specifically but a heavy beech mast year was observed in 1998 (unpub!.). Height and species of understorey trees and shrubs (> 1.3 m height) were recorded in all 0.3 m 2 plots in autumn 1999. For the statistical analyses of regeneration response to gap formation, all plots were grouped into two classes of "gap-plot", where plots with an initial light level RLI ~ 2% were considered "gap" and all plots with RLI < 2% were considered "non-gap". The grouping was based on Em-

136

borg (1998), who found that RLI was below 2% in all phases of the forest cycle except in gaps, and that regeneration of ash and beech did not survive at RLI < 2% in Suserup Skov. Also the effect of the four gaps being different was included as a class variable called "gap-effect". A general linear model (Proc GLM) (SAS, ver. 8.2) was used to investigate the effects of the above-mentioned two class variables ("gap-plot" and "gap-effect"), the metric variables "RLI" and "soil moisture" availability and the interaction ("RLI" X "soil moisture") on density and height of the regeneration. All effects were considered significant when p s 0.05.

Results Gap size and shape All studied gaps changed shape and size during the study period. Gap 1 decreased in size, whereas Gaps 2, 3, and 4 increased in size (Table 1). The average gap size was 322 m 2 before the 1999-hurricane but increased to 552 m 2 after the hurricane. The changes were not uniform, and all gaps were somewhat irregular in shape due to a variety of reasons such as the canopy-shapes of broken crowns or fallen

ECOLOGICAL RULLET1NS 52, 2007

trees or domino-like tree falls (Fig. 3). Changes in gap area were due to a combination of closure (growth and ingrowth of understorey and surrounding canopy trees) and expansion (single-tree or multiple-tree windthrows) (Table 1).

Light availability In the year of gap formation, average RLI in plots classified as gap-plot was 6.3% (± 2.9%) in comparison to 1.5% (:to.7%) in "non-gap" plots (Fig. 4, left). The between-gap variation in light conditions was significant (p< 0.0001) with average RLI values of gap-plots ranging from a low of 4.2% ± 0.9% (Gap 1) to a high of7.6% ± 3.7% (Gap 3), reflecting different gap sizes, shapes and orientations. Although most light reached the central part of the gap, it was an irregular pattern. Higher light intensities in the northern section of the gap centre, due to the location of Denmark in the northern hemisphere, were observed in Gaps 2 and 3, but not in Gaps 1 and 4 (Fig. 4, right). Slender understorey trees of beech, ash, and sycamore maple did not affect RLI significantly. However, the scattered elderberry Sambucus nigra (1.45~3 m height) and wych elm (3.5-7 m height) (often with dense sprouts) which had either established before gap formation (typically wych elm) or after gap formation (typically elderberry) caused RLI to be much lower here than in neighbouring plots free of understorey vegetation. The change of RLI over time was largely influenced by the 1999-hurricane. A slow decrease in RLI in gap-plots from 1997 to 1999 was followed by an abrupt increase in 2000, then again followed by a slow decrease in 2001-2002 (Fig. 4, left). The 1999-hurricane also caused a rise in RLI in areas which earlier were under closed canopy, whereas RLI in the original gap opening was reduced (Fig. 4, right).

Soil characteristics and soil moisture availability

analyses of regeneration response. Similarly there were no significant differences between gaps regarding pH, litter depth and carbon content. For all gaps, the average pH was 3.8-4.0, litter layers were quite thin (average 1.1-2.0 em), and the average carbon content was 3.8-4.2% (Table 2). Only for soil texture, there was a significam difference between gaps with Gap 2, in the north-eastern part of the forest having significantly higher sand can tent and lower clay and silt content (p
Regeneration density

There were no significant effects on any ofthe analysed soil variables when dividing the sample plots into "gap" and "non-gap" due to an overall high variation between plots in a gap and they were thus not incorporated in the statistical

Regeneration was dominated by ash, beech, and sycamore maple Acerpseudoplatanus, whereas other species (Aesculus

hippocastanum, Prunus avium, Quercus robur, Sambucus nigra, Sorbus aucuparia, and Tilia platyphyllos) were occa-

Table 2. Mean values and range (in brackets) of soil characteristics (soil texture, pH, carbon content and thickness of litter layer) of plots along the base line in Gaps 1,2, and 3.

Clay % Silt% Sand % pH Carbon % Litter (em)

Gap 1

Gap 2

Gap 3

8.7 (6.0-1-1.0) 15.4 (8.8-21.0) 76.0 (69.0-84.4) 4.0 (3.2-6.2) 4.9 (2.4-5.6) 2.0 (0.2-6.7)

5.7 (4.9-8.0) 9.9 (8.8-13.0) 84.3 (82.0-86.2) 3.8 (3.1-4.7) 3.8 (1.0-6.2) 1.1 (0.0-3.0)

7.7 (5.0-9.0) 12.9 (9.9-16.0) 79.4 (76.2-83.0) 3.8 (3.1-5.1) 4.0 (2.2-8.0) 1.3 (0.3-2.8)

ECOLOGICAL BULLETINS 52, 2007

137

. _10 " -I

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~

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-40

-20

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Fig. 4. Left: average relative light intensity (RLI) for gap-plots (white) and non-gap-plots (black) in the four gaps from time of gap formation to 2002. Right: change in RLI along the north-south gradient of the four gaps. The x-axis runs from -60 m in the north (left), through the gap centre (0 m) to 60 m in the south end (right). Black curve is average RLI of 1997-1999; grey curve is average RLI of 2000-2002. The black horizontal line indicates the 2% RLI threshold.

sionally found. At the time ofgap formation, beech regeneration occurred very sparsely in all gaps « 3 individuals m- 2), ash was sparse in Gaps 1-3 « 3 individuals m-2 ) but higher in Gap 4 (average of7-53 m-2 ). The average regeneration density increased over time, although levelling in year 1999 (Fig. 6). For beech, the effect of the 1998-mast was clearly seen in Gap 3, although many seedlings positioned in non-gap plots disappeared after one year. For ash,

138

regeneration density generally tended to increase under both gap and non-gap condition, except for Gap 4 where regeneration density for non-gap plots decreased strongly from 1999 to 2000. Ash became abundant in all gaps, especially in Gaps 1 and 4, whereas Gap 2 was co-dominated by sycamore maple (Fig. 6). There was a consistent and significant difference in the density of ash seedlings between gaps in the period 1998-

ECOLOGICAL BULLETINS 52. 2007

~ 50 : 40

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Fig. 5. Left: average values per gap ofvolumetric soil moisture content (%) for gap-plots (white) and non-gap-plots Iblack) measured along the north-south gradient in summer 1998, 1999 and 2002 in drought periods. Right: change in soil moisture content along the north-south gradient of the four gaps. The x-axis runs from -60 m in the north (left), through the gap centre (0 m) to 60 m in the south end (right). Black curve is average soil moisture content of 1998-1999; grey curve is soil moisture content of2002.

2002 (Table 3) with most seedlings in Gaps 1 and 4. Moreover, the density of ash seedlings was positively correlated with light availability, expressed as either RLI or RLI x soil moisture interaction by the end of the study (Table 3). Similarly, sycamore maple was positively related to gap, and the majority of maple seedlings occurred in Gap 2. The effects of RLI and gap-plot were significant for some

ECOLOGICAL BULLETINS 52, 2007

years, whereas the effect of soil moisture was very small (Table 3). In contrast to ash and sycamore maple, the density ofbeech seedlings was not strongly related to differences between gaps. Density of beech seedlings was primarily related to RLI and soil moisture availability throughout the period ofstudy (Table 3)" Generally the statistical models only explained a minor proportion of the total variability (R2

139

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Fig. 6. Average seedling density (N m-1 ) and standard deviation for ash, beech and sycamore maple in Gaps 1-4. Thin line = gap-plot. Thick line = nongap-plot. Note: different scaling for ash Gap 1 and Gap 4.

between 5 and 39%) and in many of these models the qualitative "gap-effect" was the main explanatory factor.

Regeneration height growth The general trend was an increase in average and maximum height during the time of the study with seedlings of ash and sycamore maple expressing a stronger height development than beech. Ash increased from a maximum height of 4-30 cm (1997) to 12-70 cm (2000). In all fouf gaps average height development of ash was stronger in gap-plots than in non-gap plots, and with the average height of ash in non-gap plots decreasing consistently in Gaps 2, 3, and 4 (Fig. 7). For beech, height typically increased from 14-17 cm (1997/1998) to 19-43 (2000).

140

The average height development of beech seedlings was only detectable for plots defined as "gap" from 1999 to 2000 (Fig. 7). Non-gap plots had very few observations. For sycamore maple, present only in Gap 2, height increased from 12~29 cm (1997) to 29-220 cm (2000). The development in average height was much stronger in gapplots than in non-gap-plots (Fig. 7). The height of the tallest ash seedling per plot was positively affected by light (either "gap-plot", or RLI) and/or soil moisture in all years except the first years of study (1997 and 1998) (Table 4). In contrast, the height of the tallest beech seedling per plot was only correlated with light and soil moisture in one year (1999). The height of sycamore maple seedlings was apparently not correlated with any of the variables, except for the last two years, where a significant effect of "gap-plot" was observed (Table 4).

ECOLOGICAL BULLETINS 52, 20(}7

Table 3. General linear models of density of ash, beech and sycamore maple regeneration in Gap '1~4 in years 19982002. The table shows significant effects (p-values) of gap, gap-plot, RLI, moisture, and the interaction between RLI and moisture and R2 for the models. Ash R2

Beech p-value

'1997

R2

0.1019

p-value

R2

Sycamore maple p-value

1998

0.1403

Gap: <0.0001

0.0458

Gap: 0.0072 RLI: 0.0351 RLI x moisture: 0.0268

'1999

0.3951

Gap: <0.000'1

0.1503

Moisture: 0.0032

0.1071

2000

0.2537

0.0636

RLI: 0.0088

0.1383

20m

0.2201

Gap: <0.0001 Gap-plot: 0.0254 Gap: <0.0001

Gap: 0.0002 Gap-plot: 0.0383 RLI: 0.0333 Gap: <0.0001 RLI: 0.0086 Gap: 0.0015

0.0738

0.1546

Gap: <0.0001

2002

0.1901

Gap: 0.0079 RLI: 0.0189 RLI x moisture: 0.0051

0.3886

Gap-plot: 0.0139 RLI: <0.0001 RLl: <0.0001 RU x moisture: <0.0001

0.1977

Gap-plot: <0.0001 RLI x mOisture: 0.0008

Discussion The study focussed on the spontaneous natural regeneration in a non-intervention deciduous forest, where formation of tree-fall gaps is an important part of the structural dynamics. The four gaps selected for the study were all subject to natural dynamics, primarily caused by strong storms, but lateral ingrowth also caused changes in shape and size. Average gap size changed from 322 to 514 m 2 after the 1999-hurricane. A comparison with the mean gap size of 450 m 2 f()r all gaps in Suserup Skovafter the hurricane (Bigler and Wolf 2007) indicates that the gaps selected for this study were within the "normal" size range for Suserup Skov, thereby underlining their predictive value.

Light and soil moisture availability The between-gap variation was rather high due to differences in gap structure, site conditions and topography with RLI ranging ca 2-13% in gap-plots compared to ca 1-2% in non-gap-plots. Although most light reached the central part of the gap, it was an irregular pattern, making it difficult to depict perfectly bell-shaped patterns of RLI right after gap formation as reported from other studies (Bauhus and Bartsch 1996, Emborg 1998, Page and Cameron 2006). The expected higher light intensities in the northern section of the gap centre, as an effect of Denmark's location in the northern hemisphere (Canham et al. 1990), were only observed in two out of four gaps, due to gap shape irregularities and partial shade from understorey trees and shrubs. The structural changes following the 1999-hurricane showed that gaps were not permanent in either shape or size, showing how light conditions can

ECOLOGICAL BULLETINS 52. 2007

0.0972

Gap: 0.0015

0.2166

change quite rapidly, creating new gaps in closed forest, enlarging existing gaps, and hampering regeneration in existing gaps due to fallen trees. The patterns ofsoil moisture content be-rw-een and within gaps were, like the light availability, rather heterogeneous. However, an effect of gap formation was visible, with higher soil moisture availability in the gap centre during dry periods ofthe growing season. The within-gap variation was partly due to the presence of sub-canopy trees within and around the gaps, and local topography (gaps on slopes, small, wet depressions). In conclusion, there were significant effects of gap formation on light and soil moisture, although the spatial relationship between gap size and shape and the availability oflight and soil moisture was less clear than reported from other studies (Bauhus and Bartch 1996, Ritter and Vesterdal 2005, Ritter et al. 2005, Page and Cameron 2006). These two variables only explained a small proportion ofthe total variation in regeneration density whereas a larger proportion of the height growth was explained by particularly light. We therefore concluded that light availability and soil moisture are only "weak" predictors for spontaneous regeneration in gaps of the size and over a six year period as studied here.

Response to gap formation: regeneration density and height growth Natural regeneration in gaps is often described in the literature, particularly in textbooks, as perfectly bellshaped patches of seedlings and saplings, with the tallest individuals in the gap centre and a gradual decline in density and height towards the periphery (Watt 1925, Mayer 1977, Oldeman 1990, Matthews 1991, Schlitz 2004).

141

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~ 13o·j

1,40

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1997

1998

1999

2000

i

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2000

Fig. 7. Average seedling height (em) and standard deviation for ash, beech and sycamore maple in Gaps 1-4. Thin line = gap-plot. Thick line = non-gap plot. Note: different scaling for sycamore maple Gap 2.

Such an artistic representation is unlikely to be true in all real situations, and this study showed that although regeneration was present in all gaps it was also rather diffuse and with less regular regeneration patterns with possible no gap-effect on the density of seedlings. One likely explanation is that young seedlings may survive under a canopy cover for some years, thereby blurring the ideal picture of a bell-shaped regeneration curve (Peltier et al. 1997, Emborg 1998). One example is the marked increase in beech seedling density from 1998 to 1999, especially in "non-gap" plots ofGaps 3 and 4. This increase could easily be related to the mast year of 1998, resulting in beech seedlings germinating at all available sites, even under lower light intensities. The drop in density in 2000 is likely linked to the fact that some ofthose seedlings established under too low light levels. Indeed the world's forests show many examples of bellshaped regeneration patterns under canopy gaps. However, it is important to remember that the bell-shaped regenerations

142

we observe are those that established. Those that did not are invisible at a glance and needs research data to be included in the whole picture. This study does not include treatments that can help us quantifY the deer browse impact on the regeneration. Suserup Skov itself and the surrounding landscape seem to be perfect habitat for roe deer C:apreoLus capreolus and it is likely that the regeneration at our study sites is influenced by deer. Olesen et al. (2002) provides for 1999 an overall Danish roe deer population estimate of300000-400000 roe which corresponds to 7-9 deer km-2 and with an annual harvest of2.5 km-2. The deer harvest data are reported as county averages and vary in the range 1.6--5.7 km-2 , which may reflect average deer populations up to ca 20 deer km~l. Additionally, ideal sites like Suserup Skov probably support even denser populations. The breakdown of2-3 canopy trees in a deciduous forest particularly increases soil moisture but also relative light

ECOLOGICAL BULLETINS 52, lOO?

Table 4. General linear models of height of ash, beech and sycamore maple regeneration in Gap 1-4 in the years 19982002. The table shows significant effects (p-values) of gap, gap-plot, RU, moisture, and the interaction between RU and moisture and R2 for the models. Beech

Ash

R2 1997 1998 '1999 2000 2001 2002

p-value

p-value

0.0921

Moisture: 0.0037

0.1886

RLI: <0.0001

0.3604

Gap: 0.0057 Moisture: 0.0470

0.4701

Sycamore maple p-value

RLl: 0.0018 RLl x moisture: 0.0006

intensity within the gap compared to a closed canopy situation. A gap opening therefore induces a sudden change in potential growth conditions for regeneration, which typically reaches 10-15 m from the gap centre making a potential regeneration site of 300-700 m 2 • In some gaps regeneration is fast, while other gaps appear to have a slower regeneration rate, causing a relatively low predictability of regeneration at the small-scale and in the short term. Thus, gaps - in the short term - are not solely responsible for establishment of regeneration, but should perhaps rather be seen as opportunities in time and space for regeneration that is already established. It should therefore be considered if chance plays a bigger role than determinism in regeneration processes. Similar considerations were given by Hubbell et al. (1999) and Obiri and Lawes (2004) in subtropical and tropical forest ecosystems. In a study ofa tropical forest Hubbell et al. (1999) found that gaps do promote tree diversity, but mainly by increasing communitywide seedling establishment, and they therefore stated that gaps playa relatively neutral role in maintaining species diversity, promoting whatever diversity and mix of tree species that happens to be locally present in a given forest for reasons other than the local disturbance regime. Thus a strong recruitment limitation appears to decouple the gap disturbance regime from control of tree diversity. Ash and sycamore regeneration seemed to be much more responsive to light intensity than beech. This corresponds well with other gap studies showing that successful regeneration of both ash and sycamore maple was most frequent at sites with high levels of both diffuse and direct solar radiation (Schmidt 1996, Diaci 2002). Also Einhorn et al. (2004) measured that 1-yr old ash seedlings were significantly taller than beech seedlings growing in gaps under semi-controlled conditions and that 2-yr old ash seedlings grew rapidly in height compared to the beech seedlings (Einhorn 2007). The height of beech seedlings may, although it did not increase immediately after gap creation, increase regularly in the following years (Collett et al. 2001), but mixed with ash the beech regeneration will face hard competition.

ECOLOGICAL BULLETINS 52, 2007

R2

0.3359 0.0444

Gap-plot: 0.0001 Gap-plot 0.0353

Because drought is an important factor causing seedling mortality (Topoliantz and Ponge 2000) and possible altered competitive status between beech and ash seedlings (Wagner 1999), we expected soil moisture availability within and around the gaps to be an important factor controlling regeneration density and height. Our study could confirm this only for density of beech seedlings and height growth of ash seedlings, as these two were positively influenced by higher soil moisture. In conclusion, the hypothesis about higher regeneration density and faster growth in the gap centre than outside the gaps could not be fully confirmed. The high variation in seedling response to gap formation probably reflects the highly variable conditions ofa forest with natural disturbance dynamics and a dense roe deer population. This study includes a number oftypical but relatively small gaps as they often appear in the forest. However, a six-year study-period may not leave the seedlings enough time to establish and develop. Additionally, larger and more regular or circular gaps without a dense crop of remaining understorey trees might also have shown a more "textbooklike" regeneration results (Mayer 1977, Oldeman 1990, Matthews 1991).

Implications for nature-based silviculture Light penetration to the forest floor was strongly influenced by the structural properties of the canopy and is therefore one of the most easily manipulated forest variables. Thus, by use ofsimple harvesting techniques it is possible to alter the microclimatic conditions in a homogeneous stand considerably. This knowledge has practical application in situations where it is desirable to shift towards more heterogeneous stand structure by supporting group regeneration patterns, or where e.g. target diameter harvest ofthe old and mature stand gradually and slowly opens the stand. However, our study showed that plants of ash and sycamore maple apparently grew faster than beech at all light levels - at least in the shorr term. This means that the

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silvicultural assumption ofa detailed regulation of the light availability at the forest floor can steer the species composition of the regeneration is not confirmed. In the case of more light-demanding species, e.g. oak and cherry, these were not present in significant amounts in the present study despite the presence of seed sources. Although it is expected that larger and more consistent gaps are necessary in order to initiate the process of natural regeneration and support the establishment success of those species, we can therefore not exclude the possibility for other species to establish faster or more densely under those conditions. We have, however, not been able to survey the experiments long enough to describe the long-term effects. The lack of significant gap-plot effects on regeneration density and height as well as the low predictability of light and soil moisture indicate that the regeneration we have observed may disappear again if the gaps close. This study shows that the regeneration may establish and initiate growth in gaps with remaining understorey trees, although the presence of shading elderberry and wych elm locally lowered the RLI strongly and thereby also the chances for regeneration to establish and survive. In practical forestry the understorey trees may be useful to help keeping the forest floor conditions under control during a regeneration phase, where the mature trees are felled. The forester is recommended to leave and protect the undersrorey trees as much as possible during the felling operations. He or she may then fell the undersrorey trees as the desired regeneration is established and needs less competition for light and soil moisture. An understorey is also useful during the whole rotation in a managed forest since it supports the forest micro-climate and protects against strong vegetation competition that may cause problems during the regeneration phase. Additionally, it physically protects the soil and tree roots against soil compaction and damage from heavy skidders and related machinery if the understorey is protected by declaration from the forest administration. Acknowledgements - Thanks to Sor0 Akademi for permitting research in Suserup Skov. The project was supported financially by ED-projects "Renfors" and "NatMan", and the Danish Research Council project "SpyNatForce". We thank Lars Birck, Sebastian S0rensen, Maren Madsen, Stine Rytter, Anders Busse Nielsen, Rune Kristensen, Arne Hahn, and Kristian S0gaard for heip with data collection, Sashia Nazim for analysing soil samples, and Ralph Harmer and Christian Ammer for valuable review comments.

References Anon. 1781. The Royal Forest Decree: forordning angaaende de kongeiige skove og t0rvemoser udi Danmark, 5: §63. Bauhus, J. and Bartsch, N. 1996. Fine-root growth in beech (Fagus sylvatica) forest gaps. - Can.]' For. Res. 26: 21532159.

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Bigler, ]. and Wolf, A. 2007. Structural impact ofgale damage on Suserup Skov, a near-natural temperate deciduous forest in Denmark. - Ecol. Bull. 52: 69-80. Canham, C. D. et al. 1990. Light regimes beneath dosed canopies and tree-fall gaps in temperate and tropical forests. Can. J. For. Sci. 20: 620~631. Cappelen, J. and Jorgensen, B. 1999. Danmarks klima 1998, med tilLrg af Eeroerne og Gf0nland. - Danmarks Meteologiske Inst., Trafikministeriet. Cappelen, ]. and J0rgensen, B. 2000. Danmarks klima 1999, med tillxg af Fxroerne og Gf0nland. - Danmarks Meteologiske Inst., Trafikministeriet. Cappelen, J. and Jorgensen, B. 2003. The climate of Denmark 2002 with the Faroe Islands and Greenland. Technical report 03~02. - Danish Meteorological Inst., Ministry ofTransport, <www.dmi.dk>. Christensen, M. et al. 2005. Dead wood in European beech (Fagus ~Jlvatica) forest reserves. - For. Ecol. Manage. 210: 267282. Collett, c., Lanter, O. and Pardos, M. 2001. Effects of canopy opening on height and diameter growth in naturally regenerated beech seedlings. -Ann. For. Sci. 58: 127-134. Diaci, ]. 2002. Regeneration dynamics in a Norway spruce plantation on a silver-fir beech forest site in the Slovenian Alps. For. Ecol. Manage. 161: 27--38. Einhorn, K. S. 2007. Growth and photosynthesis of ash Fraxinus excelsior and beech Fagus sylvatica seedlings in response to a light gradient following natural gap formation. Ecol. Bull. 52: 147-165. Einhorn, K. 5., Rosenqvist, E. and Leverenz, J. W. 2004. Photoinhibition in seedlings of haxinus and Fagus under natural light conditions: implications for forest regeneration? - Oecologia 140: 241-251. Emborg, J. 1998. Understorey light conditions and regeneration with respect to structural dynamics ofa near-natural temperate deciduous forest in Denmark. - For. Ecol. Manage. 106: 83-95. Emborg, ]., Christensen, M. and Heilmann-Clausen, ]. 2000. The structural dynamics ofSuserup Skov, a near natural temperate deciduous forest in Denmark. - For. EcoL Manage. 126: 173-189. Fodgaard, S. and Hansen, N. (eds) 2005. Decemberorkanen fem ar ener. [December hurricane - five years after.] - Skoven 1: 26-31. Fritzb0ger, B. 1994. Kulturskoven. Dansk skovbrug fra oldtid til nutid. - Gyldendal. Fritzboger, B. and Emborg, J. 1996. Landscape history of the deciduous forest Suserup Skov, Denmark, before 1925. For. Landscape Res. 1: 291-309. Hahn, K. et aI. 2005. Forest rehabilitation in Denmark using nature-based forestry. - In: Stanturf, J. A. and Madsen, P. (cds), Restoration of boreal and temperate forests. CRC Press, pp. 299-317. Hannon, G. E., Bradshaw, R. and Emborg, J. 2000. 6,000 years of forest dynamics in Suserup Skov, a semi-natural Danish woodland. - Global Ecol. Biogeogr. 9: 101-114. Hubbell, S. P. et al. 1999. Light-gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. _. Science 283: 554-557. Jakobsen, B. 1990. Bogeforyngelser i dansk skovbrug de sidste 200 ar. - Det Forstlige Forsogsvxsen i Danmark 42: 234265.

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Koop, H. and Hilgen, P. 1987. Forest dynamics and regeneration mosaic shifts in unexploited beech (Fagus sylvatica) stands at Fontainebleau (France). - For. Ecol. Manage. 20: l.? 5-150. Larsen, J. B. (ed.) 2005. Naturn~r skovdrift. - Dansk Skovbrugs Tidsskrift 1-2. Madsen, I~ and Larsen,]' B. 1997. Natural regeneration of beech (Fagus sylvatica L.) with respect to canopy density, soil moisture and soil carbon content. - For. Ecol. Manage. 97: 95-105. Matthews, ]. D. 1991. Silvicultural systems. Oxford Science Pub!. Mayer, H. 1977: Waldbau auf soziologisch-okologischer Grundlage. - Gustav Fischer. Nielsen, A. B. and Hahn, K. 2007. What is beneath the canopy? Structural complexity and understorey light intensity in Suserup Skov, eastern Denmark. - Eco1. Bull. 52: 43-52. Obiri, J. A. E and Lawes, M. J. 2004. Chance versus determinism in canopy gap regeneration in coastal scarp forest in South Africa. - J. Veg. Sci. 15: 539-547. Oldeman, R. A. A. 1990. Forests: elements of silvology. - Springer. Olesen, c:. R., Asferg, T. and Forchhammer, M. c:. 2002. Radyret - era fatallig til almindelig. - TEMA-rapport fra DMU 39. Page, L. M. and Cameron, A. D. 2006. Regeneration dynamics of Sitka spruce in artificially created gaps. - For. Ecol. Manage. 221: 260-266. Peltier, A. et a!' 1997. Establishment of Fagus sylvatica and Fraxinus excelsior in an old-growth beech forest. "~- ]. Veg. Sci. 8:

13-20. Ritter, E. and Vesterdal, L. 2005. Gap formation in Danish beech (Fagus Jylvatica) forests of low management intensity: soil moisture and nitrate in soil solution. - Eur. J. For. Res. 125:

139-150. Ritter, E., Dalsgaard, L. and Einhorn, K 5.2005. Light, temperature, and soil moisture regimes following gap formation in a semi-natural beech-dominated forest in Denmark. -" For. Eco!' Manage. 206: 15-33.

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Schmidt, W 1996. Zur Entwidclung det Veriilngung in zwei Femellilcken cines Kalkbuchenwaldes. - Forst und Holz 51:

201-205. Schiltz, ].-P. 2002. Silvicultural tools to develop irregular and diverse forest structures. Forestry 75: 329-337. SchUtz, J.- P. 2004. Opportunistic methods of controlling vegetation, inspired by natural plant succession dynamics with special reference to natural outmixing tendencies in a gap regeneration. - Ann. For. Sci. 61: 149-156. Tabaku, V and Meyer, P. 1999. Lilckenmuster albanischer und mitteleuropaischer Buchenwalder unterschiedlicher Nutzungsintensitat. - Forstarchiv 70: 87-97. Thomsen, A. 1994. AUTOTDR for making automated TDR measurements of soil water content. User's guide, ver. 01, January 1994. - SP report no. 38, Ministry of Agriculture, Danish lnst. of Plant and Soil Science, Denmark. Topoliantz, S. and Ponge, J.-F. 2000. Influence ofsite conditions on the survival of Fagus sylvatica seedlings in an old-growth beech forest. - ]. Veg. Sci. 11: 369-374. Topp, G. C, Davis,]. L. and Annan, A. P. 1980. Electromagnetic determination ofsoil water content: measurements in coaxial transmission lines. - Water Resour. Res. 16: 574-582. Vejre, H. and Emborg, J. 1996. Interactions between vegetation and soil in a near-natural deciduous forest. - For. Landscape Res. 1: 335-347. Wagner, S. 1999. Okologische Untersuchungen zur Initialphase der Naturverjilngung in Eschen-Buchen-Mischbestanden. - Schriften aus der Forstlichen Fakultat der Univ. GOttingen und der Niedersachsischen Forstlichen Versuchsanstalt, ]. D. Sauerlander's Verlag Frankfurt am Main, Band 129. Watt, A. S. 1925. On the ecology of British beechwoods with special reference to their regeneration. Part 2, sections II and III. - ]. EcoL 27-73. Welles, J. M. and Norman, J. M. 1991. Instrument for indirect measurement of canopy architecture. - Agron. J. 83: 818-

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Ecological Bulletins 52: 147-165,2007

Growth and photosynthesis of ash Fraxinus excelsior and beech Fagus sylvatica seedlings in response to a light gradient following natural gap formation Katrina S. Einhorn

Einhorn, K. S. 2007. Growth and photosynthesis of ash Fraxinus excelsior and beech Fagus sylvatica seedlings in response to a light gradient following natural gap formation. - Eco1. Bull. 52: 147-165.

The photosynthetic and morphological responses of ash and beech seedlings were studied along the light gradient in a small, naturally-formed gap and into the surrounding forest in Suserup Skov. Potted seedlings were used to eliminate water and nutrient availability as co-varying factors. Seedlings were placed along perpendicular transects through the center of the gap for the first two years after gap formation. Survival, growth, biomass allocation, net photosynthesis and maximum quantum yield were measured. Differences in the plasticity, defined as the slope of the response, of ash and beech to the gradient of light through the gap were also investigated. Both ash and beech seedlings showed a significant increase in overall growth with increasing irradiance up to almost 8 mol m-2 d l averaged over the growing season. During the first growing season, however, the species had significantly different strategies for growth and biomass allocation. Ash seedlings invested primarily in belowground biomass, while beech seedlings had more typical shade-plant morphology; with high leafarea and leaf weight ratios. In the second growing season, ash seedlings grew rapidly in height, suggesting that explosive growth of gap-specialist species relies on the early establishment of a large root system to supply water to the rapidly growing shoot in subsequent years. Beech seedlings, on the other hand, showed significant branching of the crown. These results support the hypothesis that there is a trade-offbetween height growth and crown width in regenerating tree species. The plasticity of a number of morphological traits was higher in ash than in beech. There was no significant difference in the plasticity of photosynthesis; however, this may have been attributed to noisy data. Measurements of maximum quantum yield suggested that beech seedlings were experiencing mild chronic photoinhibition, which increased with increasing irradiance. It is, however, suggested that factors such as crown morphology and biomass allocation have a much more central role than photosynthesis in explaining the patterns of growth and survival seen in the early stages of gap capture by these two species.

K S. Einhorn ([email protected]), The Arboretum, Forest and Landscape Denmark, Univ. ofCopenhagen, Kirkegaardsvej 3A, DK-2970 Horsholm, Denmark.

In Suserup Skov, studies have established the role of ash Fraxinus excelsior as a mid-successional, gap-specialist species, which requires sizable gaps to reach the upper canopy, while beech Fagus sylvatica can exist as a large sapling in the

Copyright © ECOLOGICAL BULLETINS, 2007

understorey for many years before finally reaching the canopy (Emborg et al. 1996, Emborg 1998). Beech is the most important deciduous tree species in the cool-temperate deciduous forests of central and northern Europe. It is

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characterized by an extraordinary dominance and competitive force due to its high shade tolerance, dark understorey, longevity and a wide range in climatic tolerance Oahn 1991). Brzeziecki and Kienast (1994) have classified beech as a competitive stress tolerator according to the life strategy classifications of Grime (1977). Trees belonging to this group are characterized by large, well-equipped seeds to buffer against the initial stresses of establishing in heavily shaded habitats (Grime 1979), as well as slow initial growth due in part to investment in protective compounds. Ash is a common deciduous tree species found throughout the climatic range of beech and is often a major component of cool-temperate beech forests on mesic calcareous soils with ample water supply Oahn 1991). Ash is characterized as a competitor species, which avoids extreme climates and soil environments and is most successful on productive forest sites (Brzeziecki and Kienast 1994). Where resource levels are high, ash is expected to overgrow and out-compete beech in the early stages of stand development, by monopolizing resource capture (Grime 1977) through high growth rates, tall stature and vigorous lateral spread above and below ground. However, the costs involved with active foraging for resources in combination with high rates of herbivory make the competitive strategy ofash unsuccessful on less productive sites (Grime et al. 1989). While both species are very shade tolerant as young seedlings (Boysen Jensen 1929), the ability to tolerate shade declines more rapidly with increasing size in ash than in beech, probably due to differences in crown architecture (Boysen Jensen 1929) which ultimately lead to a more rapid decline in the efficiency ofleafdisplay (Horn 1971). Ash is generally superior to beech when competing to dominate a forest gap and ash continues to dominate the stand throughout the early stages of the forest cycle (M0ller 1966, Diekmann et al. 1999, Rust and Savill 2000, Emborg et al. 2000). The occurrence ofcanopy gaps and sufficiently rich soils are therefore fundamental to the persistence of ash in Suserup Skov. There is a good understanding of the shifts in species composition that accompany the forest cycle discussed by Emborg et al. (2000) for the Suserup Skov ecosystem, and many studies have established the ecophysiological responses to light of beech in particular (Madsen 1994, 1995, Johnson et al. 1997, Tognetti et al. 1997, Reynolds and Frochot 2003). However, direct comparisons of the growth strategies and physiological responses of ash and beech to variations in the natural light climate of a forest are few (though see Peltier et al. 1997, Rust and Savill 2000 and references therein). Interspecific differences in patterns of biomass- and nitrogen-allocation can significantly alter species competitive relations during seedling and sapling development across the gap-understorey continuum (Niinemets 1998). In addition, excess irradiance has been found to cause photoinhibition in the seedlings

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of some tree species (Mulkey and Pearcy 1992, Pearcy 1994, Lovelock et al. 1994, Krause and Winter 1996, Naidu and DeLucia 1997, Tognetti et al. 1997, Kitao et al. 2000, Leakey et al. 2003, Einhorn et al. 2004). Beech has been shown to experience chronic photoinhibition under open and gap light conditions in the field due to a limited ability to acclimate photochemical capacity to high light conditions (Einhorn et al. 2004). The aim of this study was to investigate the morphological and physiological mechanisms behind the survival and growth of ash and beech seedlings in a forest canopy gap and the surrounding understorey. I know of no other study that has attempted to investigate the causes of the clear superiority of ash over beech in response to the creation of a forest gap. Survival, growth, biomass allocation, net photosynthesis and the occurrence of photoinhibition are estimated across the gradient oflight in a natural gap in Suserup Skov. Slopes of linear regressions of the different variables of growth, allocation and photosynthesis were used to quantify plasticity. More specifically, the following hypotheses were tested: 1) the light gradient across a naturally occurring forest canopy gap influences the survival, growth and photosynthesis of ash and beech seedlings in the first two years after formation independent ofvariation in soil conditions across the gap. 2) Being a gap-specialist species, ash will grow faster in height in the gap, while beech will expand its crown to maximize light capture in the shade. 3) Differences in maximum rates of photosynthesis or average daytime net photosynthesis explain differences in survival and growth between the species. 4) Ash shows more plasticity in the response of growth, allocation and photosynthetic rates to the light gradient across the gap than beech. 5) Seedlings growing in a forest gap experience photoinhibition when exposed to high irradiance. This photoinhibition will be more apparent in beech seedlings than in ash seedlings.

Materials and methods Experimental site and design The experiment was conducted during the 2000 and 2001 growing seasons in a naturally created gap in the beechdominated forest reserve, Suserup Skov, in central Zealand, Denmark (55°22'N, 11 °34'E, 19.2 ha). The surrounding forest is dominated by European beech Fagus sylvatica (ca 61 % of stand basal area), with common ash Fraxinus excelsior (ca 24% ofstand basal area) as a frequent element (Dalsgaard unpub!.). The structure, dynamics, species composition, history and soil conditions of SusefUp Skov are well described (see other papers in this volume, as well as Fritzb0ger and Emborg 1996, Vejre and Emborg 1996, Emborg et a1. 1996,2000, Emborg 1998, Hannon et al. 2000). The gap used as the site for this experiment was formed during a storm on 3 December

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1999, resulting in the destruction of a major portion of the crown of a large beech tree. The surviving portion of the crown carried live foliage the following summer, so the gap may best be described as a branch-fall gap. The gap and some of the adjacent forest were fenced in March 2000 to avoid browsing by deer at the study site. A detailed description of the experimental design is given in Ritter et al. (2005) and is therefore only briefly described here. In 2000, 36 potted seedlings of each species (ash and beech) were placed in 30 plots along a northsouth and east-west-oriented pair of transects which crossed in the middle of the gap and continued into the understorey beyond the gap edges. The study was conducted using potted seedlings to allow for a constant availability of nutrients and water across the gap, thereby isolating the effects of the natural variations in light caused by the canopy gap. In 2001, all potential survivors from the original 30 plots were placed back in their original plots (see below). Only 24 plots had surviving plants after bud break. Plots were ca 1 m2 and spaced at intervals of 3-8 m from 22 m south to 36 m north and 36 m east to 30 m west of the gap center. The density of potted seedlings was much lower than that of the natural regeneration in the central and northern parts of the gap. The edge of the gap (canopy crown edges) was estimated to lie at ca 12 m north, 12 m south, 8 m east and 16 m west of the gap center, however, the presence of saplings and the large gapmaker tree made definition of the exact transition from gap to understorey difficult. Plots are abbreviated according to position, for example "NO?,' for north, 7 m. Seedlings were investigated for the first two growing seasons after gap formation 0- and 2-yr-old seedlings).

Plant material Seeds of ash and beech obtained from Hedeselskabet (Farvang, Denmark) were sown on 10 April 2000. Beech seed material originated from a managed beech stand (Alsted Skov), while ash seed was collected in a seed plantation in northern Zealand (Tisvilde Hegn), ca 10 and 90 km from Suserup Skov, respectively. Seeds were sown in 0.25 I plastic pots containing a mixture of 59% peat, 20% LECA (Light Expanded Clay Aggregate) for aeration, 10% sifted ash forest soil (collected from the plantation at Tisvilde Hegn), 10% sifted beech forest soil (collected from Alsted Skov) and 1% cut ash and beech roots. Due to the protected status of Suserup Skov, it was not possible to obtain soil directly from the study site. Ash and beech soil and roots were added to give the appropriate microbial composition to the potting soil. The extent to which mycorrhizal associations were achieved was not investigated, though some were observed when the plants were harvested. Osmocote Plus Mini slow-release fertilizer was mixed into the soil at a concentration of 1 kg m-3 (16-8-11 NPK, 3-4 month). Seedlings were placed outdoors under

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50% shade net to germinate. After germination, pots with viable seedlings were selected and transporred to Suserup Skov. The potted seedlings were placed in the plots along the transects 17-23 May 2000. Since watering of seedlings was not possible at the experimental site (due to the other investigations being made in the same gap), each pot contained a strip of quilted fabric - a "wick" - placed from the soil surface and down through the pot, hanging ca 20-30 cm out of the bottom. The purpose ofthis wick was to soak water from a container above which the pots were suspended, so that the soil in the pots was always moist. The year 2000 growing season proved to be so wet, however, that it was only necessary to remove water from the containers rather than to add water. Water was therefore abundantly available throughout the study. Pots were shielded from direct sunlight by white shade cloth. Seedlings not harvested at the end of the year 2000 growing season were left to form buds and winter harden through the autumn in situ. On 5 December 2000, all seedlings were collected and returned to the Arboretum of The Royal Veterinary and Agricultural Univ. in H0rsholm, Denmark, to overwinter outdoors. To avoid frost damage to roots, pots were buried in LECA up to the top of the pots. Seedlings were carefully lifted and repotted in an unheated greenhouse in January 2001 into 2 I plastic pots using a mixture of75% peat, 20% LECA and 5% clay. No forest soil was added when reponing under the assumption that any microorganisms would spread to the new soil from the old soil core which was transferred undisturbed to the new pots. The wick was removed during repotting. l~ertilizer was added to the soil as in 2000. Seedlings were returned to their original positions in the gap in Suserup Skov at the end of March 2001, before bud break in either seedlings or canopy trees, but after the period when frost damage to roots in exposed pots might occur.

Photosynthetically active irradiance Photosynthetically active irradiance (I p) was monitored through each growing season in each plot. L, was measured as the photosynthetic photon flux fluence rate (PPFFR) (j.11I101 m- 2 S-1) in the 400-700 nm waveband using spherical sensors constructed from gallium arsenide phosphide photodiodes (see Aaslyng et al. 1999 for a detailed description of this photodiode) placed inside table-tennis balls. Two sensors were placed in each plot, just above the tops of the seedlings. I p was logged every lOs and the 10 min average was recorded from 13 June to 7 November 2000 and II May to 30 October 200 1 (data missing for 14 September-4 October 2001). Measurements ofI p are reported in more detail in Ritter et al. (2005). I p is presented here as the integrated daily I p for specific days or as the average integrated daily II' for the period 14 June-13 September (period common for both years).

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During measurements of leaf gas exchange and chlorophyll fluorescence, Ip was also measured using a cosine-corrected quantwn sensor adjacent to the upper leafsurface (built into the instruments). In this case, II' was measured as the photosynthetic photon flux density (PPFD) (J1rnol m- 2 S-l).

Survival Survival of seedlings was recorded at the end of each growing season: that is, at the first harvest in October 2000 and at the final harvest in September 200 1. The fraction ofsurviving seedlings at the final harvest was adjusted for the plants removed during the first harvest.

Growth and allocation Seedling competitive height growth was measured at intervals throughout the experiment: 3-4 July and 9-10 October 2000, and 29-30 May, 3-5 July, 2-3 and 29-30 August 2001. Competitive height in mm was recorded as the height of the seedling from the soil surface to the height of the uppermost leaf lamina in its natural position. It was necessary to distinguish between this measure of seedling height and the simple measure of stem height (referred to here as main stem length) because of the differences in aboveground architectUre of ash and beech seedlings. Ash tends to have a shoft stem, but long petioles, while beech seedlings have longer stems, but shoft petioles, so that leaves are attached much closer to the stem. Thus, ash seedlings achieve a larger height for a given stem length than beech and the main stem length can therefore be misleading. From 9 to 13 October 2000, one third of the seedlings in each plot were randomly selected for harvest (12 individuals of each species per plot). Before harvest, seedling architecture was described as the degree of branching in the seedlings: unbranched, bilaterally forked, multilaterally forked or broom-shaped. Roots were rinsed and seedlings partitioned into roots, stems and leaves. Leafarea was measured using a LI-COR 3000 leaf area meter. Cotyledons were included in the total leaf area if they were still green. Main stem length was measured as the length of the stem from the soil surface to just below the terminal bud (lateral branches were not included in this measure). Stem diameter was measured to 1/100 mm at the base of the stem, just above the soil surface, using a digital caliper. All plant parts were dried at 70°C for at least 48 hand weighed. The following biomass allocation variables were then calculated: leaf area ratio (LAR, cm 2 leafarea g-l plant biomass), leafweight ratio (LWR, g leafg-l plant biomass), specific leaf area (SLA, cm 2 leaf area g-l leaf biomass) and root/shoot ratio (RSR, g root g-l shoot biomass). All surviving seedlings were harvested from 3 to 7 September 2001 following the same protocol. Branching of seedlings was not scored in 2001.

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Gas exchange and chlorophyll fluorescence The diurnal time course of in situ net photosynthesis of leaves was measured in selected plots on two days in 2000 and once in 200 1. Sky conditions on the three measurement days varied from partly cloudy to essentially cloudless. Diurnal net photosynthesis was measured on 8 and 9 August 2000 and 13 June 2001 in six plots along the gapunderstorey light gradient at 5 times across the day between 09:00 and 19:00 (ca 2-h intervals). The uppermost, fully developed, healthy leafwas measured on each of three seedlings of each species per plot in 2000 and on each of two to four seedlings of each species per plot in 200 1. The same leaf was measured at all times through the day, unless damaged underway, in which case a new healthy leaf next to the original leaf was chosen, and this was noted. Measurements were made using the ClRAS-1 portable photosynthesis system with the standard broadleaf cuvette. During measurements, CO 2 concentration in the cuvette was set to 365 ppm and air humidity at ca 80% of ambient conditions. No additional light sources were used. For all three measuring days, a rough estimate of the integrated daytime net photosynthesis (IDNP) (mmol m- 2 d- 1) was made for each seedling by integrating the area beneath the diurnal assimilation curve. Light-use efficiency (LUE) (J1rnol CO 2 J1mol photons- 1) was calculated as the instantaneous rate of photosynthesis divided by the irradiance measured by the cuvette light sensor at the time of measurement. Water-use efficiency (WUE) (J1mol CO 2 mol H 2O~ 1) was calculated as the instantaneous rate of carbon assimilation at a given rate of leaf transpiration. In addition to measuring the diurnal time course of photosynthesis, maximum rates of photosynthesis (Am) at saturating irradiance were estimated once in August 2000 and four times (21 June, 17 July, 31 July and 15 August) through the 2001 growing season. In 2000, A max was estimated on three seedlings of each species from one gap plot and one shade plot. Plants were taken into the laboratory and allowed to reach steady-state at a PPFD of 800 J1mol m- 2 S-l (this irradiance was found to be saturating even in seedlings adapted to the highest light conditions in preliminary light response measurements) and a CO 2 concentration of365 ppm. In 200 1, two to four seedlings per species were measured from eight plots along the gap-understorey light gradient. These measurements were made in a tent at the field site, with PPFD set at 2000 fJlTIol m- 2 S-1 and incoming CO 2 concentration set to 1500 ppm to limit effects of stomatal resistance. In 2000, seedlings were darkadapted before measurement. In 2001, seedlings were taken directly from their position in the gap and Amax was recorded after 5 min in the cuvette. This relatively short time to reach steady state in the cuvette was not considered a problem since seedlings were not dark-adapted before measurement and the limitation of A by cuvette CO 2 concentration was minimized. Effects ~f any stomatal responses were therefore minimal.

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The diurnal time course of maximum quantum yield was monitOred once in 2000 and three times in 2001. This was done by measuring the dark-adapted maximum quantum yield of chlorophyll fluorescence (FJF m) in situ at intervals through the day. Measurements were made at 2-3 h intervals through the day on 7 August 2000 (5 times per day) and 4 July (3 times per day), 11 July (3 times per day) and 20 August 2001 (4 times per day) using a pulse-amplitude modulated photosynthesis yield analyzer. Each leaf was allowed to dark-adapt for 30 min before measuring FJ F rn • The uppermost, fully developed, healthy leaf was measured on each of three seedlings per species in each measurement plot in 2000 and two to four seedlings per species in each measurement plot in 2001. The same leaf was measured at all times through the day, unless damaged underway, in which case the closest, fully developed, healthy leaf was used and the change in leaf was noted. Plants from 11 representative plots along the gap-understOrey light gradient were measured on each measuring date, except 4 July 2001, when plants from only 9 plots were measured.

Statistical analysis A general linear model (Proc GLM, SAS, ver. 8.2) was used to investigate the effects of average integrated daily Ip , species and their interaction on the response of growth and photosynthesis in ash and beech seedlings across the gap. The slope of the response to mean integrated daily I p was used as an expression of the ability of a particular trait to respond to the light gradient (plasticity) which the species was exposed to. Significant differences in regression slopes between ash and beech (seen as a significant interaction term) are therefore an indication of significant species differences in plasticity of that trait. All effects were considered significant when p S 0.05 (p-values > 0.05 and < 0.1 are noted as tendencies). Re-

sponse variables were transformed using the Box-Cox optimal power transformation to meet conditions of normality and homogeneity of variance, and outliers were removed from the data set where necessary (Weisberg 1985). The Box-Cox approach allows the estimation of a parameter, A, which then determines the function to be used for transformation: when A = 1, the data do not need transformation; Iv -1 calls for inverse transformation; A = 0 logarithmic transformation; and A = 0.5 square root transformation. All other values of A are simply applied as the power to the data. Results presented in Table 2 and 3 are transformed data. Table 1 and all figures show umransformed data.

Results Light in the gap A detailed description of the effects of the gap on light conditions in the 30 plots in 2000 and the 24 plots in 2001 is given in Ritter et al. (2005), and results are therefore only summarized here. Light conditions varied considerably within the gap and into the surrounding understorey. Integrated daily I p averaged over the same time period in 2000 and 2001 (14 June-13 September) showed that light was up to 18 times higher in those plots located within the gap and just north of the gap when compared with the darkest understorey plots (Fig. 1). Plots in the southern part of the gap received predominantly diffuse light, though sunflecks did occur on cloudless days (see Fig. 2 in Ritter et al. 2005). The diurnal time course ofI p was affected by position in the gap and the sky conditions on a given day. On overcast days, I p was highest just north of the gap center and declined towards the gap edges in all directions. On cloudless days. however, sunflecks and sun patches were predominant and areas exposed to high light shifted as the sun moved across the sky,

..."0 ~

Fig. 1. Average integrated daily II' (mol m- 2 d- 1) ror plots along two perpendicular transects through the center of a canopy gap in Suserup Skov in 2000 (.) and 2001 (D). Average integrated daily II' was calculated for the same period each year: 13 June14 September. Error bars represent ±1 SE and dashed vertical lines represent the approximate gap edges.

ECOLOGICAL BULLJ':rINS 52, 2007

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somewhat independent of position relative to the center of the gap. For example, between 8:00 and 10:00 on a sunny day in August 2000, the plot furthest north along the transect experienced the highest levels of II' as a result of a canopy gap outside the study area. Plots just east of the gap center and out along the eastern transect received higher light in the afternoon than any other time during the day. Understorey plots along the western transect did not receive the same exposure to oblique sunlight shining in from the gap early in the day as seen in eastern plots late in the day since the stem of the large, gap-creating beech tree shaded plots to the west of the gap. Near midsummer, when the sun was highest in the sky, plots just north of the gap center received ca 1.5 h of direct sunlight around midday under clear sky conditions (based on 21 June 2000).

Survival Survival at the end of the first growing season (2000) was > 90% for ash seedlings in all plots regardless oElight dose, except plot S22, where average integrated daily II' was < 0.5 mol m- 2 d,·l (Fig. 2, left). Beech seedlings, on the other hand, showed a decline in seedling survival by the end of the first growing season in plots receiving < 2.2 mol m-2 d-[ average integrated daily II" This included plots at the eastern, southern and western ends of the transects. Survival of ash seedlings was six times higher than that of beech seedlings in the darkest plot 12 m into the understorey from the southern gap edge (522) (only 11 % for beech compared to 67% for ash). By the end of the second growing season (2001), survival was severely reduced for both species at nearly all positions in the gap (Fig. 2, right). Survival of ash seedlings through to the end of the second growing season was :s; 50% in all plots, independent oElight dose. Ash showed only a weak correlation between survival and average inte-

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All growth and allocation variables measured in this study showed a significant effect of mean integrated daily II' in

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Fig. 2. Percent of potted ash (U) and beech (e) seedlings that survived to the end of the 2000 (left) and 2001 (right) growing seasons as a function of average integrated daily I p (mol m 1 d- 1) in and around the study gap. Regression lines (solid", ash, dashed '" beech) are added to illustrate data trends. Adjusted R2-values are 2000: ash", 0.40, beech", 0.64; and 200 1: ash", 0.18, beech '" 0.53.

152

Although the light response of the competitive height of ash seedlings was higher than that of beech seedlings in early July 2000, on average beech seedlings were 12 mm taller than ash seedlings by the end of the first growing season (Table 1). This could, however, be attributed to taIler beech seedlings in the most shaded plots, while in gap plots, ash seedlings tended to be taller. Beech seedlings were still taller than ash seedlings across the light gradient at the beginning of the second growing season, shortly after bud break and initial shoot extension. However, byearly July 200 1, ash seedlings accelerated height growth so that by the end of the second growing season, ash was taller than beech in all but 3 of the plots studied (data not shown). Ash seedlings were 45 mm taller than beech seedlings when averaged across the light gradient and 143 rnm taller in the lightest plot 4 m north of the gap center. Competitive height of beech was less dependent on ambient light conditions ofthe plot than ash seedlings over both growing seasons (Table 1). Regressions of competitive height against average integrated daily II' at each measurement time were never significant for beech, with a relatively small estimated slope, while competitive height of ash seedlings was significantly correlated to ambient light conditions at five of the six measurement times (see Table 1 for R2_ and p-values). The slope of the correlation between competitive height and light increased from the beginning to the end of the experiment for ash, indicating an increa..<;ing differentiation in height of ash seedlings from understorey shaded plots to high light plots in the gap with time.

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grated daily IT" suggesting that poor seedling survival was only to some extent an effect ofIow light (regression slope :::; 3.35, R2 :::; 0.18, p := 0.02). Beech seedlings showed a stronger correlation between seedling survival and light than ash (regression slope:::; 8.58, R 2 '" 0.53, P < 0.0001). Survival of beech seedlings was > 50% in the four most centrally located plots in the gap, namely N02, N04, E06 and 506 (average integrated daily II' = 6.79, 7.39, 5.70 and 4.23 mol m-2 d~l, respectively).

the first (2000) year of growth, with coefficients of determination (R2-values) above 0.6 (though not for leaf number, LAR, LWR and SLA in ash and lWR and SLA in beech; R 2-values not shown) and highly significant p-values in nearly all cases. Hence, irradiance measurably affected growth and allocation in both species across the gapunderstorey light gradient (significant light effect, Table 2; Fig. 3). In the second year of growth, the effects of irradi-

ECOLOGICAL HULLETINS 52, 2007

Table 1. Mean competitive heights (mm) and regression statistics of ash and beech seedlings on six different days throughout the study along the gap-understorey light gradient. Slope and R2 describe the relationship between competitive height and average integrated daily Ip (mol m-2 d- ' ). Significance of R2 noted in same column. p of paired Ttest gives the results of a simple paired T-test of differences between heights in ash and beech. (*) 0.05 < P < 0.1; *p < 0.05; **p < 0.01; ***p < 0.001; ****p < 0.0001. Ash

Beech

Date

slope

R2

mean

slope

R2

4Jul2000 10 Oct 2000 30 May 2001 5 Jul 2001 2 Aug 2001 30 Aug 2001

8.85 9.41 3.67 10.4 16.8 18.5

0.65 **** 0.63 **** 0.06 ns 0.24 * 0.29 * 0.28 *

89.3 87.5 126.6 170.2 219.0 232.6

0.960 0.327 4.15 6.42 7.94 6.89

0.00 0.00 0.07 0.19 0.20 0.21

ance on growth and allocation were generally less significant (Table 3; Fig. 3). For ash, seedling biomass (leaf, root and stem), stem diameter and leaf area still increased with increasing irradiance, while LAR, LWR and SLA decreased as irradiance increased. RSR was no longer affected by the level of irradiance. Despite smaller coefficients of determination (all < 0.6) for nearly all variables in ash and beech, the slopes ofresponse to integrated daily II' were steeper for most variables in 2001 than in 2000. The steeper slopes and lower R2 are indicative of a greater differentiation (intraspecific) between the most successful seedlings growing in plots with high light versus seedlings in the shade. There was a smaller range in II' across the gap in 2001 than in 2000 due to poor winter survival of seedlings growing in heavily shaded plots. This too may have played a role in the lower R2. In 2000, beech seedlings had 10% longer main stems, as well as significantly higher LAR, LWR and SLA and significantly lower RSR than ash seedlings (significant species effect). This provides evidence for beech seedlings investing in leaf area and leaf biomass during the first growing season regardless oflight conditions, while ash generally invested more heavily in belowground growth. In 2001, differences between the species in biomass accumulation and allocation were less significant due to a high withinspecies variation. Beech had 11 % lower LAR and a tendency towards lower total leaf area and leaf biomass than ash (0.05 < p < 0.1). There were no significant differences in total, root or stem biomass of ash or beech seedlings averaged for all plots in either 2000 or 200 1 (no significant species effects). The response of a number of growth and biomass allocation variables to average integrated daily II' across the gap was significantly different in the two species (significant light x species effect; Table 2 and 3). By the end of the 2000 growing season, ash seedlings had significantly higher plasticity of root biomass (regression slopes: ash == 0.135, beech == 0.097), which was reflected in total plant biomass (regression slopes: ash == 0.153, beech::: O. 122; Table 2; Fig. 3). The stronger response of root growth in ash seedlings

ECOLOGICAL HULLrTINS 52. l007

ns ns ns (*) (*) (*)

mean

Paired T-test p

83.7 99.5 155.8 177.4 183.2 187.4

0.085 <0.0001 0.003 0.63 0.004 0.003

also yielded a higher RSR than in beech seedlings in high light plots within the gap. Beech exhibited nearly double the plasticity of total leaf number by the end of2000 compared to ash. In 2001, LAR and SLA showed a significant1y stronger response to light in ash than beech (Table 3; Fig. 3).

Branching architecture All ash seedlings in all plots, regardless of location within or around the gap, were straight with no branching, indicating zero plasticity in this trait. Beech, on the other hand, showed more variation in crown shape and branching frequency across the light gradient of the gap (Fig. 4). Seedlings found in the most heavily shaded plots were predominantly unbranched. Seedlings growing in plots located within the gap were increasingly forked or broom-shaped.

Daily net photosynthesis Light conditions differed considerably between days on which the diurnal pattern of net photosynthesis was estimated (Fig. 5). The lowest light levels were seen on 8 August 2000 due to generally overcast sky conditions. Light levels were the highest on 9 August 2000 with a cloudless sky, particularly in plots north of the gap center, which received periods of direct sun during the course of the day. Finally, 13 June 2001 was intermediate, characterized by periods of both direct solar radiation and overcast conditions. On all three measuring days, ash and beech experienced similar light conditions during measurement (Fig. 5). Ash seedlings did not have consistently higher rates of mean net photosynthesis or integrated daytime net photosynthesis (IDNP) than beech seedlings on all three days (Fig. 5A~C and J-L). Although ash appeared to have higher rates of net photosynthesis over the day on 9 August at high PPFD (these were plots in the northern part of the gap characterized by longer sun patches), the other two

153

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Table 2. Plant growth and allocation in ash and beech seedlings at the end of the first (2000) growing season in response to the light gradient across a canopy gap in Suserup Skov. A gives the Box-Cox power transformation used to normalize the data. Least-squared means (95% confidence interval) and slopes are for transformed data. p-values for significant effects of light! species or their interaction are from the overall regression model (see text). (*) 0.05 < P < 0.1; *p < 0.05; **p < 0.01; ***p < 0.001; ****p < 0.0001 . Ash Variable

A

LS means

slope

Total biomass (g)

0.5

0.153

Leaf biomass (g)

0.5

Root biomass (g)

0.5

Stem biomass (g)

0.4

Stem diameter (mm)

0.7

0.845 (0.787:0.902) 0.336 (0.311 :0.361) 0.649 (0.603:0.694) 0.484 (0.454:0.514) 2.19 (2.09:2.29) 1.83 (1 .80: 1.85) 5.61 (5.14:6.07) 1.56 (1.50:1.61) 50.03 (44.0:58.1 ) 0.174 (0.161 :0.187) 1.75 (1.74: 1.77) 1.42 (1.34:1.50)

Length of main stem (mm) Total leaf area (cm 2 )

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Leaf number

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Beech LS means slope

light

p species

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0.122

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0.777 (0.719:0.835) 0.364 (0.339:0.389) 0.528 (0.483:0.574) 0.504 (0.474:0.534) 1.90 (1.80:2.00) 2.01 (1.98:2.03) 6.47 (6.00:6.94) 1.49 (1.44:1.54) 77.03 (70.0:84.1 ) 0.226 (0.212 :0.239) 1.79 (1.77:1.80) 0.84 (0.76:0.92)

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........ VI VI

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0

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0

Stem diameter (mm)

1

Length of main stem (mm)

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0

Leaf number

0

LAR (cm 2 leaf area g-1 total biomass)

0

LWR (g leaf biomass g-1 total biomass)

0

SLA (cm 2 leaf area g-1 leaf biomass)

1

RSR (g root biomass g-1 shoot biomass)

1

0.569 (0.455:0.682) 0.018 (~O. 11 5 :O. 151 ) 0.238 (0.136:0.341 ) -0.041 (-0.167:0.084) 5.72 (5.25:6.19) 165.9 (139:192) 2.42 (2.28:2.55) 0.922 (0.839:1.01 ) 1.82 (1.77:1.86) -0.586 (-0.619:-0.552) 250.2 (234:266) 0.941 (0.841 :1.04)

0.102 0.105 0.109 0.414 11.77 0.082 0.035 -0.036 -0.014 -15.3 0.011

Beech LS means slope

0.277 (0.146:0.408) -0.532 (-0.686:-0.379) -0.047 (-0.165:0.072) -0.158 (-0.303:-0.014) 4.21 (3.66:4.75) 205.3 (175:236) 1.92 (1.76:2.07) 1.18 (1.08:1.27) 1.64 (1.59: 1.69) -0.809 (-0.848:-0.771 ) 277.9 (259:296) 0.949 (0.833:1.06)

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Fig, 3. Variation in total seedling biomass, root biomass, root/shoot ratio (RSR), leaf area ratio (LAR) and specific leafarea (SLA) of ash (0) and beech (e) seedlings as a function of average integrated daily 11' (mol m- 2 d·· l ) in the forest canopy gap in Suserup Skov in 2000 (left column) and 2001 (right column). Data are untransformed. n ;:: 2-20, depending on plot. Note different axis scales.

measurement days did not show a consistent pattern to support this (Fig. SA-C), In general, seedlings of both species exhibited twice the LUE in plots south of the gap center on the cloudless day, plots where ambient light was predominantly diffuse, compared to plots north of the gap center which were exposed to direct light (Fig_ 5H), This effect was more pronounced in beech than in ash. Both species showed a steady decline in net photosynthesis and stomatal conductance (g) through the day in individual

156

plots (data not shown). The patterns of consistently higher WUE across the gap and more than twice the LUE in plots north of the gap center for ash compared to beech on the sunniest day were not seen on days with less direct sunlight (Fig, 5D-I) , WUE was, however, consistently higher in ash than in beech in well-illuminated plots north and east of the gap center on the other measurement days, IDNP f()r a given plot was significantly correlated to integrated daily If' for the particular day measured (p < 0,0001 for 8

ECOLOGICAL BULLETINS 52. 2007

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Fig. 4. Frequency of branching pattern (straight, bilaterally fi)tked, multilaterally forked or broom-shaped) in beech seedlings at the end of the first growing season (2000) as a function of average integrated daily I p (mol m- 2 d- I ). No branching was observed in ash seedlings, so they are not depicted graphically. The 12 seedlings per plot which were harvested in October 2000 were scored for branching pattern.

and 9 August 2000; p = 0.018 for 13 June 2001; data not shown). There were no significant differences between the species in mean IDNP for all plots or in the plasticity of IDNP across the gap. Steady-state A measured in the lab in 2000 was not significantly diffe;;nt for ash and beech from either the high (plot N04) or very low light plots (plot 522) (p > 0.05 in all pairwise comparisons) (Fig. 6, left). Both species showed more than twice the rates of maximum photosynthesis in seedlings occurring just north of the gap center compared to seedlings growing in the darkest plot (p < 0.003). In 2001, both species showed a significant response of A rnax to average integrated daily Ip (regression slopes: ash == 0.933, beech = 0.537; p = 0.005; Fig. 6, right). Although beech appears to have lower Amax across the gap, this difference was not statistically significant, nor was there any difference in plasticity of A"m;: between ash and beech (no significant interaction effect).

Chlorophyll fluorescence In all plots, beech had consistently lower FJF m than ash through the day (Fig. 7). This was also seen in deep shade (data not shown). Ifowever, the difference between ash and beech appeared to be more pronounced as ambient light increased, suggesting that there was a build-up of chronic photoinhibition in beech seedlings with increasing light availability in the plot. On days characterized by

ECOLOGICAL BULLETINS 52,2007

periods of high direct I p , both species showed a reduction in FjF m (dynamic photoinhibition) by 4-10%. This was seen on 7 August 2000 and 4 and 11 July 2001 after periods of high light (II' >1000 J.lmol m- 2 S-I). On some days, a slight recovery was seen in ash seedlings as light levels declined again towards the end of the day (Fig. 7A, C, G, H).

Survival In the present study, survival of both ash and beech seedlings in the gap was high at the end of the first growing season. However, despite considerably higher seed weight in beech compared to ash (Grime et at 1989), which should buffer against the stresses associated with establishment in deep shade (Grime 1979, We1ander and Ottosson 1998), beech seedlings did not appear better equipped for surviving on shaded sites than ash seedlings in the first season after germination. The high degree of shade tolerance of ash seedlings is in agreement with early studies which established this species as having very shade tolerant seedlings (Boysen Jensen 1929, Wardle 1961). Ash saplings have been found to survive up to 28 yr below the closed canopy, forming a large potential reserve for canopy replacement in the event of gap formation (Gardner 1975) By the end of the second growing season, both species showed a significant reduction in seedling survival. A weak correlation between survival and average integrated daily Ip in ash seedlings suggests that factors in addition to overall seedling carbon balance were affecting survival of this species in the understorey. Predator and parasite attacks on heavily shaded seedlings ofash have been suggested to play a role in the ability ofseedlings to survive the winter (Wardle 1961). Small non-structural carbohydrate reserves at the end of the growing season could also playa role in survival in shade plants (Canham et al. 1999). Chazdon (1992) noted that the tropical pioneer species, Piper sanctifelids, suffered higher rates of mortality due to herbivory and pathogens than its shade-adapted congener, E arieianum, on shaded sites and it was unable to survive long periods of suppression. Kitajima (I994) recorded higher frequencies of seedling mortality among species with high relative growth rates than species with low relative growth rates in shaded sites. She attributed survival of slow growing seedlings in part to greater allocation of resources to defense against herbivores and pathogens, for example through the establishment of dense, tough leaves. The present study excludes any effects of browsing by large herbivores such ~<; deer, which can have a profound effect on the balance between ash and beech seedlings since ash is much preferred over beech (M011er 1966, Modry- et al. 2004, though see Kullberg and Bergstrom 2001). Howev-

157

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Fig. 5. Leaf gas exchange of ash (0) and beech (e) seedlings as a function of photosynthetic photon flux density at the time of measurement in six plots along the gap-understorey light gradient in Suserup Skov. Measurements were made on 3 different days in the first and second growing seasons after gap formation: 8 August 2000, 9 August 2000 and 13 June 200 1. A-C: mean rate of net photosynthesis (A), D-F: water-use efficiency (WUE), G-I: instantaneous light-use efficiency (LUE) andJ-L: integrated daytime net photosynthesis (IDNP). Each point represents the mean of 5 measurements made at ca 2-h intervals through the day on 3 (2000) or 24 (2001) seedlings per plot.

er, a negative effect of insects, small herbivores and parasites on the survival rates of ash after the second growing season, more so in the shaded than in sunny plots, cannot be excluded. Whether higher allocation to defense in beech seedlings than in ash seedlings plays a role in the long-term survivability of beech in the understorey was not investigated in this study and therefore remains unclear.

158

Overallgrowth and biomass allocation The growth and allocational responses to average integrated daily Ip seen in both species by the end of the first growing season were generally those to be expected: increased overall biomass gain, increased allocation to roots and stems, decreased allocation to leaves (area and biomass) and a reduction in SLA (Abrams and Kubiske 1990, Madsen 1994, 1995, Abrams and Mostoller 1995, Grubb et al.

ECOLOGICAL BULLETINS 52, 2007

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1996, van Hees 1997, Welander and Ottosson 1997, 1998, Niinemets 1998, Beaudet and Messier 1998, DeLucia et al. 1998, Collet et a1. 2002, Reynolds and Frochot 2003). The allocation of assimilated resources between plant parts represents the balance of physiological supply and demand within the plant as a whole (Kuppers 1994) and the morphological adjustments seen here reflect the priority of root growth over shoot growth as light becomes less limiting for seedling growth and the demand for soil resources (nutrients and water) increases (Niinemets 1998 and references therein). The less significant effect of the light gradient on growth and allocation in ash seedlings at the end of the second growing season appeared due in part to greater intraspecific differentiation between individuals along the light gradient: ash seedlings seemed to separate into two distinct groups of stronger and weaker growers with no trees between these two groups. In contrast, the poor correlation to light in beech seedlings in 2001 was probably in part due to the minimal response to light seen in many growth and allocation variables across the light gradient (small slope). It is particularly striking that for beech, many of the allocation variables related to leaf area were not significantly affected by the light gradient by the second year harvest. A possible explanation for this may be that beech seedlings were no longer growing under comparable light conditions to those of ash, but instead in the shade of the ash canopy and the surrounding natural vegetation (Ritter et a1. 2005, Fig. 9). Thus, light measurements made using the spherical light sensors in each plot were not representative of light conditions experienced by beech seedlings by the end of the second growing season. A second explanation for insignificant correlations to light was the absence of very low light seedlings in 2001 due to poor survival in these plots.

ECOLOGICAl BULLETINS 52, 2007

Roots At the end of the first growing season, it is dear that ash seedlings have invested heavily in root grov,'th. RSR is significantly higher and LAR and LWR significantly lower in ash seedlings than in beech seedlings by October 2000. Other studies support the high allocation to root growth in young ash plants (Kerr and Cahalan 2004 and references (herein). Studies of seedling response to sudden increases in ambient light conditions with the removal of the upper canopy have established the importance of biomass allocation to roots and stems to quickly achieve a high RSR and the necessary conductivity to offset increased transpiration demands associated with increased light and leaf temperatures in a gap (Kneeshaw et al. 2002, Reynolds and Frochot 2003). These responses are essential before height growth can resume. While these studies relate to advanced regeneration, already established in the understorey prior to gap formation, they reveal nonetheless a strategy which is effective in the early stages of gap capture. The seedlings which are successful in capturing a gap are those which exhibit the most rapid establishment of a large root system to allow for rapid aboveground growth wilhout suffering from water or nutrient shortages as a result of insufficient root capacity. Species differ in their ability to show this response in biomass allocation. In a study of four North American tree species of varying shade tolerance, Canham et al. (1996) found that sugar maple Acer saccharum and red oak Quercus rubra had a relatively fixed allocation of total biomass to roots (regardless oflight and soil conditions) in the first year of seedling growth, while red maple Acer rubrum and white pine Pinus strobus clearly showed variation in allocation patterns in response to changes in soil conditions. These species differed in the plasticity of their root allocation response. The authors suggest that a lack of plasticity in some species may be the result of a balance between maximizing aboveground growth and minimizing the risk of mortality during droughts (Canham et al. 1996). A lack of response such as that seen in beech seedlings to increased light may be attributed to restricted allocation to root biomass, making plants incapable of keeping up with increased water and nutrient supply demand (Strauss-Debenedetti and Bazzaz 1991). The lack of response in root growth ofbeech to the light gradient in this study truly has consequences for its growth and dominance in the gap. By the end of the second year, however, the high allocation to roots in ash disappeared. Welander and Ottosson (1998) reported a similar ontogenetic shift in two-year-old pedunculate oak Quercus robur seedlings from growth favoring allocation to roots to growth favoring aboveground biomass. Total root biomass still tended to be higher in ash seedlings, but this was simply a result of total seedling size, not higher relative biomass allocation to roots in ash than in beech. Successful growth by ash into the canopy in a gap appears to be related to the early establishment ofan extensive root system, allowing this species to dominate below-

159

Fig. 7. Maximum quantum yield efficienc; (FjF J of ash (C) and beech (e) seedlings through the day in two representative plots in the gap (11 m north and 6 m south of gap center) on 7 August 2000 (A-B), 4 July 2001 (C-D), 11 July 2001 (E-F) and 20 August 2001 (G-H). Photosynthetic photon flux fluence rate (PPFFR) for each plot and day are indicated in the figures as well (note different y-axis scales between dates). Vertical drop lines are meant to aid in reading the time of each FiF m measurement. Error bars represent ± 1 SE. n = 3 (2000) or 2-4 (2001).

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ground competition for nutrients and water from an early stage and resulting in rapid aboveground growth in subsequent growing seasons regardless oElight and soil moisture levels encountered in the gap in the course of the day. This is despite the fact that moisture availability is expected to increase with the formation ofa gap relative to understorey conditions (Bauhus and Bartsch 1995, Gray et al. 2002, Ritter et al. 2005). However, NHcN concentrations in mineral soil have been found to be lower in the gap compared to the forest understorey during the growing season (Ritter and Bj0fnlund 2005), supporting the hypothesis that root growth is also affected by the need for increased nutrient uptake. It is possible that the disappearance of a light effect on RSR was an artifact of using potted plants in

160

this study. High nutrient availability in the pots in combination with the absence of belowground competition may cause seedlings to redirect investments to aboveground compartments. It would therefore be interesting to study the response of ash and beech seedlings to the light gradient while including the element of root competition (inter- and intraspecific).

Height growth versus crown expansion Rapid height growth precludes the formation of a broad, shade-adapted crown (Horn 1971). This hypothesis is based on the assumption that there is a finite amollnt of resources available to the plant and that there is a trade-off

ECOLOGICAL BULl.FTINS 52.2007

between height growth and crown expansion (King 1990, Kohyama and Hotta 1990). Therefore, a dichotomy exists in natural forest stands between those species which invest primarily in height growth in order to exploit better lit conditions higher up in the canopy and those species which expand the assimilation system to maximize light capture in the understorey (Kohyama 1987, Kohyama and Hotta 1990, Lei and Lechowicz 1990). Saplings with slender crown shapes or with large leaves and no branching until a considerable height is attained seem to have been selected for a regeneration niche in which they are successful in the early stages after gap formation (Kohyama 1987). The species studied here support this. Beech seedlings were on average taller than ash seedlings at the end of2000 and shortly after bud burst in 2001. However, beech seedlings did not markedly increase competitive height through the second growing season, while ash seedlings in the lightest plots exhibited explosive height growth. This may in part be due to the mode by which the two species grow. Beech seedlings show one (sometimes two) shoot elongation stages during the growing season, one after bud break in May and one around the beginning ofJuly if conditions are optimal (Moller and Staun 2001). Ash seedlings, on the other hand, appear to be less constrained in their pattern of shoot growth, exhibiting rhythmic growth through to July (Kerr and Cahalan 2004) or even August (unpub!. and Fig. 3) if growing conditions are good. This growth pattern in combination with an extensive root system established in the first year ofgrowth allowed ash seedlings to grow significantly taller than beech in high light plots by the end of the second growing season. The strong response of height growth in ash to the light gradient across the gap was seen as an increasing slope of competitive height versus average integrated daily I p with successive measurement dates. Thus, ash showed an increasingly differentiated competitive height in response to the gapunderstorey light gradient In agreement with the hypothesis that height growth comes at a cost to crown width, observations of the degree of branching exhibited by seedlings by the end of the first growing season suggest that already at the early seedling stage in a forest gap, ash has a strategy of rapid height growth while beech expands horizontally to maximize light capture in the shade. This was seen as branching of the leader shoot in > 50% of all beech seedlings in many plots in or near the gap, while no ash seedlings were branched. This pattern of increased branching with increasing light availability probably reflects the size of the seedlings: shaded seedlings were smaller, with fewer leaves, and therefore had not reached a size where branching of the crown became possible or necessary. Nonetheless, it is clear that while ash consistently grew in an upward direction, beech tended to grow horizontally. The monaxial habit of ash seedlings and saplings has been described before (Wardle 1961, Kerr and Cahalan 2004). The large compound leaves of ash, with their long petioles are

ECOIJ)GICAI. BUI.LETINS 52, 2007

thought to function as inexpensive branches, freeing the seedlings from investing in expensive woody branches (Givnish 1979). The broad crown exhibited by beech is thought to be representative of a shade tolerance strategy, while the upward growth of ash is consistent with a strategy of shade avoidance (Henry and Aarsen 1997). Beech is simply not capable of achieving such rapid height growth.

Photosynthesis Early successional species generally have higher photosynthetic capacities than late successional species (Bazzaz 1979, Bazzaz and Carlson 1982, Ktippers 1984a, Chazdon 1992). Gas exchange measurements made both in the field and in the lab did not, however, show significantly higher rates of photosynthesis in ash than in beech in this study. Both species showed a signifIcant increase in 1\,ax and IDNP in response to increasing light across the gap, but differences in overall growth of ash and beech could not be directly related to differences in rates of net photosynthesis and were therefore probably more correlated to the patterns of carbon allocation and seedling morphology discussed above. More variable Ip and a smaller range in light levels across the gap in the present study compared to the study by Einhorn et aL (2004) may be responsible for the apparent lack ofdifferences between the species in the present study. Different seed sources between this study and the study by Einhorn et al. (2004) may also have played a role. Finally, there may be too much noise in the gas exchange data obtained in this study, because measurements were made in the field and relatively few measurement days were successful. While field measurements of photosynthesis reflect the variable light conditions that dominate in and around the forest gap, it is nearly impossible to measure representative net photosynthesis under continuously changing light conditions. In addition to variable field conditions, net gas exchange measurements take time, limiting the number of samples compared for example to fluorescence measurements. Yet, leaf physiological parameters, such as photosynthetic and stomatal characteristics, have often failed to predict successional position and competitive ability of woody species growing under favorable conditions (Ktippers 1984a, b, 1985). Kiippers (1994) argues that branching patterns rather than leaf physiology ultimately determine the competitive roles of co-occurring species in nature. This in turn supports the arguments put forth earlier in this discussion.

Phenotypic plasticity of ash and beech seedlings in response to the light gradient In Suserup Skov, ash seedlings exhibited higher phenotypic plasticity in response to average integrated daily I p for all

161

growth and biomass allocation variables where there were significant differences between the species (except leaf number in year 2000). Together with the results ofVaHadares et a1. (2002), who found higher morphological plasticity in beech compared to oak, these results indicate the highest plasticity occurs in the mid-successional, gap-specialist (ash) followed by the shade tolerant species (beech), with the early successional species (oak) being least plastic in its morphology. This supports the findings of Abrams and Mostoller (1995), Naidu and DeLucia (1998) and Valladares et al. (2000) that mid-successional species may in fact be the most plastic. Measurements of A m3X in this study did not reveal significant differences in photosynthetic plasticity between the two species, however earlier studies showed significantly higher plasticity of maximum electron transport rate across 3 different light treatments in ash over beech (Einhorn et al. 2004). Gap species have been found to be more plastic in their allocation to roots or leaves than understorey species of the tropical rainforest shrub Psychotria (Valladares et a1. 2000). Although comparisons between tropical rainforest shrub species and temperate canopy tree species should be made with caution, patterns of allocation were also more plastic in ash seedlings across the gap in Suserup Skov. Valladares et al. (2000) argue that their results for Psychotria support the idea that genetic restrictions in morphological plasticity are greater in understorey species than in gap species. This suggests that limited plasticity of growth and allocation in beech may be attributed to an inability to respond due to genetic limitations. Alternatively, growth in beech may be too slow to respond to the increase in light before ash has gotten a head start. Chazdon (1992) suggests that simply by being fast-growing, a species will have a greater acclimation potential because it will be able to track and respond to the environment better. This implies that successional status is secondary to growth rate with regards to acclimation. Higher plasticity of height growth in response to ambient light conditions may therefore be restricted in beech by the fact that this species only has a few chances to respond to environmental conditions with shoot extension in a given growing season. There was, however, one morphological characteristic for which beech showed considerably more variation than ash, namely branching pattern. This variable was only measured at the end of the first growing season, but differences between the species were already apparent. Beech showed at least four different patterns of branching of the seedling crown, while ash showed no plasticity of response. While the degree of branching was to some extent an artifact of total plant biomass, it appears that beech is programmed to produce branches already early in seedling establishment. In a comparison of three North American maple species, one canopy species and two understorey species, Lei and Lechowicz (1990) point out that saplings of sugar maple Acer saccharum, a canopy species, are not truly shade-adapted, but merely capable of enduring

162

shade. Traits of sugar maple were clearly constrained by adaptations optimal to the adult tree, while the truly shade tolerant understorey species, striped maple A. pennsylvanicum, showed traits adapted to life in the understorey (Lei and Lechowicz 1990). This included a flat mosaic branching structure, with little overlap of leaves in order to maximize light capture. Although both ash and beech are canopy tree species, beech is adapted to a long existence as a sapling in the understorey and therefore establishes a flat mosaic architecture early in development. In order to maximize light interception per unit leaf area, plants in shaded habitats will minimize self-shading by reducing leaf overlap in the horizontal plane (Biisgen and Munch 1931, Horn 1971, Valladares 1999). Ash appears constrained to a more rigid canopy architecture under the light conditions in and around the gap, which coupled with faster growth help this species to reach the canopy first.

Effects on chlorophyll fluorescence - a role for

photoinhibition? Diurnal measurements ofmaximum quantum yield of ash and beech seedlings along the light gradient studied here showed that beech seedlings were experiencing mild chronic photoinhibition in the gap. Other studies have shown that beech seedlings can experience a build-up of photoinhibition under moderate light levels like those experienced in a small forest canopy gap (Tognetti et a1. 1997, Valladares et a1. 2002, Einhorn et a1. 2004). Valladares et al. (2002) recorded decreasing F)F m with increasing light exposure in beech, but not in oak and predawn FiF in beech was lower than oak under all but the lowest light conditions. Chronic photoinhibition has also been seen in the shade-tolerant tropical species Piper arieianum in high light areas of gaps and was associated with an inability to increase rates of photochemistry in high light (Chazdon 1992). The occurrence of chronic photoinhibition in beech seedlings has also been explained by a lower acclimation potential ofelectron transport rates in this species compared to ash (Einhorn et al. 2004). A closer look at the patterns of FJF m for ash and beech seedlings through the day suggest that although beech experienced chronic photoinhibition and ash did not, both species experienced some degree of dynamic photoinhibition through the day. This was seen a.o;; a decline in F)F rn through the day, followed by a recovery as light levels declined again towards sunset. In a previous study (Einhorn et al. 2004), ash and beech seedlings also experienced similar levels ofdynamic photoinhibition through the day, but a higher photosynthetic capacity (electron transport rates) in ash was seen to protect this species from chronic photoinhibition. In contrast, maximum rates of photosynthesis were not significantly different between the two study species along the light gradient in Suserup Skov. Since In

ECOLOGICAL BULLETINS 51, 1007

both species experienced a reversible build-up of photoinhibition during the day, the mild chronic photoinhibition seen in beech seedlings could be the result of slower repair of photodamage in beech than in ash (Mulkey and Pearcy 1992) or retention of protective pigments which are builtup in the light-harvesting antenna of beech leaves during periods of high light (Demmig-Adams et aI. 1998). It has been suggested that the relatively mild chronic photoinhibition seen in beech seedlings growing in the gap may in fact have an adaptive role, making up for the lower capacity for photochemical acclimation seen in this species (Einhorn et aI. 2004). The occurrence of photoinhibition in seedlings exposed to high light does not reduce total carbon gain enough to make these seedlings grow as poorly as they would in deep shade (Chazdon 1992, Einhorn et al. 2004). Shade-tolerant species may simply accept a certain level of photoinhibition when light availability is high because the benefits of high light with regard to net carbon assimilation are too good. This suggests that the degree of photoinhibition observed in beech seedlings in the gap in Suserup Skov is oflittle importance to the overall competitive balance between ash and beech.

Conclusions The purpose of this study was to investigate the morphological and physiological mechanisms behind the strategies for survival and growth of ash and beech seedlings along the natural light gradient in a forest canopy gap. Ash seedlings invested in root growth in the first year of growth, while beech seedlings prioritized the efficiency of leaf display (branching and leaf area), a typical shade tolerance response. In the second year, ash seedlings exhibited rapid height growth, which appeared only possible as a result of the establishment of an extensive root system in the first growing season. There were no significant differences in net photosynthesis rates between ash and beech seedlings in the gap, perhaps a consequence ofnoise in the data typical of such field studies. Yet it may be argued that factors such as crown morphology and biomass allocation have a much more central role in explaining the patterns of growth and survival seen in the early stages of gap capture by these twO species. Slower growth by beech seedlings results in the rapid over-shading by ash due to differences in biomass allocation and the direction of growth, resulting in lower light availability for beech in the understorey of ash in the initial phases of gap invasion. However, since beech quickly establishes a morphology which increases shade tolerance, beech is able to survive in the understorey despite early competition with ash. Acknowledgements - This study was made possible by grants from the Danish Agricultural and Veterinary Research Council (SJVF) and the Royal Veterinary and Agricultural Dniv. I wish to thank Som Akademi for permission to work in Suserup Skov, K. S0gaard Jensen and V Vranova for assistance in the field and B.

ECOLOGICAL BUllETINS 52, 2007

Skriver for technical support. Finally, thanks to J. W Leverenz, E. Rosenqvist, 1. Dalsgaard and E. Ritter for helpful discussions during the experimental and writing phases of this study.

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Kitao, M. et al. 2000. Susceptibility to photoinhibition of three deciduous broadleaf tree species with different successional traits raised under various light regimes. - Plant Cell Environ. 23: 81-89. Kneeshaw, D. D. et aI. 2002. Patterns of above- and belowground response of understorey conifer release 6 years after partial cutting. - Can. J. For. Res. 32: 255-265. Kohyama, T 1987. Significance of architecture and allometry of saplings. - Funct. Ecol. 1: 399-404. Kohyama, T. and Hotta, M. 1990. Significance of allometry in tropical saplings. -- Funct. Eco1. 4: 515-521. Krause, G. H. and Winter, K. 1996. Photoinhibition of photosynthesis in plants growing in natural tropical forest gaps. A chlorophyll fluorescence study. - Bot. Acta 109: 456-462. Kullberg, Y. and Bergstrom, R. 2001. Winter browsing by large herbivores on planted deciduous seedlings in southern Sweden. - Scand. J. For. Res. 16: 371-378. KUppers, M. 1984a. Carbon relations and competition between woody species in a c(~ntral European hedgerow. L Photosynthetic characteristics. - Oecologia 64: 332-343. Klippers, M. 1984b. Carbon relations and competition between woody species in a central European hedgerow. II. Stomatal responses, water use, and hydraulic conductivity in the root! leaf pathway. - Oecologia 64: 344-354. KUppers, M. 1985. Carbon relations and competition between woody species in a central European hedgerow. III. Carbon and water balance on the leaf level. - Oecologia 65: 94100. Klippers, M. 1994. Canopy gaps: competitive light interception and economic space filling - a matter of whole plant allocation. - In: Caldwell, M. M. and Pearcy, R. W (eds), Exploitation of environmental heterogeneity by plants: ecophysiological processes above- and belowground. Academic Press, pp. 1] 1-139. Leakey, A. D. B., Press, M. C. and Scholes, J. D. 2003. Hightemperature inhibition of photosynthesis is greater under sunflecks than uniform irradiance in a tropical rain forest tree seedling. - Plant Cell Environ. 26: 1681-1690. Lei, T T. and Lechowicz, M. J. 1990. Shade adaptation and shade tolerance in saplings of three Acer species from eastern North America. - Oecologia 84: 224-228. Lovelock, C E., Jebb, M. and Osmond, C B. 1994. Photoinhibition and recovery in tropical plant species: response to disturbance. - Oecologia 97: 297-307. Madsen, P. 1994. Growth and survival of Fagus ~ylvatica seedlings in relation to light intensity and soil water content. - Scand. ]. For. Res. 9: 316-322. Madsen, P. 1995. Effects of soil water content, fertilization, light, weed competition and seedbed type on natural regeneration of beech (Fagus sylvatica). - For. Ecol. Manage. 72: 25] -264. Modry, M., Hubeny, D. and Rejsek, K. 2004. Differential response of naturally regenerated European shade tolerant tree species to soil type and light availability. - For. Ecol. Manage. 188: 185-195. M011er, C M. 1966. Vore skovtr<earter og deres dyrkning. Dansk Skovforening, in Danish. M011er, P. F. and Staun, H. 2001. Danmarks tr<eer og buske. Politikens Forlag, in Danish. Mulkey, S. S. and Pearcy, R. .\X~ 1992. Interactions between acclimation and photoinhibition of photosynthesis of a tropical forest understorey herb, Alocasia macrorrhiza, during simulated canopy gap formation. - Funcr. Ecol. 6: 719--729.

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Naidu, S. 1. and DeLucia, E. H. 1997. Acclimation of shadedeveloped leaves on saplings exposed to late~season canopy gaps. -- Tree Physiol. 17: 367-376. Naidu, S. 1. and Delucia, E. H. 1998. Physiological and morphological acclimation of shade-grown tree seedlings to lateseason canopy gap formation. - Plant Eco!' 138: 27-40. Niinemets, O. 1998. Growth of young trees of Acer platanoides and Quercus robur along a gap-understorey continuum: interrelationships between allometry, biomass partitioning, nitrogen, and shade tolerance. -- Int. J. Plant Sci. 159: 318330. Pearcy, R. W. 1994. Photosynthetic responses to sunflecks and light gaps: mechanisms and constraints. - In: Baker, N. R. and Bowyer, J. R (eds), Photoinhibition of photosynthesis: from molecular mechanisms to the field. BIOS Scientific Publ., pp. 255-271. Peltier, A. et al. 1997. Establishment of Fagus sylvatica and hax"inus excelsior in an old-gtowth beech forest. - J. Veg. Sci. 8: 13-20. Reynolds, P. E. and Frochot, H. 2003. Photosynthetic acclimation of beech seedlings to full sunlight following a major windstorm event in France. - Ann. For. Sci. 60: 701-709. Ritter, E. and Bj0rnlund, 1. 2005. Nitrogen availability and nematode populations in soil and litter after gap formation in a semi-natural beech-dominated forest. Appl. Soil Ecol. 28: 175-189. Ritter, E., Dalsgaard, L. and Einhorn, K. S. 2005. light, temperature and soil moisture regimes following gap formation in a semi-natural beech-dominated forest in Denmark. - For. Ecol. Manage. 206: 15-33. Rust, S. and Savill, P. S. 2000. The root systems of Fraxinus excelsior and fagus sylvatica and their competitive relationships. Forestly 73: 499-508.

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Strauss-Debenedetti, S. and Bazzaz, F. A. 1991. Plasticity and acclimation to light in tropical moraceae of different successional positions. - Oecologia 87: 377-387. Tognetti, R., Johnson, J. D. and Michelozzi, M. 1997. Ecophysiological responses of Fagus sylvatica seedlings to changing light conditions. 1. Interactions between photosynthetic acclimation and photoinhibition during simulated canopy gap formation. Physiol. Plant. 101: 115-123. Valladares, F. 1999. Architecture, ecology and evolution of plant crowns. - In: Pugnaire, E I. and Valladares, F. 'eds), Handbook of functional plant ecology. Marcel Dekker, pp. 121-194. Valladares, F. et al. 2000. Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. - Ecology 81: 1925~-1936. Valladares, F. er al. 2002. The greater seedling high-light tolerance of Quercus robur over Fagus sylvatica is linked to a greater physiological plasticity. - Trees 16: 395-403. van Hees, A. F. M. 1997. Growth and morphology of pedunculate oak (Quercus robur L.) and beech (Fagus sylvatica L.) seedlings in relation to shading and drought. - Ann. Sci. For. 54: 9-18. Vejre, H. and Emborg, J. 1996. Interactions between vegetation and soil in a near-natural temperate deciduous forest. - For. Landscape Res. 1: 335-347. Wardle, P. 1961. Biological flora of the British Isles: F'raxinus excelsior 1. - J. Eco!' 49: 739-751. Weisberg, S. 1985. Applied linear regression, 2nd ed. - Wiley. Welander, N. T. and Ottosson, B. 1997. Influence ofphotosynthetic photon flux density on growth and transpiration in seedlings of Fagus syfvatica. - Tree Physiol. 17: 133-140. Welander, N. T. and Ottosson, B. 1998. Influence of shading on growth and morphology of Quercus robur L. and Fagus sylvatica L. - For. Ecol. Manage. 107: 117-126.

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Ecological Bulletins 52: 167-181,2007

Ground flora in Suserup Skov: characterized by forest continuity and natural gap dynamics or edge-effect and introduced species? Katrine Hahn and Rikke Pape Thomsen

Hahn, K. and Thomsen, R. P. 2007. Ground flora in Suserup Skov: characterized by forest continuity and natural gap dynamics or edge-effect and introduced species? Ecol. Bull. 52: 167-181.

The aim of this study is to describe the characteristics of the flora in Suserup Skov, Denmark, a small, ancient forest stand in a fragmented agricultural landscape. We ana~ lysed whether the ground flora is still characterised by forest continuity and natural gap dynamics or ifit is increasingly influenced by edge effect and introduced species. For the analyses we used a species list including all floristic recordings 1870-2005, presence/ absence data from two complete stand-scale surveys (50 x 50 m grid cells) collected in 1992 and 2002, floristic and environmental data from 163 randomly located lOX 10m plots collected in 2003, and floristic and environmental data from 91 plots each in and around five gaps collected 1999-2002. The flora list for Suserup Skov contains 182 herbaceous species of which 42 are regarded ancient forest indicators. A characteristic trait of the forest is the vast cover of spring~ephemeralsin often large and continuous patches. The effect of gaps was most evident for the summer flora, with both percent cover and species richness being higher in the gaps than under dosed canopy. The forest edge was only weakly influenced by disturbance-related species, and it appears that the closed structure of the forest edges make them relatively impermeable to invasion of competitive and exotic species. However, the presence of the lake as an edge and diverse habitat contributes positively to the overall species diversity of the forest. Only few introduced herbaceous species are of concern and are primarily located to three highly disturbed sites in the forest. However, their expansion may cause a substantial threat to native species. We conclude that the floristic composition of Suserup Skov - despite its smallness and isolated position ~ has a relatively high proportion of ancient forest indicators and large, continuous patches of especially spring-ephemerals. Moreover, even though the forest is quite small, the functional interior area of the forest is not much smaller than the actual area of the forest.

K Hahn (katrine.hahn@gmailcom), Forest and Landscape Denmark Univ. ofCopenhagen, RolighedlVej 23, DK-1958 Frederiksberg C, Denmark. - R. P Thomsen, /Egirsgade 70, st., DK-2200 K@benhavnN, Denmark.

Fragments of original forests with a continuous history of forest cover serve as important references for both species conservation and sustainable forest management. Managed forests often contain a higher number of species than unmanaged forests, but these are typically representatives

Copyrighr © ECOLOGICAL BULLETINS, 2007

of light-open and disturbed habitats (Skov and Svenning 2003, Zenner et al. 2006). Intensive management of forests often results in a decline in specific woodland species (L0jtnam and Wors0e 1993, Graae and Sunde 2000), and managed forests have lower ancient forest species richness

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than unmanaged forests (Petersen 1994, Peterken 1996, Lawesson et aL 1998, Verheyen et aI. 2003). Moreover, unmanaged forests have almost complete ground flora covers (Goebel et al. 1999) with larger mosaics of single-species patches (Peterken 1996, Vellend 2005). It is suggested that management schemes, which mimic natural disturbance dynamics, may be the most promising way to ensure longterm survival of the field layer flora in managed forests (Brunet and Oheimb 1998), partly because species composition and diversity is linked to the habitat diversity within the forest (Dzwonko and Loster 1988, Kolb and Diekmann 2004). In western Europe, where unmanaged forest reserves are often very small, the question of the influence on reserve size to the flora is of large importance. At present, we do not know much about minimum reserve sizes, i.e. are some forest reserves too small or dominated by an edge effect (Honnay et aL 2002, Harper et aI. 2005), so that introduced species establish and possibly outcompete the natural vegetation. Furthermore, the scientific knowledge on how the floristic composition in unmanaged forests relates to the spatial patterns and temporal dynamics is rather limited. In Denmark like in the rest oflowland NW Europe, the natural mixed-deciduous forest cover has decreased dramatically over the last 1000 yr, and most remnant forests, although with long continuity, have been altered severely with regard to species composition and stand structure. Only few unmanaged forest remnants are left as protected islands in a matrix ofintensively managed land. In terms of research on floristic patterns and processes in protected long-term forest reserves, Suserup Skov in eastern Denmark is of particular interest. The low human impact, the presence of a continuous forest cover in combination with a well-described forest structure, disturbance dynamics, and forest history (Heilmann-Clausen et al. 2007) makes Suserup Skov a desirable study object. The flora ofSuserup Skov has been subject to a range of floristic studies including single-species studies (Olesen and Knudsen 1993, Olesen 1994, 1996, Olesen and Ehlers 2001), stand-scale inventories (Holst and Holst 1993, Christensen et al.

1993, Wind 1999, Bigler et al. 2003, Holst and J0rgensen unpub!.), and comparisons with other undisturbed deciduous forests (Feilberg 1990, 1993, Graae and Heskj<er 1997). However, most studies are not comparable, many are not published in available journals, and only few have focused on the relationship between flora and forest structure and dynamics (Hahn 2000, Jelsbak 2003, Thomsen et al. 2005). The aim of the present study is to describe and analyse the overall characteristics of the flora of Suserup Skov, particularly focussing on: 1) the floristic composition and spatial distribution of the ground flora; 2) the role of gap dynamic processes creating a temporary niche for herbaceous species; 3) the effect of edges on the ground flora; 4) the status and distribution of introduced woody and herbaceous species.

Materials and methods Study area Suserup Skov is a mixed-deciduous forest reserve in eastern Denmark with long-term forest continuity and low human impact (Fritzb0ger and Emborg 1996, Hannon et aI. 2000, Heilmann-Clausen et aI. 2007). The forest is situated at the north-eastern shore of Lake Tystrup in the Susa valley system (55°22'N, 11°34'E). On the other sides, the forest is surrounded by wood pastures and (since 19961998) abandoned farmland. Emborg et al. (1996) divided the forest into four parts, A, B, C, and D based on forest structure and former use. Part A (10.4 ha) is high forest dominated by beech Fagus sylvatica and ash Fraxinus excelsior, part B (4.9 ha) is dominated by large, old oaks Quercus roburwith indications of former grazing, part C (3.9 ha) is an alder swamp Alnus glutinosa along the lake shore, and part D is a small site (0.5 ha) in the SE part of the forest, close to the lakeshore, characterised by remnants of an abandoned house lot and related semi-open areas (Fig. 1). In contrast to the original division (Emborg et aL 1996) we

Fig. 1. Most of Suserup Skov is dosed high forest, but a small area (Part D, see Fig. 2) close to the lake was earlier kept in open condition as a result of human activities around the now gone foresters' house "Sarauwsminde" (burned down in 1968). The photo (ca 1920) is taken from the lakeshore as indicated on Fig. 2. Printed with permission from Kongskilde Friluftsgard.

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ECOLOGICAL BULLETINS 52, 2007

expanded part 0 and reduced part C by one 50 X 50 m plot due to the clear human impact on the species composition here (Fig. 1). An abandoned freshwater field research station is located in the south-western corner of the forest, but only little disturbance of the surrounding forest is observed here (unpubl.). Suserup Skov is characterised by a high standing volume (722 m 3 ha- l ) (Emborg et al. 1996), and a high volume of dead wood (162 m3 ha- I ) (Christensen et al. 2005). The disturbance regime is dominated by small-scale disturbances with occasional large-scale windthrows, contributing to the small-scale mosaic structure with a high number of small gaps and few very large gaps (Emborg et al. 2000, Bigler and Wolf 2007, Hahn et aL 2007).

Sanlpling methods and data analyses As a baseline, a species list was collated, including all published and available unpublished surveys and voucher specimens from 1870 to 2005 totalling 15 independent surveys and reports with the majority of full-scale surveys 1992-2003. A critical examination of the surveys resulted in an exclusion of 69 species, which had all been 1) observed by only one author and 2) were clearly observed outside the forest boundary. The revised flora list contains 240 species, which were grouped into "herbs", "trees and shrubs", "introduced species", and species which have not been re-observed since 1915 ("pre-1915") (Table 1).

For the mapping of spatial patterns and indicators of forest continuity we included all red-listed species (Anon. 2004) and ancient forest indicators (sensu Wulf 1997, Lawesson et al. 1998) from the flora list. This information was combined with two stand-scale surveys covering the whole forest, which were conducted in summer 1992 and spring/summer 2002 by recordings ofpresence/absence in 50 X 50 m grid cells (see Christensen et aI. 1993, Bigler et al. 2003 for details). Analyses of spatial distribution of those species indicating forest continuity were carried out using maps with presence/absence for each 50 X 50 m grid cell. In addition we used data from a total of 163 square plots, each 100 m 2 , which were either placed by random (134 plots) or stratified random sampling (29 plots), collected in April-May andJuly~August 2003. The 134 random plot-coordinates were generated and placed in the forest by use of the permanent 50 X 50 m grid established by Christensen et al. (1993). Plots were excluded if they extended beyond the forest border. The additional 29 plots were placed in gaps in part A as indicated on the map of forest development phases 2002 (Bigler et al. 2003) (Fig. 2). Also 28 explanatory variables relatcd to overstorey (10), broad-scale spatial trcnds (9), topography and soil (5) and anthropogenic disturbance (4) were subjected to the analysis (Table 2a). A canonical correspondence analysis (CCA) was used to relate floristic variation at ground floor to explanatory variables and assign amount of explained variation to these different factors. Partial CCA (pCCA) was used to partition the total explained floristic variation

1\ Fig. 1 I 0

\ 50

I

100 m

Fig. 2. Suserup Skov with indication of the 50 x 50 m grid net, the lOx 10m randomly located plots, and the small grid plots within and around the five gaps. The division of the forest into four parts (A, B, C, and D) is also shown.

ECOLOCICAL BULLETINS 52, 2007

169

........ '--J

o

Table 1. Flora list from Suserup Skov grouped into Ilherbs" and Iitrees and shrubs". All species classified as lIintroduced'l are grouped separately and all species not reregistered after 1915 are also grouped separately. Red-listed species are marked with (R)I and ancient forest indicators are marked with asterisks (*). Herbs

I Achiflaea

tTl

8r oCl

Q r o;l

F r;; J

~

~

N N

o

~

mil/efolium Actaea "pieata i Adoxa moschatellina* Agrimona eupatoria' Agrostis tenuis Aiuga replans Alliaria peliolata Allium oleraceum Allium scorodoprasum* Anemone hepatica * Anemone nemorosa Anemone nem. x ran. Anemone ranunculoides* Angelica sylvestris Anthoxanlhurn odoratum Anthriscus sylvestris Arclium nemorosum ssp. nem. Arrhenatherum elatius Arum dlpinurn ssp. danieurn* Athyrium filix-remina Bellis perennis Braehypodium sylvaticum* Bromus benekeni Bromus ramosus Caltha palustris Calystegia sepium Campanula trachelium* Cardamine amara Cardamine pratensis ssp. pra. Carex acutHormis Carex elata Carc'x montana Carex pairaei Carex paffescens Carex panieulata Carex pilulifera Carex polyphylla Carex remota* Carex riparia Carex sylvatica* Carex vulpina

Cerastium fontanum ssp. triv. semidecandrum Chaerophyllum temu/entum I Chamanaerion angustifolium Chrysosplenium alternifolium* Circaea lutetiana* Cirsium arvense Cirsium oleraceum Cirsium palustre I Cirsium vulgare Corydalis bulbosa Corydalis intermedia* Crepis paludosa Cyperus fuscus Cystopteris rragilis Dactylis glomerata Dactylis polygama I Daucus carota ssp. carota i Deschampsia caespitosa Descharnpsia flexuosa Dryopteris carthusiana Dryopteris dilatata Dryopteris filix-mas* Eleocharis pa!ustris Epilobium hirsutum Epi/obium montanurn* Epi/ohium obscurum Epilobium parviflorum Epilobium roseum EpipacUs confusa (R) Equisetum arvense Equisetum ffuviatile Equisetum palustre Eupatorium eannabinum Festuca gigantea * Festuca pratensis Festuea rubra* Ficaria verna Filipendula u/maria Fragaria vesca* Cagea lutea * Cagea minima

I Cerastium

I Neottia nidus-a VIS' iR) spathacea' Calanthus nivalis Oxa/is acerosella i Caleopsis tetrahit/bifida i Paris quadrifolia* I Pha!aris arundinacea i Calium aparine Calium odoratum' Phragrnites australis Ceranium robertianum Plantago major ssp. major Ceum rivale Poa annua Ceum rivale x urbanum Poa nemoralis Ceum urbanum* Poa trivialis Polygonatum muftiflorum* Clechoma hederacea Clyceria maxima Primula elatior Hedera helix Primula veris * Hieracium piloseffa Pulmonaria obscura* Hordelymus europaeus I~anunclllus auricomus* Ranunculus rc!pens Humulus lupulus Hypericum perforatorum Roegneria canina Hypericum tetrapterum Rubus caesius Rubus fruticosus Impatiens noli-tangere'" ' Rubus idaeus Iris pseudaeorus Lactuca muralis Rumex hydrolapathum Lamiastrum galeobdo/ol1* Rumex sanguineus Lapsana communis Sanicula europaea * Leontodon autumnalis Scirpus sylvaticus !.istera ovata* (R) Scrophularia umbrosa I Serophularia nodosa* I Lolium perenne i Lonicera periclymenum i Scuteffaria galericulata Luzula multiflora Senecio jacohaea Luzula pi/osa Silene dioied Lycopus europaeus Solanum dulcamara Lysimachia nummularia* Sparganium erectum ssp. Lysimachia th yrsiflora Sta ch ys palustris Stachys sylvaliea* Lysimachia vulgaris Lythrum salicaria Stellaria alsine Majanthemum biro/ia Stellaria holostea * Melica uniflora* Stellaria media Mentha aquatica Stellaria nemorum* Mereurialis perennis* Taraxacum sp. Milium effusum* Thalietrum fla vum ; Moehringia lrinervia Torilis japonica Trienta/is europaea I Monot,opa hypopity' Trifolium repens Myosotis palu5tris Tussi/ago farfara Myosytis sylvatica* I Cagea

l

Trees and shrubs Typha latifolia AceI' platanoides Urtica dioica Valerian a officinalis ssp. offi. Alnus glutinosa Valeriana officinalis ssp. repens Betula pendula Betula pubescens Veronica beccabunga Veronica catenata Carpinus betulus* Comus sanguinea Veronica chamaedrys Corylus a vellana Veronica montana Veronica of{icinalis Crataegus laevigatd Vicja cracea Crataegus monogyna Vicia sepium I Euonymus europaeus* Viola canina I Fagus sylvatica Frangu!a alnus Viola hirta Fraxinus excelsior Viola reichenbachiana* Malus sylveslris* Viola riviniana Prunus a vium* Prunus cerasifera Prunus spinosa Pre-1915 herbs Cephalanthera longifo/ia (R) Pyrus communis Quercus robur Oactylorhiza mandata s.l (R) Rhamnus cathartica Melampyrum nemorosum Ribes nigrum Melampyrum pratense* Ribes rubrum ssp. rubr. * Orchis maseula* (R) Primula vulgaris I Rosa can ina , Salix caprea Salix cinerea Introduced herbs Salix fragilis Aegopodium podagraria Allium ursinum* Salix viminalis Sambucus nigra Chelidonium majus Epilobium cilialum Sorbus aucuparia Tilia cordata Eranthis h yema/e Ulmus glabra Hordeum vulgare Viburnum opulus Impa tiens parvif/ora" Petasites hybridus Reynoutria japonica Introduced trees/shrubs Acer pseudoplatanus Sonchus asper Sonehus oleraceus Aesculus hippocastanum Amelanchier spicata UrUea urens Ribes uva-crispa Veronica tfMormis Veronica hederifolia ssp. hede. Tilia platyplyllos

Table 2a. List of explanatory variables included in the CCA analysis of 163 plots. Numbers of variables are indicated in parentheses. For further details on the variables see Thomsen et al. 2005. Variable

Category Overstorey related variables

Edaphic and topographic variables

Anthropogenic variables Spatial variables

RLI (1)

Canopy openness (2) Dominant overstorey species (4) Vertical forest structure (3) Soil pH (1) Heat index (1) Litter depth (1) Soil moisture (2) Site history (2) Edge effect (2) Terms of a cubic trend surface polynomial (X, Y, X2, y2, XV, X3 , y 3 , X2Y, XY2) (9)

Table 2b. Variance decomposition by CCA and pCCA of species distribution data from the 163 plotsinto 6 nonoverlapping fractions. Cp_O := pure overstorey-controlled component; Cp_t = pure topography and soil, Cp_a := pure anthropogenic and Cp_s = pure spatial. Cm_s ::::: mixed spatial variables; and Cm_ota mixed topography and soil, anthropogenic and overstorey related. Total inerti = 7.214; total variation explained by constraIned axes (TVE) := 2.449; % TVE explained by constrained axes = 2.449/7.214:= 34%. TV = total variance; TVE total variance explained. Fractions

Cp_o Cp_t Cp_a Cp_s Cm_s Cm_ota Residuals

Herbs (frequency) % of TV % TVE 6.6 7.1 4.1 8.6 5.6 2.0 66.0

19.4 20.8 12.0 25.4 16.4 6.0

(lYE) into six non-overlapping fractions (Borcard et al. 1992, 0k1and and Eilertsen 1994, 0k1and 2003), namely the pure overstorey-related (Cp_o), pure topography and soil (Cp_t), pure anthropogenic (Cp_a), pure spatial (Cp_s), mixed overstorey-related-topographic-soil-anthropogenic-spatial (Cm_o) and a mixed overstorey-topography-soil-anthropogenic (em_ota). The two m-fractions refer to variance exclusively shared by the variable classes. For the analyses ofgaps and their importance as temporary niches, we analysed data from a detailed study of the gap phase flora within and around five selected gaps. Within and around each of the five gaps (Gap 1-5), species presence, percent cover and light availability was recorded in 91 plots (size 0.3 m 2 ) in summer 1999, spring 2000, spring and summer 200 1, spring and summer 2002 (see Hahn 2000, Hahn et al. 2007 for details). The possible effect of gap formation and the associated increase in light availability on species richness and cover was analysed by use ofa general linear model, PROC GLM (SAS, ver. 8.2), where "Gap", "Year" and "Light" (two classes of relative light intensity: "<2% RLI" or "~2%RLI") were qualitative covariates. "Light" was based on measurements of the rela-

ECOLOGICAL BULLETINS 52, 2007

tive light intensity at 1 m height over the forest floor compared to open field conditions. RLI was measured in summers 1999 and 2001 as there wa.~ a significant difference in light conditions before and after the hurricane in December 1999 (see Hahn et al. 2007 for details). Species specifically associated to open gap conditions were defined as those, which exclusively occurred in plots with> 2% RLI, and which were observed two or more times in different plots in the period 1998--2002. The cut-off level of 2% used was based on previous gap studies in Suserup Skov showing that RLI was below 2% in all developmental phases of the forest cycle except in gaps (Emborg 1998, Hahn et al. 2007). Attributes of these species were analysed with regard to their dispersal mode (Grime et al. 1989) and indicator values (Ellenberg et al. 1992). A temporary fencing of Gap 5 during 2000-2003 prevented roe deer browsing within and around the gap. The effect of this fencing will be treated separately in the discussion of the effects of gap formation on flora. For the analyses of edge effect we used the dataset from the 163 random plots. One variable was created by measuring the distance from plot centres to the nearest forest edge (terrestrial edge in directions N, E, and W, lake shore

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in direction S) .This variable was log, transformed to reflect the typically sharp increase in edge effects near forest margins (Laurance et al. 1998). An indicator species analysis (PC-ORD ver. 4.10, McCune and Mefford (1999» was applied to find characteristic species related to two groups of the edge variable: 1) edge area (0-20 m from forest edge) and 2) interior of the forest (20 m from forest edge and inwards). The aim of this analysis was to identifY indicator species corresponding to the two groups (McCune and Grace 2002). The indicator value (IV) reflects both high abundance and frequency of a species. We divided species into two groups based on a cut-off value of 10 (Thomsen et a1. 2005). The status of introduced species and their spatial distribution was evaluated by selecting those species from the two stand-scale surveys, which were classified as either non-native to Denmark defined by the Danish Forest and Nature Agency (Anon. 2005) or as native to Denmark, but directly or indirectly introduced to Suserup Skov. The spatial distribution of a selected group of introduced species, namely those with a combination of high frequency (this study) and high concern (0. Hamann pers. comm.) was mapped using the information from the 50 X 50 m grid cells. An overview of the spatial distribution of all sample plots in Suserup Skov used for the analyses in this paper is given in Fig. 2. Ground flora was defined as all herbaceous species and shrubs sensu Hansen (1991). A few species were identified only to genus level e.g. Taraxacum species. The highly variable Rubus ftuticosus was considered a single species. Viola reichenbachiana, 1.<' canina, and 1.<' rivinianawere registered as Viola sp., Bromus benek(~nii and B. ramosus were registered as Bromus sp., and Dactylis glomerata and D. polygama were registered as Dactylis sp. Nomenclature follows Hansen (1991). Red list status follows L0jtnant and Wors0e (1993) and Anon. (2004).

Results Floristic composition and spatial patterns The flora list for Suserup Skov contains 182 herbaceous species, of which 42 are ancient forest indicators, and 32 tree and shrub species, ofwhich five are ancient forest indicators (Table 1). The forest has experienced a smalL but nonetheless significant loss of herbaceous species during the 20th century. A total of six species, all characteristic of semi-open deciduous forest conditions and three of them presently red-listed, have not been re-observed since 1915

(Cephalanthera longiftlia, Dactylorhiza maculata s.l., Orchis mascula) (Table 1). Three other red-listed species still occur in the forest (Epiptutis confUsa, Listera ovata, Neottia nidus-avis). A characteristic trait ofSuserup Skov is the vast cover of spring-ephemerals, primarily Anemone nemorosa, Anemone

172

ranunculoides, Corydalis bulbosa, Ficaria verna, Lamiastrum galeobdolon, and Mercurialis perennis (Fig. 3). Other, less-dominant species are Anemone hepatica, Galium odoratum, Pulmonaria obscura, and Viola sp., primarily found on the down-slope, calcareous soils towards the lake (Fig. 3). Patches are often large and continuous, i.e. for Anemone nemorosa and Corydalis bulbosa. In summer, the flora is much sparser. Ancient forest species occurred in all four parts of the forest, typically in patches ofvarious sizes (Fig. 4). Variation partitioning showed that the fraction of the floristic variation purely attributable to broad-scale spatial variables was 25.4% ofTVE. The mixed fraction involving spatial variables was 16.4%. Considering the pure variance fractions space and topography clearly had the strongest effects on the floristic variation at ground floor (Table 2b).

Gap dynamics and ground flora The percent cover of spring herbs (sum of all species recorded in spring) was significantly different between the five gaps (p 2% RLI) to 1.4 species m~2 in non-gap plots « 2% RLI). The model explained 9% of the variation in summer species richness (Table 4). The differences in spring and summer species richness per gap over years is further illustrated in Fig. 5. The majority of species occurred in both high and lowlight plots, but ten species were explicitly registered in plots with RLI over 2%. Most ofthese species were characterised as long-distance dispersed (e.g. Chamaenerion angustifOlium, Taraxacum sp., EuonJJmus europaeus), light and soil

ECOLOCICAL BULLETINS 52, 2007

Anemone hepatica

Galium odoratum

Anemone nemorosa

Pulmonaria obscura

Ficaria verna

Viola sp. ~------r-------,

Fig. 3. Spatial distribution ofdominam spring ephemerals in Suseup Skov in the 50 x 50 m grid net. Grey grid cells species, white grid cells := absence of the species.

nitrogen demanding (e.g. Poa annua, Rubus idaeus, Urtica dioica) and could be characterised as competitive or ruderal (Table 5).

:=

presence of the

reached a significant and high indicator value (IV ~ 10) for forest interior. An analysis excluding the lakeshore as a forest edge reduced the number of forest edge indicator species considerably; from 24 to 9, and removed all the indicator species growing in moisturized and fertile areas.

The effect of edges on ground flora A total of 24 species reached significantly high indicator values (IV) (IV ~ 10) relating to forest edge (Table 6). These species can be divided into three ecological groups: 1) species occurring in or tolerating disturbed environments, e.g. Epilobium montanum, Geum urbanum, Plantago major, Poa annua and Taraxacum sp., 2) species occurring throughout the forest, e.g. Carex sylvatica, Galium odoraturn, Horde~yrnus europaeus, Melica uniflora, and Viola sp., and 3) species growing in well moisturized and fertile areas such as Ajuga reptans, Epilobiurn hirsutum, and Impatiens noli-tangere. Only one species, Anemone nemorosa

ECOLOGICAL Bl..)LLETINS 52, 2007

The status of introduced species The flora list of Suserup Skov includes 14 herbaceous and 6 woody introduced species, of which two are classified as native species in Denmark, but likely introduced to the forest (Allium ursinum, TiNa platyphyllos), and one species for which the origin is debatable, but it is known to have established in the forest only recently (Acerpseudoplatanus) (Table 1). Of the 14 herbaceous introduced species, only a few have been observed more than once in recent time:

Aegopodium podagraria, Aesculus hippocastanurn, l:,ranthis

173

Arum alpinum ssp_ danicum

Paris quadrifolia

Circaea lutetiana

Primula veris

Stachys sylvatica

Melica uniflora

=----""""""_-r----------,

Fig. 4. Spatial distribution of selected ancient forest indicators in Suseup Skov in the 50 X 50 one or more ancient forest indicators, white grid cells absence of ancient forest indicators.

ill

grid net. Grey grid cells

=

presence of

hyemalis, Impatiens parviflora, Petasites hybridus, and Reynoutria japonica (syn. Fallopica japonica). The stand-scale

podagraria (12%), Allium ursinum (5%), Petasites hybridus (5%), and Eranthis hyemalis (2%). The introduced woody

recordings in 1992 and 2002 show that the herbaceous species mainly occur at three highly disturbed sites: 1) the area of the abandoned house lot, 2) the north-western entrance to the forest, and 3) the lake shore (Fig. 6, top). The most frequent species are Impatiens parviflora which was recorded in 20(% of the plots, followed by Aegopodium

species mainly occur in the south-eastern part of the forest (part B, C, and D) leaving part A less influenced by exotic species (Fig. 6, bottom). The most frequent species are Acer pseudoplatanus, which was recorded in 30% of alISO X 50 m plots, followed by Tilia pfatyphyllos (23%) and Aesculus hippocastanum (11 %).

174

ECOLOGICAL BULLETINS 52. 2007

Table 3. Linear regression models for the two data sets of spring flora and summer flora in five gaps. The model had percentage herbaceous cover as response variable and "Gap", "Light", and "Year" and their interactions as explanatory variables. For the spring data set only "Gap" was found to have a significant effect on herbaceous cover. The summer data set showed that both "Cap", "Light" and "Year" and their interactions significantly influenced the herbaceous cover. The rather low correlation coefficients (R2) are indicated for each model. Factor

DF

Sum of squares

Mean square

F-value

p

Spring n=776 R2 = 0.149

Gap Error

4 771

174765 99'1436

43691 1285

33.98

< 0.0001

Summer n= 1230 R2 = 0.224

Gap Light Year Gap x light Gap x year Year x light Error

4 1 2 4 7 2 1090

47228 15742 55978 6282 8530 8267 627429

11807 15742 27898 1571 1219 4134 576

20.51 27.35 48.62 2.73 2.12 7.18

<0.0001 <0.0001 <0.0001 0.0281 0.0393 0.0008

Discussion Indicators of forest continuity and spatial patterns The flora in Suserup Skov is characterised by dense patches of spring-ephemerals, particularly Anemone nemorosa, Anemone ranunculoides, and Corydalis bulbosa, a feature which is rarely found in managed forests (Peterken 1996, Vellend 2005). T'he patchiness of the vegetation was also observed by Olesen (1996)} who found that the Corydalis bulbosa patches consisted of thousands of individuals covering the forest floor and displayed a pronounced patchiness of varying densities. The behind-lying factors explaining the floristic variation at ground floor were mainly controlled by unknown broad-scale factors. Several factors contribute in explaining the spatial autocorrelation found in the species data. First, the species assemblage structure at surrounding localities, because of contagious biotic processes such as growth, reproduction, migration etc. (Legendre 1993). Second, the dispersal mode of many forest herbs by clonal growth and/ or limited seed dispersal (Valverde and Silvertown 1997, Svenning and Skov 2002, Miller et al. 2002) and recruitment (Brunet and Oheimb 1998, Bossuyt et al. 1999, Verheyen and Hermy 2001). Finally, the low level of anthropogenic disturbance and long forest continuity seen in Suserup Skov can be expected to create homogeneous, favourable environments, which can support the growth of continually expanding patches thereby showing autocorrelation on greater distances than in unfavourable environments. All of the above mentioned factors can contribute to the generation of a spatial structure of the ground-layer species (high degree of patchiness) found in an unmanaged forest such as Suserup Skov.

ECOLOGICAL BULLETINS 52,2007

Gap dynamics and ground flora Gap dynamics and specifically the gap phase might help contribute to the long-term survival of light-demanding herbaceous vegetation, which naturally occurs in forests (Emborg et al. 1996, Schutz 1998). Naturally, the gapphase is not a permanent stage, and gaps vary in time as well as space. This means that the flora in gaps will contain species not present elsewhere in the forest, and be less predictable in space than in time. Gap-specialising species have been described and categorised in various ways i.e. with regard to fruit-size (Kollmann 1997), nutrient and light demands (Grime et aI. 1989) and as spring- or summer herbs (Collins et al. 1985, Moore and Vankat 1986). The time from gap formation and the degree of disturbance needed for a specific gap flora to develop has been the topic of a very limited number of studies (Cook and Lyons 1983, Moore and Vankat 1986). This study showed that species diversity in summer was significantly higher in plots with RLI>2% than in plots with lower RLL whereas the RLI availability did not have any signifIcant effect on the species diversity ofthe spring flora. Also the herbaceous cover in summer responded significantly to gap formation with a higher cover in plots with RLI >2% than in plots with RLI :S:2%. In contrast, the herbaceous cover in spring was not affected by either RLI or the development over time since gap formation. These findings are in accordance with Moore and Vankat (I986) who found that 1) total herb cover increased with gap formation and decreased with canopy reestablishment, and 2) that herb species, which increased were spring/summer or summer species, whereas spring species were either unaffected by gaps or decreased. The non-permanent status of the gaps has impact on the species present in a gap, as they must either disperse from gap to gap or be adapted to the transient gap condi-

175

100 80 60 40 20

C1III .

o 1999 100 80 60 40 20

5i 4 3 2

Gap 1 summer - cover

2001

1998

2000

2001

1 -:

01 2002

Gap 2 spring - abundance

2

~ ; [IJ}I 1998

2002 5

Gap 3 summer - cover

2000

[1[1__ 2001

2001

2002

~L~ . c. ~-~ 1998

5 1 4 -;

Gap 4 summer - cover

2000

1998

2002 5

Gap 5 summer - cover

~

c=- . . ~.. 2000

3 2

1

o 1999

2001

2002

1999

2001

2002

Gap 3 summer - abundance

l 3j 4

~ lcI~[l. _c. 1999

51

2001

2

[]I

2001

2002

Gap 4 summer - abundance

1998

2000

~~ 2001

2002

JI

~u=I~CII-,

2002

Gap 5 spring - abundance

4

o

o

3

o1II.. 2001

2002

4.J,

1~

1999

2001

Gap 2 summer - abundance

2002

Gap 4 spring - abundance

3i 21

o

2001

5 4 3 2 1

5·1

Gap 3 spring - abundance

[}I 1999

2002

4

1999

100 80 60 40 20

~ lILIL--CII 4~

o 100 80 60 40 20

2-

3

2001

Gap 1 summer - abundance

3 I

5:

Gap 2 summer - cover

5J

4 ;

2002

o 100 80 60 40 20

Gap 1spring - abundance

1999 5 4 3

2001

2002

Gap 5 summer- abundance

2

1

o 1999

2001

2002

Fig. 5. Mean values ofground flora cover (0/0) (left column) and species abundance (centre and right column) for sample plots divided into the two groups; "gap" and "nongap" with regard to specific gaps, year of recording, and season ("spring" and "summer"). White= gap-plots, black = nongap-plots. There is no figure of ground flora cover for "spring" as there were no significant effects of "Light" or "Year" or their interactions for this group.

tions. Most of the species specifically inhabiting gaps (plots with RLI >2%) were characterised as light demanding and/or nitrophile and dispersed by either wind or animals. Thus, when an opening of the upper canopy in the forest interior occurs, wind-dispersed species easily establish in the gap, a phenomenon also evidenced in studies by

176

Mountford and Groome (2003) and Thomsen et aI. (2005). The main inflow most likely originates from the open land surrounding the forest Oelsbak 2003), e.g. Cirsiurn arlJcnse from the adjacent abandoned fields (unpubL). However, some of the individuals may also have originated from the soil seed bank, as seeds of Rubus idaeus, 'Etraxa-

ECOLOGICAL BULLETINS 52. 2007

Table 4. Linear regression model showing the significant effects of "Gap", "Light", and "Year" and their interactions on the species richness (n m-3 ) of spring and summer herbaceous layer in five gaps. The rather low correlation coefficients (R2 ) are indicated for each model. DF

Sum of squares

Mean square

F-value

p

Gap x Light Year x Gap Error

4 1 5 4 1013

124 46 72 104 4070

31 46 14 26

7.61 11.19 3.51 6.38

<0.0001 0.0009 0.0037 <0.0001

Gap Light Gap x Light Error

4 1 4 1110

123 9 23 1843

31 9 6

18.32 5.10 3.36

<0.0001 0.0241 0.0095

Factor Spring n:::: 1140

R2 = 0.166

Summer n= 1230

R2 = 0.084

Gap Year

cum sp. and Urtica dioica have all been found in the seed bank in Suserup Skov (Jelsbak 2003). Species which persist in stable populations in undisturbed areas of the forest; such as Carex sylvatica and (zntlea lutetiana gained higher frequencies and abundance beneath the openings in the upper canopy; success of Rubus idaeus and R. fructicosus was also evident beneath canopy openings (Thomsen 2004). It has formerly been shown that perennials increase in abundance by vegetative growth in gaps; also several species supplement the increased vegetative growth with sexual reproduction in disturbed areas with increased resources (Pitelka et al. 1980, Hughes and Fahey 1991). Browsing by roe deer Capreolus capreolus may significantly reduce the species richness and cover ofground flora in forests, especially Anemone nemorosa (Bille-Hansen and Riis-Nielsen 1997, Watkinson et al. 200 1). In Suserup Skov, where roe deer are present year round, browsing, not only on tree seedlings but also on herbs, especially roots and shoots of Anemone nemorosa in late wimer/early spring occur. Fencing, even for a few years time, increases the cover ofground flora, specifically Anemone nemorosa, positive-

ly (Bille-Hansen and Riis- Nielsen 1997) and we therefore suggest that the significantly higher species richness and percent cover in spring in Gap 5 compared to the other four gaps, can therefore partly be explained by the effect of fencing.

The effect of edges on ground flora Changes in microclimate reach far into the forest interior (Matlack 1994, Laurance et aL 1998, Harper et al. 2005). At high latitudes the microclimate at forest edges is strongly influenced by edge orientation (Chen et al. 1993, Matlack 1994). Lower recruitment rates for forest herbs (Tomimatsu and Ohara 2004) and increases of competitive and exotic species (Fraver 1994, Honnayet aI. 2002) have been observed at forest edges. In this study the forest edge was only weakly influenced by disturbance-related species. Moreover, strict forest species gained high frequencies and abundances near the edge, and no reduced abundance at forest edge from native forest interior species were detect-

Table 5. Species occurring exclusively in plots with> 2% RLI listed together with their frequency (% observations per gapt Ellenberg-values (light, soil nitrogen, soil moisture, and pH requirements sensu Ellenberg et al. 1992), dispersal modes (W = wind-dispersed, F :::: fleshy-fruited/bird-dispersed, A = ant-dispersed) and life strategies (C = competitor, I = intermediate,S = stress tolerant, R ruderal sensu Grime et a!' 1989). Species

Ajuga repens Chamaenerion angustifolium Oryopteris dilatata Euonymus europaeus Ficaria verna Poa annua Rubus idaeus Taraxacum sp. Urtica dioica Viola sp.

ECOLOGICAL BULLETINS 52,2007

Frequency (%)

Light

Soil nitrogen

Soil moisture

pH

4 '17 4 4

6 8 4

6 8 7

6 5 6

6

17

4 7 7 7

7 8 6 7 9 6

6 6

7

4 27 11 11 '17

4.5

5 6 4.5

,5

7

5.5

177

Table 6. Species with statistically significant indicator values (IV ~ 10) (in brackets) for the two groups; "edge including lakeshore" and "interior ll • The analyses included 163 plots. Levels of significance: p$O.OOl ***, p$O.Ol **, p$0.05*. The test of significance was assessed using Monte Carlo test based on 49999 permutations. Edge (0-20 m from forest edge)

Interior (> 20 m from forest edge)

Ceum urbanum (41 .8)*** Taraxacum sp. (29.1 )** Me/ica unifJora (26.6)*** Ca/ium odoratum (26.5)** I-Iorde/ymus europaeus (24.5)*** Epi/obium montanum (19.2)* Dacty/is sp. (1 6.5)* Viola sp. (16.0)** Viburnum opulus (15.8)** Ribes rubrum (14.6)*** Brachypodium sylvaticum (14.5)*** Carex remota (14.4)*** Plantago major (12.5)*** Bromus sp. (12.4)** Epilobium hirsutum (12.4)** Geranium robertianum (12.3)* Polygonum multiflorum (12.2)* Poa nemoralis (11.5)* Poa annua (11 .0)** Oeschampsia caespitosa (10.4)** Eupatorium cannabinum (10.4)** Rubus caesius (10.4)** Impatiens noli-tangere (10.3)* Ajuga reptans (10.1)*

Anemone nemorosa (54.4)*

ed, except for Anemone nemorosa. Despite the difficulty in separating the effects of a south-facing forest edge and the lake-shore is seems reasonable to say that 1) the many species reaching significant but low indicator values at the forest edge are related to the presence of the lakeshore, and 2) the low amount of ruderal species in the edge-zone is probably linked to the absence of a dry and light-open southoriented forest edge. Further, we suggest that the position of the lakeshore reduces the changes in the microclimate otherwise characteristic for edges, due to higher air humidity and well-moisturized soils, thereby eliminating the conditions favourable for ruderal/open field species. Likewise, incoming seeds have to be carried over a long distances (wind or water dispersal) in order to establish on this side of the forest. Interestingly, the moist and fertile conditions along dle lakeshore make excellent conditions for many forest- and non-forest species, and the lakeshore-upland gradient and the presence of natural springs dose to the shore adds se\i'eral ecological niches to the otherwise upland-dominated forest. Thus, the species diversity in Suserup Skov would unquestionably be much lower without the lake. Finally, most of the forest edges are characterised by a quite closed structure making them relatively impermeable to invasion of competitive and exotic species (Cadenasso and Pickett 2001, Honnay et aI. 2002). Thus, the occurrence of light-demanding and ruderal species in the

178

forest interior of Suserup Skov is not due to a deep penetrating effect. Instead, long-distance transport of wind and animal dispersed seeds, which gain success in newly established gaps and along paths, plays a major role, as reported by Gill and Beardall (2001), Graae (2002), Mountford and Groome (2003).

o1 2

3 4

I IWmmliS

Fig. 6. Spatial distribution and number of anthropogenic/introduced herbaceous (top) and woody (bottom) species observed in Suserup Skov in the 50 x 50 m grid net.

ECOLOGICAl.. BULLETINS 52, 200?

The status of introduced species Most introduced species are observed in recent time only. Although this can be related to the more thorough inventories carried out in recent time, it is likely that most nonnative species, which typically are recorded post-1945 are linked to an increased anthropogenic disturbance. Examples are Aegopodium podagraria, Allium ursinum, and Petasites hybridus, (which spread from the abandoned house lot, Reynoutriajaponica, which possibly originates from deposit of garden debris), and Acer pseudoplatanus, which spreads from a mature tree near to a farm east of the forest. This explanation is supported by the obvious spatial patterns for the herbaceous species, showing a clear nucleus around the abandoned house lot, a small spot at the northwestern entrance to the forest, and in the light-open conditions along the lake-shore. The eastern distribution pattern of Acer pseudoplatanus in the forest corresponds well with the gradual spread west-wards from the single mother tree east of the forest. The question of the status of the present Tilia platyphyllos trees in Suserup Skov is not fully settled. Although the native origin has been supported (Lawesson 2004) the trees are most likely not ancestors of the original Tilia population, as pollen and macrofossil analysis show that both TiLia cordata and T. pla0lphyllosdisappeared from Suserup Skov over 2500 yr ago (Hannon et al. 2000). Moreover, the evidently concentrated occurrence of Tilia platyphyllos in part of the forest is an indication of a planting (Christensen et al. 1993). Although the results are not detailed enough to show the spatial effect ofinternal trails and paths on the distribution of non-native species, other studies document that the presence of a path generally results in an increase in the amount of ruderal species, disturbance indicators, and nitrogen-demanding species ('lyser and Worley 1992, Godefroid and Koedam 2004). Moreover, the expansion of introduced species may cause a decrease in the presence and cover of native species, as the introduced species take over the site and/or alter the site conditions. Such a concern has been expressed for the locally dominant Allium ursinum, which under Danish conditions is characterised as an indigenous but dispersal-aggressive species (Pedersen and Lange 1996). Other studies confirm that Allium ursinum can create a dense cover on favourable sites therebyexcluding most other herbaceous species, both other vernal herbaceous species and also species appearing later in the growing season Qandl et al. 1997).

Conclusion Despite its smallness and isolated position in an agricultural landscape Suserup Skov contains a high proportion of ancient forest indicators and a dense spring flora in large continuous patches, especially visible for the spring flora. This can be related to unknown broad scale t1.ctors such as

ECOLOGICAL BULLETINS 52, 2007

dispersal. The occurrence of wind-throw gaps contributed positively to the overall species diversity. The species abundance was significantly higher in gap plots than in non-gap plots and certain species were specifically related to the elevated light and/or nutrient conditions within the gaps. The effect was evident for species present in summer only. The study showed a rather small edge effect evidenced by few disturbance-related species reaching high indicator values at the forest edge whereas open-habitat and ruderal species were less frequent. The low number of ruderal species in the edge-zone can be explained by the absence of a south-oriented forest edge, the generally closed structure of the edges and the presence of the lake. The high species diversity and the occurrence of many non-forest but nonruderal species near the lake is probably caused by moist soils, and a high nutrient and light level rather than a traditional microc!imatic gradient along a forest edge. In conclusion, we suggest that even though the forest is quite small the functional interior area of the forest is not much smaller that the actual area of the forest. Most introduced species are linked to sites with past or present human activity, which has either on purpose or by accident introduced the species to the forest with dear nuclei around the abandoned house lot, the north-western entrance to the forest, and in the light-open conditions along the lake-shore. The most prominent species are Ae-

gopodium podagraria, Allium ursinum, Petasites hybridus, and Reynoutriajaponica. Although the present populations of introduced species are small, their expansion definitely causes a concern in a conservation perspective, as the introduced species can take over the site and/or alter the site conditions. Acknowledgements ~ The studies were financially supported by the Danish National Veterinary and Agricultural Research Council (Spy-Nat-Force), NatMan - Nature-based Management of beech in Europe (EO-grant no. QLKS-CT-1999-01349), and Renfors - Regeneration of Natural Forest Stands (EV-grant no. FAIR1-CT95-0420). We are grateful to the owner of Suserup forest, Som Akademi, for permission to undertake studies in the forest. We thank Peter Wind, Morten Christensen, Jacob Heilmann-Clausen, Jaris Bigler, and Anders Busse Nielsen for access to unpublished data and Bente Jessen Graae and Ole Hamann for valuable review comments.

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Bille-Hansen, J. and Riis-Nielsen, T. 1997. Skovarter i tilbagegang? Nyhedsbrev. Grrenser i landskabet. - The Danish Forest and Landscape Research Inst. 5: 6-10. Borcard, D., Legendre, P. and Drapeau, P. 1992. Partialling out the spatial component of ecological variation. - Ecology 73: 1045-1055. Bossuyt, B., Hermy, M. and Deckers, J. 1999. Migration of herbaceous plant species across ancient-recent forest ecotones in central Belgium. - J. Eco1. 87: 628-638. Brunet, J. and Oheimb, G. V. 1998. Migration ofvascular plants to secondary woodlands in southern Sweden. - J. Eco1. 86: 429-438. Cadenasso, M. L. and Pickett, S. T. A. 2001. Effect of edge structure on the flux of species into forest interiors. - Conserv. BioI. 15: 91-97. Chen, J., Franklin, J. F. and Spies, T. A. 1993. Contrasting microclimates among clearcut, edge, and interior of old-growth Douglas-fir forest. - Agricult. For. Meteoro1. 63: 2] 9-237. Christensen, M., Heilmann-Clausen, J. and Emborg, J. ]993. Suserup Skov 1992. Opmaling og srrukturanalyse af en dansk naturskov. Feltstationsrapport. - Milj0ministeriet, Skov- og Naturstyrelsen. Christensen, M. et al. 2005. Dead wood in European beech (Fagus sylvatica) forest reserves. - For. Ecol. Manage. 2] 0: 267282. Collins, B.S., Dunne, K P. and Pickett, S. T. A. 1985. Response of forest herbs to canopy gaps. - In: Pickett, S. T. A. and White, P. S. (eds), The ecology of natural disturbance and patch dynamics. Academic Press, pp. 218-234. Cook, R. E. and Lyons, E. E. 1983. The biology of Viola fimbriatufa in a natural disturbance. - Ecology 64: 654-660. Dzwonko, Z. and Loster, S. 1988. Species richness of small woodlands on the western Carpathian foothills. - Vegetatio 76: 15-27. Ellenberg, H. et al. 1992. Zeigelwerte von Pflanzen in Mitteleuropa. - Scripta Geobotanica 18, 2nd ed., Gottingen, Germany. Emborg, J. 1998. Understorey light conditions and regeneration with respect to the structural dynamics ofa near-natural temperate deciduous forest in Denmark. - For. Ecol. Manage. 106: 83-95. Emborg, J., Christensen, M. and Heilmann-Clausen, ]. 1996. The structure of Suserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Landscape Res. 1: 311333. Emborg, J., Christensen, M. and Heilmann-Clausen, J. 2000. The structural dynamics of Suserup Skov, a near-natural temperate deciduous forest in Denmark. - For. Ecol. Manage. 126: 173-189. Feilberg, J. 1990. Skov-vegetarionen i Tystrup-Bavelse omradet. Etablering og analyse af referenceomrader i Som Akademis Skovdisrrikter. - Biomedia for Skov- og Naturstyrelsen. Feilberg,]. 1993. Skovbundsvegetationen i Akademiskovene ved Som. - Flora Fauna 99: 22·-39. Fraver, S. 1994. Vegetation responses along edge-to-inrerior gra-

dients in the mixed hardwood forests of the Roanoke River Basin, North Carolina. - Conserv. BioI. 8: 822-832. Fritzb0ger, B. and Emborg, J. 1996. Landscape history of the deciduous forest Suserup Skov, before 1925. ~ For. Landscape Res. 1: 291-309.

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Gill, R. M. A. and Beardall, V. 2001. The impact of deer on woodlands: the effects of browsing and seed dispersal on vegetation structure and composition. - Forestry 74: 209~-218. Godefroid, S. and Koedam, N. 2004. The impact of forest paths upon adjacent vegetation: effects of the path surfacing material on the species composition and soil compaction. BioI. Conserv. 119: 405--419. Goebel, P. c., Hix, D. M. and Olivero, A. M. 1999. Seasonal ground-flora patterns and site factor relationships of secondgrowth and old-growth south-facing forest eeo-systems, southeastern Ohio, USA - Nat. Areas J. 91: 12~29. Graae, B. J. 2002. The role of epizoochorous seed dispersal of forest plant species in a fragmented landscape. - Seed Sci. Res. 12: 113--120. Graae, B.]. and Heskjrer, V S. 1997. A comparison of understory vegetation between untouched and managed deciduous forest in Denmark. - For. EcoI. Manage. 96: 111-123. Graae, B. J. and Sunde, P. 2000. The impact of forest continuity and management on forest floor vegetation evaluated by species traits. - Ecography 23: 720-731. Grime, ]. P., Hodgson, ]. G. and Hunt, R. 1989. Comparative plant ecology. A functional approach to common British species. - Unwin Hyman. Hahn, K 2000. Development of natural regeneration and flora in gaps in three deciduous forests in Denmark. - Master thesis, The Royal Veterinary and Agricultural Univ., Denmark. Hahn, K, Madsen, P. and Lindholt, S. 2007. Gap regeneration in four natural gaps in Suserup Skov - a mixed deciduous forest reserve in Denmark. - Ecol. Bull. 52: 133-145. Hannon, G., Bradshaw, R. and Emborg, J. 2000. 6000 years of forest dynamics in Suserup Skov, a seminatural Dan ish woodland. - Global Ecol. Biogeogr. 9: 101-114. Hansen, K. (ed.) 1991. Dansk feltflora. - Gyldendal. Harper, K A et aI. 2005. Edge influence on forest structure and composition in fragmented landscapes. - Conserv. BioI. 19: 768-782. Heilmann-Clausen,]. et al. 2007. The history and present conditions of Suserup Skov - a nemoral, deciduous forest reserve in a culturaIlandscape. -- Ecol. Bull. 52: 7-17. Holst, J. and Holst, 1" 1993. Artsliste for h0jere plamer og mosser i Suserup Skov. Kongskilde Friluftsgard. Hannay, 0., Verheyen, K and Hermy, M. 2002. Permeability of ancient forest edges for weedy species invasion. - For. Eco1. Manage. 161: 109-122. Hughes, ]. Wand Fahey, T J. 1991. Colonization dynamics of herbs and scrubs in a disturbed northern hardwood forest. ]. Ecol. 79: 605-116. Jand!, R., Kopeszki, H. and Glatzel, G. 1997. Effect of a dense Allium ursinum (L.) cover on nutrient dynamics and mesofauna of a Fagus sylvatica (L.) woodland. - Plant Soil 189: 245-255. ]elsbak, S. S. 2003. Driftens indflydelse pa fmbanken i skov - en analyse af fmbanken i Suserup Skov, N;esbyholmStorskov og Gulstav Vesterskov. -- Master thesis, Copenhagen Univ., Denmark. Kolb, A. and Diekmann, M. 2004. Effects of environment, habitat configuration and forest continuity on the distribution

of forest plant species. - ]. Veg. Sci. 15: 199-208. Kollmann, J. 1997. Hypotheses on the regeneration niche of fleshy-fruited species in natural gaps and edges in central Europe. - Verhandlungen der Geselischaft fur Okologie 27: 85-91.

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Laurance, W F. et a1. 1998. Rain forest fragmentation and the dynamics of Amazonian tree communities. - Ecology 79: 2023-2040. Lawesson, J. E. 2004. Ancient forests in Denmark and the importance of Tilia. - In Honnay, O. et al. (eds), Forest biodiversity: lessons from history for conservation. CABI Pub!., pp.97-115. Lawesson, J. E. et al. 1998. Species diversity and area-relationships in Danish beech forests. - For. Eea!' Manage. 106: 235-245. Legendre, P. 1993. Spatial autocorrelation - trouble or a new paradigm. - Ecology 74: 1659-1673. Lojtnant, B. and Worsoe, E. 1993. Status over den danske flora 1993. - GEC Gads Forlag. Matlack, G. R. 1994. Vegetation dynamics of the forest edge trends in space and successional time. - J. Eco1. 82: 113-123. McCune, B. and Mefford, M. J. 1999. PC-ORO. Multivariate analysis of ecological data, ver. 4. - MjM Software design, Gleneden Beach, 0 R, USA. McCune, B. and Grace, J. B. 2002. Analysis of ecological communities. - MjM Software design, Gleneden Beach, OR, USA. Miller, T F., Mladenoff, D. J. and Clayton, M. K. 2002. Oldgrowth northern hardwood forests: spatial autocorrelation and patterns of understory vegetation. ~ Eco1. Monogr. 72: 48l~503.

Moore, M. R. and Vankat,]. L. 1986. Responses of the herb layer to the gap dynamics of a mature beech-maple forest. Am. MidI. Nat. 115: 336-347. Mountford, E. P and Groome, G. 2003. Changes in ground vegetation following severe storm-damage at Noar Hill Hanger Beechwood. - The NatMan project, Working report 16, . 0kland, R H. 2003. Partitioning the variation in a plot-by-species data matrix that is related to n sets of explanatory variables. - J. Veg. Sci. 14: 693-700. 0kJand, R. H. and Eilertsen, O. 1994. Canonical correspondence analysis with variation partitioning: some comments and an application. - ]. Veg. Sci. 5: 117-126. Olesen,]. M. 1994. A fatal growth-pattern and ways suspected of postponing death - corm dynamics in the perennial herb Corydalis cava. - Bot. J. Linn. Soc. 115: 95-113. Olesen,' J. M. 1996. From naivete to experience: bumblebee queens (Bombus terrestris) foraging on Corydalis cava (Fumariaceae). - J. Kansas Entomol. Soc. 69: 274-286. Olesen, J. M. and Knudsen,]. T. 1993. Scent profiles of flower colour morphs of Corydalis cava (Fumariaceae) in relation to foraging behaviour of bumblebee queens (Bombus terrestris). - Biochem. Syst. Ecol. 22: 231-237. Olesen,]. M. and Ehlers, B. K. 2001. Age determination of individuals of Corydalis species and other perennial herbs. Nord.]. Bot. 21: 187-193. Pedersen H. lEo and Lange C. 1996. Rams-log (Allium ursinum) - en indigen, spredningsaggresiv plante. - Urr 20: 46-51. Peterken, G. E 1996. Natural woodland. Ecology and conservation in northern temperate regions. - Cambridge Univ. Press.

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Petersen, P. M. 1994. Flora, vegetation, and soil in broadleaved ancient and planted woodland, and shrub on RoSl1xs, Denmark. - Nord. J. Bot. 14: 693-709. Pitelka, L. E, Stanton, D. S. and Peckenham, M. O. 1980. Effects of light and density on resource allocation in a forest herb, Aster acuminatus (Compositae). - Am. J. Bot. 67: 942948. Schutz, ]. P. 1998. Licht bis auf den Waldboden: Waldbauliche Moglichkeiten zur Optimierung des Lichtenfalls im Walde. - Schweizerische Zeitschrift fur Forstwesen 149: 843-864. Skov, F. and Svenning, ] .-c. 2003. Predicting plant species richness in a managed forest. For. Eco!' Manage. 180: 583593. Svenning, ].-c. and Skov, F. 2002. Mesoscale distribution of understorey plants in temperate forest (Kalo, Denmark): the importance of environment and dispersal. - Plant £CoL 160: 169-185. Thomsen, R. P. 2004. The importance of the fl)rest overstorey as a control of understorey species composition in a nearnatural temperate forest, Denmark. "- M.Sc. thesis, Aarhus Univ. Thomsen, R. P., Svenning, ].-c. and Balsley, H. 2005. Overstorey control of understorey species composition in a near-natural temperate broadleaved forest in Denmark. - Plant Ecol. 181: 113-126. Tomimatsu, H. and Ohara, M. 2004. Edge etlects on recruitmen t of Trillium camschatcense in small forest fragments. Bio!' Conserv. 117: 509~ 519. Tyser, R. Wand Worley, C. A. 1992. Alien flora in grasslands adjacent to road and trail corridors in Glacier National Park, Montana (USA). - Conserv. BioI. 6: 253-262. Valverde, T. and Silvertown,]. 1997. Canopy closure rate and forest structure. - Ecology 5: 1555·-,1562. Vellend, M. 2005. Land-use history and plant performance in populations of Trillium grandiflorum. - BioI. Conserv. 124: 217-224. Verheyen, K. and Hermy, M. 2001. The relative importance of dispersal limitation of vascular plants in secondary forest succession in Muizen Forest, Belgium. - J. Eco!' 89: 829840. Verheyen, K. et al. 2003. Herbaceous plant community structure of ancient and recent forests in two contrasting forest types.Basic App!. Ecol. 4: 537-546. Watkinson. A. R., Riding, A. E. and Cowie, N. R. 2001. A community and population perspective on the possible tole of grazing in determining the ground Hora of ancient woodlands. - Forestry 74: 231-239. Wind, P. 1999. Suserup 1998. - In: Laursen, K. (cd.), Overvagning affugle, sxler og planter 1998-99, med resultater fra feltstationerne. Danmarks Milj0unders0gelser, Faglig rapport fra DMU 304: 44-49. Wult: M. 1997. Plant species as indicators of ancient woodland in northwestern Germany. - J. Veg. Sci. 8: 635-642. Zenner, E. K. et al. 2006. Responses of ground flora to a gradient of harvest intensity in the Missouri Ozarks. - For. Ecol. Manage. 222: 326-334.

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Ecological Bulletins 52: 183~194, 2007

Natural forest stand dynamics in time and space - synthesis of research in Suserup Skov, Denmark and perspectives for forest management Katrine Hahn, Jens Emborg, Lars Vesterdal, Soren Christensen, Richard H. W. Bradshaw, Karsten Raulund-Rasmussen and]. Bo Larsen

Hahn, K., Emborg, ]., Vesterdal, L., Christensen,S., Bradshaw, R. H. W, RaulundRasmussen, K. and Larsen, J. B. 2007. Natural forest stand dynamics in time and space - synthesis of research in Suserup Skov, Denmark and perspectives for forest management. - Eco!. Bull. 52: 183-194.

This paper synthesises results on short-term and long-term forest dynamics based on research during 1992--2002 in Suserup Skov - a semi-natural deciduous forest in Denmark. We evaluate stand-scale and gap-scale dynamics and discuss the possible implications of this research for sustainable forest management. The prominent long~term trend (millennia) is the loss of diversity of trees and shrubs during Iron Age settlements in the region, and the subsequent establishment of beech. A short-term trend (centuries) is mainly the retreat of oak, reflecting a change from open wood-pasture to closed stands. Most recently (decades) Dutch elm disease has reduced elm to a short-rotation sub-canopy species. Parallel to this, ash, lime (re-introduced), and maple (recently naturalised) have expanded. Monitoring of the 10 yr structural dynamics suggests that the initial forest cycle model was too simplistic because it did not incorporate the processes of crown expansion and canopy replacement. A strong storm in 1999 accelerated already ongoing processes: changes in diameter distribution, species composition, developmental phases, and dead wood accumulation, but the forest ecosystem also showed high stability, especially in terms of resilience. Detailed studies of gaps showed a temporal increase in light, soil moisture, and nutrient availability as well as a shift in soil microfauna, followed by a strong regeneration response of plants as well as soil biota within two years. Fencing excluded deer browsing. One of the most surprising results of the gap study was that Suserup Skov did not support the general notion that natural forests with limited disturbance have dosed N-cydes. In Suserup Skov, leaching rates of ca 20 kg N ha- I ye l from the root zone were recorded under dosed canopy. The high stability of Suserup Skov in terms of resistance and resilience encourages development ofspecies- and structurally rich forest ecosystems within practical forestry. The observed shortcuts within the forest cycle can directly be an integrated part of practical forestry, especially in forests managed by continuous cover principles. The study provided a benchmark case for carbon (C) pools in semi~natural forests, and the high C pool in Suserup Skov suggests that there is a potential for additional C-storage in managed beech forests.

Copyright © ECOLOGICAL BULLETINS, 20m

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K Hahn ([email protected]) and j Emborg, Forest and Landscape Denmark, Univ. o/Copenhagen, Rolighedsvej 23, DK-1958 Frederiksberg C Denmark. - L. Vesterdal and K Raulund-Rasmussen, Forest and Landscape Denmark, Urdv. o/Copenhagen, HlfJrsholm Kongevej 11, DK-2970 HlfJrsholm, Denmark. - S. Christensen, Dept o/Biology, Univ. o/Copenhagen, 0ster Farimagsgade 2D, DK-1353 Copenhagen K, Denmark. - R. H. W Bradshaw, Dept ofGeography, Univ. ofLiverpool, Liverpool L69 7ZT, UK - J B. Larsen, Forest and Landscape Denmark, Univ. o/Copenhagen, Rolighedsvej 23, DK-1958 Frederiksberg C Denmark.

The combination ofa thousand year history ofcontinuous forest cover with a century of strict protection makes the forest ecosystem ofSuserup Skov a unique outdoor laboratory. This large-scale research laboratory functions as a relevant reference for the general understanding of forest ecology and more specific questions related to sustainable forest management. In 1992, a full-scale inventory of forest structure with mapping of developmental phases was initiated. Besides unravelling the forest dynamics the aim was to place these dynamics in a long-term palaeoecological perspective (Hannon et al. 2000). The study was partly inspired by the early, classical studies of "virgin" forest structures in central and eastern Europe (e.g. Leibundgut 1982, Korpel1995). An outcome of the study was a basic model of forest dynamics in Suserup Skov (Emborg et al. 1996, 2000). Research integrating ecosystem processes and studies of forest structure dynamics was initiated in 1999. This research was inspired by ecosystem studies in temperate forests, e.g. Hubbard Brook and Harvard Forest, USA, which have set high standards for long-term, large-scale ecological research in deciduous forests. The full-scale inventory was repeated in 2002 for comparison with the 1992-inventory (Emborg and Heilmann-Clausen 2007, Christensen et al. 2007). Detailed studies on nutrients, hydrology and ecophysiology in an instrumented gap (Ritter et a1. 2005, Dalsgaard 2007, Einhorn 2007) were combined with analyses of regeneration and growth of dominant tree species (Emborg 2007, Hahn et al. 2007), dead wood and carbon pools (Bigler and Wolf 2007, Vesterdal and Christensen 2007), and biodiversity offungi, soil nematodes, and the vascular flora (Heilmann-Clausen and Christensen 2003, Bj0rnlund and Christensen 2005, Thomsen et al. 2005, Bj0rnlund and Lekfeldt 2007, Hahn and Thomsen 2007). The multi-disciplinary approach allows us to focus on interacting structures, processes, and disturbance agents, above- as well as below-ground. Finally, to establish a common basis Heilmann-Clausen et al. (2007) compiled the history and present conditions of Suserup Skov. In this paper we synthesise and discuss the outcomes of the research activities in Suserup Skov; those reported in this issue of Ecological Bulletins as well as many others. The aim is twofold. First, we expand the present understanding of stand and gap dynamics in time and space (Emborg et al. 2000) by illustrating the complexity of the forest ecosystem in gap phase (duration of ca

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25 yr), within the forest cycle (ca 300 yr) and in the longterm perspective (thousands of years). Second, we discuss the possible implications for forestry in order to achieve sustainable forest management.

Stand scale dynamics In Suserup Skov, short-term successional trends are based on direct observations and inferred from stand structure studies, and long-term successional trends are reconstructed from pollen and plant macrofossil analyses. The longterm trends and changes are considerable and often appear surprising or irrelevant to present-day ecologists, yet they place forested areas such as Suserup Skov in a valuable broader perspective in time and space. The history ofSuserup Skov during the last 6000 yr is rather typical of temperate, deciduous forest in western Europe and quite distinct from the boreal region and broadleaved forests of eastern Europe. The major long-term trend is the loss of diversity of trees and shrubs associated with Iron Age settlement in the region (Hannon et al. 2000, HeilmannClausen et al. 2007). Between ca 500 BC and AD 1000 Suserup Skov was transformed from a diverse, species-rich deciduous forest containing pine and abundant lime into the present relatively species-poor beech woodland (Photo 1). Periodic burning was a feature of the disturbance regime of the older forest. Studies elsewhere in Denmark strongly suggest that the changed nature of the forest was driven by cultural activities that have now ceased (Bradshaw et al. 2005). The present-day woodland is affected by various natural processes, but the species pool, at least for woody plants, has been severely reduced. The ground flora of Suserup Skov is - despite the small size and isolated location of the forest - characterised by a high number of ancient forest indicators and a vast cover ofspring ephemerals in often large and continuous patches (Photo 2). Moreover, the forest edge is only weakly influenced by disturbance-related species, and it appears that the closed structure of the forest edges make them relatively impermeable to invasion of competitive and exotic species (Hahn and Thomsen 2(07). Thus, even though the forest is quite small, the functional interior area of the forest is not much smaller than the actual area of the forest.

ECOLOGICAL BULLETINS 52.2007

Photo 1. Beech Fagus sy/vatica is a dominant tree species in Suserup Skov at present. The vegcracion hisrory of the forest over the last 6000 yr has been reconstructed by smdying pollen, macrofossils and charcoal from sedimenr cores sampled from a small, wet hollow in

the forest (centre of the picture). Photo: Jens Emborg.

One of che most obvious short-cerm trends is che distinct retreat ofoak from Suserup Skov. This reBects a landuse change from open wood-paseure to the present day forest characterized by closed stands and dynamics on che small seale (Embotg and Heilmann-Clausen 2007). The palaeoecological studies confirm this trend, suggesting that oak populations are returning CO more natural (lower) lev~ els. Because established oaks can be vety long-lived and persistent, at least some oak (rees will remain as a component in the forest for many years. However, it is likely that oak, in che long tetm, will disappear from che forest interior, unless dramatic changes in the disturbance regime tawards small-seale fire disturbance occur (Hannon et aI. 2000, Emborg and Heilmann-Clausen 2007). Dutch elm disease has been a distutbance agent, since it was first observed in Suserup Skov in 1994 (Emborg et aI. 1996). During the 10-yr period, a considerable number of large elm trees died, and several new canopy gaps were created where gtoups of 10-12 m tall elms had been killed (Christensen et aI. 2007). This has, however, been compensated by a plentiful tecruitment ofsmaller elms into che group of larget elms (Embotg and Heilmann-Clausen 2007). It is most likely chat che disease will continue but it is toO eatly to evaluate the full consequences of this relatively slowly developing distutbance of the system. It is

ECOLOGICAL BUumNS ~2. 2007

probable that Dutch elm disease causes a shift to shortrotation sub-<:anopy elms, because large and vigorous trees are most susceptible to che disease (Peterken and Mountford 1998), checeby maintaining che elm as an important component of the undetstorey for many decades (photo 3). While beech was the first species to benefit ftom the retreat of oak (Heilmann-Clausen et aI. 2007), analyses of the 2002 data show that ash, lime (te-introduced) and sycamore maple (recently naturalised) are dearly expanding. Their increased role represents a partial return co the species richness recorded in che pre-Iron Age forest and is a significant "naruralisation" trend. They will probably be more prominent in the future, especially in gaps C<eated by eithet storm or Dutch elm disease (Emborg and Heilmann-Clausen 2007, Hahn and Thomsen 2007, Hahn et aI.2007). A comparison of the inventories in 1992 and 2002 shows that the diametet distribution has shifred towatds a steeper negative exponential curve and (here is a general smooching across the larger diameter-classes (Emborg and Heilmann-Clausen 2007). This indicates a tendeney to stronger recruitment in the smaller diarneter-classes and is related to the loss of large trees in che I999-storm and a vigorous rectuitment of younget trees {Emborg and Heil-

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Photo 2. The spring Aora of Suserup Skov is

V3S[

and dense: and includes typical woodland species like wood anemone Anemone

nemorostJ, ydlow anemone Anemone ranunculoitks, and violets Viola sp. Pharo: Monen Christensen.

mann-Clausen 2007). The canopy scructure in Suserup Skov proves to be rather complex and variable. In comparison to the forest cycle model (Emborg et aI. 2000), detailed studies of forest structure in a I-ha plot in Suserup Skov revealed a weB-developed stratification into several structural canopy and sub-canopy layers. Forest structure is therefore more than the structure ofthe uppermost canopy layer. The well-developed, multilayered strucrure can be explained by 1) the presence of four co-occurring tree species wirh differenr regeneration strategies and life cycles, 2) the vertical stratification among beech trees due to competition in the aggradarion phases, 3) beech gradually taking over rhe canopy space from old, degenerating ash and oak trees, and 4) the presence of elm as an undersrorey species (Nielsen and Hahn 2007). The study by Emborg (1998) focused on the upper canopy layer. The detailed I-ha study of Nielsen and Hahn (2007) provides a supplemenrary and more detailed understanding of the canopy structure and its impacts on light availability at the forest floor. The study showed that the continuous cover of dense growing understorey layers across neighbouring structural units was

186

the main determinanr for lighr to the forest floor (Nielsen and Hahn 2007). This highlights rhe importance of paying as much attenrion to the density of sub-canopy layers as to the species and developmenral phase of the canopy in management schemes for natural regeneration of unevcnaged foresrs. The results based on the monitoring of 10 yr structural dynamics suggesr that rhe forest cycle model (Emborg er ai. 2000) (Fig. I, left) was too simplistic and lacked representation of several processes. Moreover, due to a multitude ofdifferenr dynamic processes, nearly halfof the total area changed phase during the 10 yr between inventories, which was more than three times the expected area (Chrisrensen er ai. 2007). This is amibured to four evenrs: Storm damage causing aggregate treefalls, Dutch elm disease resulting in sudden dieback, crown expansion of trees surrounding gaps, and understorey replacing the degraded canopy (Fig. I, centre) (Bigler and Wolf2007, Nielsen and Hahn 2007, Christensen et aI. 2007). In an atrempt to synthesize these complex patterns, [he changes can be grouped inro fWO major processes, I) "ser-back mecha-

ECOLOCICAL BULL..I::TINS )2. 2007

Photo 3. Elm Ulmus glnbra is presently an understorey Lree species in Suserup Skov. The umbrella-shaped branching and large leaves are characteristic traits, which together with the ability [0 re-sprour makes it a strong competitor for light whenever a canopy tree breaks down. Photo: Jens Embarg.

nisms" (e.g. caused by srorm harvesting in the oversrorey giving way to undersrorey trees, or Dutch elm disease) that cause a backward hin in developmental phase, and 2) "fust-forward mechanisms" (e.g. caused by lateral crown expansion, advance regeneration taking over, or storm creating a gap in e.g. eady biostatic phase) that cause a "phasejump" so that one or more developmental phases in the simple forest cycle are by-passed (Fig. I, tight). The classification ofchanges as either a forward or a backward phase jump is a matter of discussion, but the innovation phase is here defined as the starting point. The majority of the deviations from expectations occurred because the simple forest cycle model did not incorporate the processes of crown expansion and canopy replacement (Christensen et al. 2007). Thus, in practical terms, an improved understanding of the processes related to "horizontal" (crown expansion) and "vertical" (canopy replacement) changes in phases are therefore crucial for the development of small-scale, group-selection silviculrural systems. It should also be realised that stochastic events and disturbances certainly come into play in both shortand long-teem dynamics. arutal fluctuations in dead wood volume and its spatial diStribution can be rather substantial in the windy cli-

ECOLOGICAL BUUETINS 52. 2Wl

mate ofNW Europe (Christensen et al. 2005). Two independent post 1999-srorm SUlVeys estimated mean volumes of dead wood of71-168 m' ha- ' (Bigler and Wolf 2007. Vesterdal and Christensen 2007) with ca 10% as snags and 90% as logs (Phoro 4). Typical features of the storm wete the cascade effect, which caused high accumulation of dead wood in certain areas rather than a uniform disuibution, and the formation of pits and mounds (Biglet and Wolf 2007). Dead wood contributes ro the roral carbon (C) pool, and it was at first expected that dead wood would be an important contribution ro the overall C pool in SusetUP Skov. The roral C pool (tree biomass, dead wood, forest floor, and mineral soil) for userup Skov is 382 Mg ha- ' with 225 Mg C ha- ' in the woody biomass, 132 Mg C ha- ' in the mineral soil, 21 Mg C ha- ' in dead wood, and 4.5 Mg C ha- ' in the forest floor, i.e. only 6% of the rotal C pool is in dead wood (Vesterdal and Christensen 2007). Compared ro managed beech forests, the rotal C pool in Suserup Skov is substantial. The C pool of the biomass is much higher than the average estimate for Danish beech forests across age classes (77 Mg C ha- ' ), but the soil C pool is also high compared to that of similar Danish soil types (Vejre et al. 2003, Vesterdal and Christensen 2007). The high roral C pool can probably be attributed to long

187

J!Q ......."..

1992-research

I~'

2002-research

Synthesis

Set-back mechanisms: Storm + Dutch elm disease Fast-forward mechanisms: Crown expansion + Understorey take over rig. 1. The development ofthe forest cycle model from me first simple version (left) (Emborg er at. 2(00) over 3 more complex, derailed version (centre) (Christensen Ct at. 2007) to a new, combined synthesis (right).

term absence of harvesting resulting in boch a very high C pool in the living biomass and a relatively high content in the mineral soil. The high C pool in Suserup Skov as a representative of a semi-natural forest, suggestS that more carhon could be stored in managed forests by conversion from tradirional forest management systems based on clear-cutting and replanting to continuous cover foresuy with focus on maimenance of the dead wood component

(Vesterdal and Christensen 2007). In conclusion, most of the processes and structures that

characterize Suserup Skov at present - as opposed ro the low diversity ofwoody species - are natural and not results of human activities (Heilmann-Clausen et aI. 2007). The understanding of the patterns and processes in the forest has been improved by the insight in the dynamics at stand scale, and the studies provided an opportunity ro evaluate the existing forest models. The 1999-storm induced abrupt changes ro the userup Skov ecosystem and provid-

ed us with a unique chance co evaluate the resistance and response of the ecosystem ro such disrurbance. Although the overall standing volume of wood increased sligbtly in the 10-yr period, the forest was not unaffected by the storm. Together with the slower, but probably more longlasting effects of Dutch elm disease, the storm accelerated certain processes, which were already ongoing, e.g. chang-

es in diameter distribution, in species composition, in de· velopmental phases, and in dead wood accumulation.

Gap scale dynamics The degeneration and innovation phases are short periods in the forest cycle but nevertheless serve as the driver ofthe forest dynamics. Resource availability to plants changes dramatically following gap formation, but the question re-

188

mains how gap dynamics of natural temperate forests impacts nutrient cycles compared to large-scale disturbances in managed forests. The aim of the specific gap studies in Suserup Skov (Ritter et aI. 2005, Dalsgaard 2007, Einhorn 2007, Ritter 2007) was to quantify changes in resource availability and the relevant ecosystem processes following gap establishment. This would serve as a benchmark ca.,e

regarding the impact of innovacion phase dynamics within temperate beech-dominated forests. Gap formation initiated a substantial change in availability of resources, i.e. light, water, and nitrogen ( ). In four newly formed gaps in Suserup Skov, relative light intensity increased to 6.3% compared to 1.5% under the surrounding closed canopy (Hahn et aI. 2007). In a fenced, instrumented and intensively studied gap, the photOsynthetically active light had already decreased by 20% the second year after gap formation (Ritter et aI. 2005). In me absence of deer browsing, plants covered on average 21 % ofthe ground in the gap the year after gap formation increasing to 71 % in the third year (Ritter et al. 2005) (Photo 5). The water balance changed markedly following gap formation (Fig. 2a). Measurements during the first 20 months after gap fOrmation showed that throughfall precipitation was 15% higher in the gap than in the closed fOrest. As transpiration at the same time decreased, soil moisrure was consistently high through the year at 90% of water holding capacity (WHC) within the gap compared to only 63% of WHC in the surrounding fotest (Dalsgaard 2007). Water seepage from the roOt zone in the forest was therefore only 36% of water seepage in the gap area (Fig. 2a, Ri tter and Vesterdal 2006). As a result of these changes in physical conditions and plant cover, nittate leaching from 90 em depth was almost four times higher in the gap than in the surrounding forest 6--30 months after gap formation (Fig. 2b, Ritter

ECOlOGICAL BULLETINS 52. 2007

Photo 4. Large quamities of dead wood in all size classes and stages ofdecay are a characteristic feature ofSuserup Skov. Photo: Morten Christensen.

2007). Higher nitrare leaching in the gap occurred although the N input by throughfaU was reduced by > 50% in the gap compared ro the surrounding forest (Fig. 2b). The remarkable difference in leaching berween gap and forest had already disappeared by rhe third season afrer crearion of the gap. where nitrate leaching was comparable in gap and forese. Larer studies in Susecup Skov suggest thar rhe e1evared nitrate leaching in rhe gap did nor complerely disappear by the third year afrer gap establishment (Vesterdal unpub!.). Comparable gap srudies in managed temperate beech forests have also indicared that elevated nirrare leaching may last up ro 5 yr, depending on the development in plant cover (Bartsch 2000. Ritter and Vesterdal 2006). Studies in other Danish forest sites (Ritter and Vesterdal 2006) have suggested a relatively simple pattern regarding availability ofwater and N in and around gaps. In Suserup Skov it was therefore expected that the heterotrophic activity would limit N availability ro the vegetation. and would consequently be retained under closed canopy for-

ese. In contrast, a limired and short-term increase in heter-

ECOLOGICAL BULlETINS ~z. 2007

otrophic activity would lead ro loss of excess N from the gap as the demand by vegetation would be insufficient. The gap formation case study in Susecup Skov did confirm that resource availabiliry was increased. in terms of soil moisture, but there were no profound signs of increased availability resulting from stimulated heterotrophic activity. Studies of internal N cycling did not identifY gap-induced changes in rates of mineralization that could explain this marked and temporal increase in N leaching (Ritter 2007). Elevated N losses from the gap can therefore and inmainly be attributed ro decreased demand for creased water fluxes from the root wne afrer the death ofa tree. The gap study also emphasized the shorr-term nature of gap effects on resource availability and diversity of soil biota. With deer-prooffencing, regeneration is vety fust in Suserup compared ro many other forest sites. and disappearance of gap effects were also noted to be less fust in other beech forest gaps with slower developing regeneration (Ritter and Vesterdal 2006). The decomposer subsystem also reacted ro the change in physical environment within the gap. The observed

189

Phoro 5. Ash FmximtJ excelsior regenerated in high density within the fenced and instrumented gap. Asharp gradient of height growth towards the edges of the gap was observed. The board walk crossed through the g'J.p centre. Photo: Lars Vesterdal.

changes were markedly differenr in the soil compared to the aboveground litter. Ncmacodes, mainly consisting of microbivores, decrea.l;jcd in the soil within the gap compared co the surrounding forest soil during the first two years following creation of the gap. but this difference already diminished during the thitd yeat (Ritter and Bj0rnlund 2005). The ftaction of nemarodes being omnivorous or predacors increased within the gap during the first year after gap formation but this increase had already disappeared by the third yeat. Moteover. the reversal to the pregap situation within the gap predominantly occurred in the soil covered with colonizing ash trees compared [Q the surrounding bare soil (Ritter and Bj0fnlund 2005). These changes in the microhivorous fauna therefore indicate that the decomposer activity performed by microorganisms, and to a large extent fuelled by rhizodeposition ftom living plants, temporarily decreased in the gap. In contrast CO the situation in the soil environment, decomposition activity and nematOde numbers increased in litter under the gap compared to the surrounding forest. This is probably due to the increased moisture in the gap. Remarkably. the N cycle has genetally proved very open in Suserup Skov as indicated by leaching rates of ca 20 kg ha- I yrl from the root zone also under closed canopy (Fig. 2b). Leaching undet closed canopy occurs at a medi-

190

urn input of N by throughfalJ (24 kg ha- l yr'). which in many other Danish foreSt sites are not associated with N leaching. Moreover, N is lost by leaching in several phases of the forest cycle. i.e. the late biostatic phase. the degradacion phase and even the innovation phase where abundant regeneration would be a significant sink for N. One of the most surprising results of the gap study was that this protected forest ecosystem did not support the general notion that natural temperate forest ecosystems with limited disturbance per se are cllaracterized by a dosed N cycle (Schulze 2000). One possible explanation is that N removals by harvesting have been negligible over the last 200 yr due to the protected status ofSuserup Skov. This has led to accumulation of N within the ecosyStem ovet time (Wardle et aI. 2004) so that the system today may almost be in a steady state situation as demonstratcd by the telatively low C/N ratio of 11 in 0-20 em depth of the mineral soil (Ritter and Vesterdal 2006). As a consequence. even small N inputs by deposition trigger loss of excess N by leaching (Gundersen et al. 2006). We can by no means extrapolate these findings to other natural forest ecosystems, however, under thc specific site conditions of Suserup Skov (soil type. cumate and N deposition) it is conceivable thar a natural foresr with no exploitarion of biomass is susceptible to N losses by leaching.

ECOLOGICAl. BULlETINS 52. 2007

110 mm

303mm

20 kg N ha-1

75 kg N ha-1

Fig. 2. Annual fluxes of (a) water and (b) nitrogen (NO.1 N) fluxes in the gap centre and surrounding forest the period 6-30 months after gap formation (annual throughfall precipitation based on 20 months only). Water and N fluxes from Ritter (2004) and Dalsgaard (2007).

In conclusion, shoft lasting and parallel changes in the physical environment, plant cover, and in soil chemistry and biology as well as activity in the litter layer were observed during the first two years following establishment of the gap. These changes thereafter reversed to the pre-gap situation following the development of regeneration. The surprisingly rapid response of the soil biota to the gap formation is most likely related to the decrease in density of live tree roots in the soil. The remarkable resilience of the soil population returning to the pre-gap situation within very few years also opens the question to which extent these belowground organisms control the direction of the development of the aboveground vegetation filling the gap.

Perspectives on natural forest dynamics in time and space Within the forest cycle, the gap phase plays an important role as a dynamic motor and determinant of the successional trend of a given spot in the forest. On the contrary, the long-term development of Suserup Skov - e.g. change from a species-rich system to a more species-poor system, successional retreat ofoak, and increasing standing volume - is largely determined by external factors. Such factors include fast disturbances like storm and outbreaks of pests or slowly occurring disturbances like climate change, nitro-

ECOLOGICAL BUL.IHINS 52, 2007

gen deposition, or species migration. When combining the short-term and small-scale perspective (gap phase, ca 25 yr) with the intermediate scale (forest stand, ca 280 yr) and the long-term perspective at landscape scale it is possible to analyse how the factors and processes at each level interact with the others, altogether influencing the long-term development of the forest. Examples of interactions across levels in such a hierarchical concept (O'Neill et al. 1986) are 1) the effect ofthe 1999-storm, which at the stand level altered the structural composition of the stand towards a more natural state by eliminating the overrepresentation of old trees in the stand and thereby accelerating the process of regeneration of ash in many gaps, 2) the strong establishment of lime and sycamore maple in the stand due to human activities, which can be viewed as a reversing process toward the species richness of the forest in the past, 3) the competitive aspects of ash and beech establishment in gaps, which under altered climatic conditions may become even more favourable for ash (Saxe and Kerstiens 2005). As a contrast to these long-term changes in forest composition generation times for the soil fauna and soil microbes are much shorter than generation times for the trees. Therefore, changes in the soil biota and the biogeochemical processes it performs will not interact directly with the dynamic processes at the century scale but may be crucial for the processes in the short term such as the gap phase. It should be the aim of future research to unravel to what extent long-term forest deve1opmem: in a forest like

191

Suserup is governed by events in the gap phase, alternatively by external events. This forms part ofimportant up-scaling exercises in both space and time that assess how general are the conclusions reached from the detailed studies presented here. The dynamic vegetation model LPJ-GUESS combines a forest-stand simulator with a global biome model and many insights have been gained into processes that are important both at the stand-scale over short time periods and at regional scales over millennia (Smith et al. 2001). At present, climatic factors appear to be the main drivers of forest dynamics, but these can be considerably modified by anthropogenic disturbance at finer spatial scales (Cowling et al. 2001). The effects of climate are also modified by atmospheric CO 2 concentrations and local competitive interactions between species, the latter being the focus ofthe studies presented in this book. These competitive interactions are of vital importance in the development of silvicultural systems, but specific modelling of Suserup Skov is needed to explore their influence at broader spatial and temporal scales.

Perspectives for sustainable forest management Suserup Skov is one of the most important references for understanding the relationship between disturbances and structural and functional dynamics of mixed deciduous forest ecosystems in north-west Europe. This knowledge is crucial for development of forest management methods in accordance with nature-based principles, which may offer a means to achieve sustainable forest management (Gamborg and Larsen 2003, Larsen and Nielsen 2006). What then are the main lessons learned from Suserup Skov?

Disturbance and resilience The influence of larger disturbances on forest structure and the resilience of the ecosystem are highly interesting from a management perspective. In Suserup Skov major disturbances include forest fires (pre-historic), Dutch elm disease (present), and extreme storms (present) (Bigler and Wolf 2007, Emborg and Heilmann-Clausen 2007, Heilmann-Clausen et al. 2007). The role of fire as a means to maintain species richness in pre-historic time, and the promotion of the dominance of beech in the absence of fire during the last 1000 yr shows the potential of fire as a possible management tool to enhance species richness - even in mixed deciduous forest. Suserup Skov proved very robust in the 1999-storm and regenerated almost instantaneously, thereby maintaining the ecosystem, its processes and functions. The observed high stability of Suserup Skov in terms of resistance and especially resilience encourages de-

192

velopment of species and structurally rich forest ecosystems within practical forestry.

Structural dynamics The small-scale structure and dynamics related to the forest cycle can also be directly adapted to practical forestry, especially in relation to development of nature-based, small-scale selection systems. An interesting feature is the revision of the forest cycle (Christensen et al. 2007), which provides a rather complex picture with several short-cuts of the developmental processes in Suserup Skov. These shortcuts, which for example bypass the innovation phase and/ or omit the late biostatic and the degeneration phase, can directly be an integrated part of practical forestry, especially in forests managed by continuous cover principles. Another important finding is that continuous cover of dense sub-canopy layers across neighbouring structural units is the main control on light reaching the forest floor (Nielsen and Hahn 2007). This highlights the importance of paying equal attention to the density ofsub-canopy layers as to the species and development of the canopy in managing natural regeneration of uneven-aged forests.

Nutrient and water cycling The finding that a semi-natural forest ecosystem with little disturbance is not always characterized by a closed N cycle is surprising (Ritter 2007). It gives, however, more "degrees of freedom" for larger scale forest regeneration methods, at least with respect to biogeochemical stability. Within the gap, the high moisture retention during the growing season (Dalsgaard 2007) supports the importance oflight and water supply in gaps for successful regeneration. The large variation in ecological parameters emphasizes the importance of forest structures in creating and maintaining micro-niche variation for biodiversity conservation. Finally, a study of the C pools showed that the total C pool in Suserup Skov is substantially larger than in comparable managed beech forests (Vesterdal and Christensen 2007), suggesting a potential for additional C-storage as a result of changed management.

Regeneration Gap regeneration is often suggested as a key feature in close-to-nature forest management. The shifting mosaic regeneration pattern represents typical group-wise forest regeneration where beech is favoured. The well-recognized rush-strategy for ash and the stop-and-go strategy for beech often lead to group micro-succession from ash to beech in the climax stage (Photo 6). However, a more complex pattern with rush-beech and stop-and-go ash in

ECOLOGICAL BULLETINS 52, 2007

Photo 6. Within this newly formed gap, ash expressed strong height increment, while beech has established below the ash with a lower height increment. Behind the root plate of the fallen canopy beech, an underscoreyelm tree is expanding ics crown cover. Photo: Jens Emborg.

combination with a rather high shade tolerance of young ash trees can explain the co-existence of early- and latesuccession species in the climax forest (Emborg 2007). In order to maintain or promote more light demanding spe cies, e.g. oak, interventions on a larger scale (up to 2 ha) are required, as shown in the I999-storm. Finally, there is a good correlation berween gap Strucrute, light, and soil moisture (Einhorn 2007, Hahn et aI. 2007). bur the regeneration response to gap creation seems less predictable. This probably reflects the rather small gaps studied but it also pinpoints the general uncertainty in ecosystem response which calls for patience in managing forest ecosystems. It is possible to lead an ecosystem in a cerrain direction but the outcome cannot be exactly predicted. Consequently, ecosystem management must be based on a conStant dialogue with nature. p

Admowkdgmztnts - Thanks to the SpyNat-group for valuable commencs on the manuscript. Thanks to Eva Riner for providing the basic drawing of the gap and surroundings in Fig. 2.

Suserup Skov, a near-natural temperate deciduous forest in

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Suserup Skov, a. semi-narural forest. - &01. Bull. 52: 123-131. Bradshaw, R. H. W, Wolf, A. and Moller, P. F. 2005. Long-term succession in a Danish temperate deciduous forest. - Ecogra-

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41. The cultural landscape during 6000 years in southern Sweden - the Ystad project (1991). Editor B. E. Berglund. Price £ 21.00. 42. Trace gas exchange in a global perspective (1992). Editors D. S. Ojima and B. H. Svensson. Price £ 5.00. 43. Environmental constraints of the structure and productivity of pine forst ecosystems: a comparative analysis (1994). Editors H. L. Goltz, S. Linder and R. E. McMurtie. Price £ 5.00. 44. Effects of acid deposition and tropospheric ozone on forest ecosystems in Sweden (1995). Editors H. Staaf and G. Tyler. Price £ 5.00. 45. Plant ecology in the subarctic Swedish Lapland (1996). Editors P. S. Karlsson and T. v: Callaghan. Price £ 5.00. 48. The use ofpopulation viability analyses in conservation planning (2000). Editors P. Sjogren-Gulve and T Ebenhard. Price £ 25.00. 49. Ecology of woody debris in boreal forests (2001). Editors B. G. Jonsson and N. Kruys. Price £ 29.00. 50. Biodiversity Evaluation Tools for European forests (2001). Coordinator T.-B. Larsson. Price f 35.00. 51. Targets and tools for the maintenance afforest biodiversity (2004). Editors P. Ange1stam, M. Donz-Breuss andJ.-M. Roberge. Price f 40. 52. Suserup Skov: structures and processes in a temperate, deciduous forest reserve (2007). Editors Katrine Hahn and Jens Emborg. Price £ 30.

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195

Ecological Bulletins, Suserup Skov: Structures and Processes in a Temperate, Deciduous Forest Reserve

Forest Dynamics and Disturbance Regimes: Studies from Temperate Evergreen-Deciduous Forests (Cambridge Studies in Ecology)

Edible Forest Gardens: Ecological Vision, Theory For Temperate Climate Permaculture

Edible Forest Gardens: Ecological Vision, Theory For Temperate Climate Permaculture

Ecological Bulletins No. 51, Targets and Tools for the Maintenance of Forest Biodiversity

Forest Diversity and Function: Temperate and Boreal Systems (Ecological Studies, 176)

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Forest Dynamics: An Ecological Model

Forest Fires: Behavior and Ecological Effects

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Ecological Bulletins, Suserup Skov: Structures and Processes in a Temperate, Deciduous Forest Reserve

Forest Dynamics and Disturbance Regimes: Studies from Temperate Evergreen-Deciduous Forests (Cambridge Studies in Ecology)

Edible Forest Gardens: Ecological Vision, Theory For Temperate Climate Permaculture

Edible Forest Gardens: Ecological Vision, Theory For Temperate Climate Permaculture

Ecological Bulletins No. 51, Targets and Tools for the Maintenance of Forest Biodiversity

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