The effect of forest clearcutting in Norway on the community of saproxylic beetles on aspen

Biological Conservation 106 (2002) 347–357 www.elsevier.com/locate/biocon

The effect of forest clearcutting in Norway on the community of saproxylic beetles on aspen A. Sverdrup-Thygeson*, R.A. Ims Division of Zoology, Department of Biology, University of Oslo, PO Box 1050 Blindern, N-0316 Oslo, Norway Received 11 April 2001; received in revised form 21 November 2001; accepted 21 November 2001

Abstract In a study of the effect of forest clear-cutting on the saproxylic beetle fauna in aspen in Norwegian boreonemoral forest, we find that both sun exposure and substrate are important structuring factors for the community of saproxylic beetles. Even though the species number and abundance is rather similar across the gradient of sun exposure, there is a major turnover in species composition in decaying aspen from mature forest to clear-cuttings. Our results confirm that aspen is an important element for beetle biodiversity both because of a generally species-rich community and a high number of rare and threatened (red-listed) beetles. There is a higher probability of presence of red-listed beetle species in snags than in logs. Sun exposure increases the probability of presence of red-listed species, but this was largely an effect of one dominating species. We conclude that retention of trees when clear-cutting is an important means for safeguarding the fauna of saproxylic beetles in aspen. # 2002 Elsevier Science Ltd. All rights reserved. Keywords: Coleoptera; Conservation; Populus tremula; Sun exposure; Tree retention

1. Introduction When discussing strategies for boreal forest conservation, the focus tends to be on old-growth habitats and species (Peterken et al., 1992; Lattin, 1993; Bader et al., 1995; Noon and McKelvey, 1996; Økland, 1996; Spence et al., 1996; Thor, 1998; Burton et al., 1999; Jonsell, 1999). Old-growth forests are disappearing at a rapid rate in many areas of the boreal forest (Esseen et al., 1997), and it is important to safeguard these habitats and species before they are lost. However, a forest biodiversity strategy must not ignore critical habitats created by disturbance. Forest fires, windstorms, insects and disease outbreaks are natural disturbance agents that used to influence the forest landscape by creating open areas with large amounts of sun-exposed dead wood (Kaila et al., 1997). More recently in the Scandinavian agricultural landscape, livestock grazed the forest and created an open, * Corresponding author. Present address: NORSKOG, PO Box 123 Lilleaker, N-0216 Oslo, Norway. Tel.: +46-22-51-8900; fax: +4622-51-8910. E-mail address: [email protected] (A. Sverdrup-Thygeson).

park-like forest with solitary, sun-exposed trees (Samuelsson et al., 1994). Today, these processes are to a large degree prevented by effective wild fire control, removal of wind-thrown and weakened trees, and reduced grazing in forest areas. These factors, together with the profound effects of recent forest management, result in a general lack of coarse woody debris (CWD) in Scandinavian forest, especially CWD that is sunexposed. A large and diverse invertebrate fauna in the boreal forest depends on decaying wood for food, shelter, or reproductive activities (Hunter, 1990; Esseen et al., 1997; Jonsell et al., 1998). These saproxylic (woodliving, see Speight, 1989) organisms are important components of forest ecosystems, and play a vital role in decomposition and nutrient recycling (Samuelsson et al., 1994). In Scandinavia, many insects are considered threatened as a result of forestry and other humaninduced changes in the forest landscape. Saproxylic beetles constitute more than 20% of the species listed as forest-dwelling on the National Red Lists of rare and threatened species in Norway (Gundersen and Rolstad, 1998). Studies of all red-listed wood-living invertebrates in Sweden show that approximately 24% prefer sunexposed sites, while only 9% prefer shade. Thirty-five

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per cent are indifferent to light conditions, while 23% have an unknown preference concerning light conditions (Jonsell et al., 1998). This means that sun-exposed dead wood is a crucial habitat if we want to protect the fauna of forest invertebrates. Populus is a widely distributed genus, native to the Northern Hemisphere. While European aspen Populus tremula L. is a Eurasian species, the closely related and similar trembling aspen Populus tremuloides Michaux has a wide North-American distribution (Encyclopædia Britannica, 2000). European aspen has been called ‘‘a keystone resource amidst the conifers’’ (Niemela¨, 1997, p. 603). Large aspen trees host a diverse epiphytic flora (Gustafsson and Eriksson, 1995; Kuusinen, 1996; Kuusinen and Siitonen, 1998) and the litter is favourable for many invertebrates (Niemela¨, 1990; Koivula et al., 1999). More than 250 species of fungi are associated with aspen decay in North America (Lindsey and Gilbertson, 1978). Saproxylic invertebrates other than economically important pest species have been little studied in North America, but Hammond (1997) found a high arthropod diversity associated with Populus CWD. In Fennoscandia, decaying aspen is valued as a rich substrate for saproxylic insects, especially beetles, and many insect species associated with aspen are considered threatened (see Siitonen and Martikainen, 1994 and references therein; Martikainen, 2001). Even though aspen has a wide geographic distribution and contributes significantly to biodiversity in boreal forests, few studies of the associated invertebrate fauna have been published internationally (but see Siitonen and Martikainen, 1994; Hammond, 1997; Martikainen, 2001). Also, there is little information concerning the micro- and macrohabitat variables influencing species richness, presence of rare species and community structure of insects in decaying wood. In this study, we evaluated how forest clear-cutting affected the community structure and species richness of saproxylic beetles using aspen CWD, with special attention to red-listed beetles. The sampling design was stratified with respect to two design variables: sun exposure and type of dead wood habitat (snag/downed log). We compared the saproxylic beetle assemblage of snags and downed logs across a gradient of sun exposure, from completely open clearcuts, to mature forest. Finally, we discuss the management consequences of our findings.

2. Methods The study area covered approx. 15 km2 within a forest approximately 250 km2 in extent, 200–300 m above sea level in the boreonemoral zone 15 km east of Oslo, Norway. The forest is mostly coniferous and dominated by Norway spruce (Picea abies L. Karst.) and Scots pine

(Pinus silvestris L.), but also contains a considerable number of deciduous trees including birch (Betula spp.) and European aspen (Populus tremula L.). The bedrock is silica-dominated gneiss with a dominating north– south strike orientation, resulting in a landscape intersected by many low-relief ridges and valleys. Forestry was especially intensive in the area around 1970, and large areas are in various stages of regrowth today. Earlier, herbicides were frequently used to exclude herbs and deciduous trees, but the mature aspen trees were often left when clear-cutting to prevent massive resprouting from the stumps. A nature reserve was established in 1994 in the southern part of the study area. Our field study was conducted during the summers of 1998 and 1999. We identified appropriate areas by searching the forest management plan for stands with presence of large deciduous trees. A snag was defined as a tree ( > 20 cm diameter 1.3 m above ground) that had broken more than 2.5 m from the base but not less than 2 m from the top, creating an upright decaying snag with no green branches and an accompanying decaying log lying in contact with the forest floor. The time since snag creation could not be established, but probably varied from at least 10 to 1 years (Erling Bergsaker personal communication). Forty sites, 28 in 1998 and 12 in 1999, each represented by a snag and an accompanying log, were chosen in a random stratified sampling procedure to achieve a variation in sun exposure. All sites were more than 100 m apart. We mounted two slightly different kinds of trunk-window (flight-interception) traps Kaila, 1993; window area 130 and 200 cm2) on both the snag and on the corresponding log. On the snag, one trap was placed with the top of the window between 0.5 and 1.5 m, and the other between 1.5 and 2.5 m. Which trap to mount in which height zone as well as which cardinal direction the trap faced was determined randomly. On logs, the traps were similarly spaced and were mounted randomly on either side of the log. The traps were operated in June and July and emptied twice during this time. Habitat variables were recorded as described in Table 1. Decay stage categories were recorded according to a slightly modified modified version of Dynesius and Johnsson (1991; Table 1). We used a relascope to quantify degree of sun exposure at the site level. A relascope measures the total basal area of standing trees per area. It is commonly used in forest management planning and has also been used in ecological studies as a measurement of sun exposure (Økland et al., 1996; Rukke and Midtgaard, 1998). The range of this variable was 0–320 m2 ha 1. Because the distribution of this variable was highly skewed, we chose to represent the degree of sun exposure by an ordinal variable with three levels: Level 1 (closed forest with low sun exposure): Rscope > 210, n=13, Level 2 (medium sun exposure): 80< Rscope4210,

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Table 1 Description of habitat variables Variable

Description

Site variables CutClass Rscope AspenDens

Cut class: 1: clearcut, 2: young regenerating forest, 3: young production forest, 4: old production forest, 5: old forest Basal area of standing trees per area, in m2 ha 1:- 1: Rscope>210, 2: 80
Substrate variables Substrate HeigSnag LengLog Decay

Diam PercBark ThicBark LoosBark

Snag/downed log Height of snag Length of log Decay stage (modified from Dynesius and Johnsson 1991):- 1: wood hard, bark mostly intact; 2: wood starting to soften, bark falling off, texture smooth; 3: wood soft, with crevices, pieces of wood lost so the outline was deformed; 4: wood soft, possibly with a hard core, outer surface of the log hard to define. Diameter of snag/log, 1.3 m above ground/from thickest end % bark left on snag/log Thickness of bark: thick & coarse/intermediate/thin & smooth Looseness of bark: loose/intermediate/stuck

n=11, Level 3 (clearcuts with high sun exposure): Rscope470, n=16. 2.1. Data analyses Analyses were based on the two study design variables; i.e. degree of sun exposure (three levels) and substrate type (snags and downed logs). The effects of degree of sun exposure and substrate type on total abundance (total number of individuals), species richness (number of species) and probability of occurrence (presence/absence data for rare species) were analyzed by using mixed generalized linear models (i.e. the SASmacro GLIMMIX, Littell et al., 1996) applied to substrate specific samples of saproxylic species. Site was included as a random effect. The random site effect variable also accounts for possible year effects, as the sites were different in the two years. The models on abundance and species number were specified with logarithmic link function and Poisson error, while models applied to presence/absence data used a logit link and binomial error. Overdispersion from pure Poisson or binomial error was corrected for by the scale parameter suggested by McCullagh and Nedler (1989). The structure of the community of saproxylic species (i.e. the relative abundance of individual species) at the substrate level was analyzed by canonical correspondence analysis (CCA) with substrate type and degree of sun exposure as instrumental variables (Yoccoz and Chessel, 1988; Ter Braak, 1995). CCA is an ordination technique well suited for detecting patterns of variation in species data that can be explained by environmental data (i.e. here by the design variables). Possible confounding between the design variable sun exposure and other site and substrate specific environmental variables (Table 1) was checked for by computing Spearman rank correlation coefficients between

continuous or ordinal environmental variables. Eventually, confounded covariates were entered in the new analyses together with the design variables to explore whether the design variables had effects independent of the confounding variables.

3. Results In total 3831 individuals of 367 beetle species were caught. The number of species in this sample accounts for 11% of the total known Norwegian Coleopteran fauna. Of these, 2757 individuals (72%) and 223 species (61%) were saproxylic (Jogeir Stokland, unpublished database; Hansen et al., 1908–1965; Palm, 1959). Of the saproxylic species 18 (122 individuals) were red-listed in Norway (Table 2), all as care-demanding (Direktoratet for naturforvaltning, 1999). The majority of these species are also redlisted according to the Swedish (Ga¨rdenfors, 2000) or Finnish (Rytta¨ri, 2000) Red Lists (Table 2). Notably, three individuals of Cucujus cinnaberinus Scopoli, which is endangered in Norway (Hanssen et al., 1997) and also listed in the IUCN Red List of Threatened Animals (Baillie and Groombridge, 1996) were present in the sample. Scaphisoma boreale Lundblad was numerically dominant among the red-listed species (Table 2). According to habitat descriptions (species fact sheets from Wikars, 1992; Gundersen and Rolstad, 1998; Direktoratet for naturforvaltning, 1999; Martikainen, 2001; Threatened Species Unit, 2001; Jonsell et al., unpublished database; Stokland, unpublished database), two of the red-listed species are (at least in Scandinavia) dependent on presence of Populus tremula, three of the singletons are listed as primarily associated with fungus on coniferous trees and the remaining are described as preferring various deciduous trees (Table 2).

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Table 2 The total abundance (number of individuals), habitat description (for references see text) and distribution (number of occurrences on sites and substrate types) of red-listed saproxylic beetlesa Species

Family

Habitat

Status Sweden

Scaphisoma boreale Lundblad Cyphaea curtula Erichson

Scaphidiidae Staphylinidae

Plegaderus caesus Herbst Ampedus nigroflavus Goeze Xylophilus corticalis Paykull Microrhagus lefidus Rosenhauer Corcatoma punctulata Mulsant & Rey Cucujus cinnaberinus Scopoli

Histeridae Elateridae Eucnemidae Eucnemidae Anobiidae Cucujidae

Cryptophagus populi Paykull Atomaria alpina Heer Atomaria subangulata J. Sahlberg Leiesthes seminigra Gyllenhal Cortucaria lapponica Zetterstedt Cis dentatus Mellie Ennearthron laricinum Mellie Mycetophagus fulvicollis F Pseudocistela ceramboides L Necydalis major L No. of sites/snags/logs with red-listed beetles

Cryptophagidae Cryptophagidae Cryptophagidae Endomychidae Latridiidae Cisidae Cisidae Mycetophagidae Tenebrionidae Cerembycidae

Decid. Populus tremula in Scandinavia Decid. Decid. Decid.+conif. Decid. Decid.+conif. Decid, primarily Populus tremula Decid. Conif. Conif. Decid. Decid. Decid. Conif. Decid. Decid. Decid.

Status Finland NT

VU CR NT

NT NT NT NT

CR

EN

VU NT NT NT NT VU NT

Individuals

Sites

Snags

Logs

77 1

29 1

17 1

12 0

7 3 7 5 8 3

6 3 7 2 6 3

4 3 6 0 5 3

2 0 1 2 1 0

1 1 1 2 1 1 1 1 1 1 122

1 1 1 2 1 1 1 1 1 1 31

1 1 0 2 1 1 1 0 1 1 29

0 0 1 0 0 0 0 1 0 0 16

a Decid.= primarily deciduous trees, Conif.= primarily coniferous trees. All species are listed as care-demanding (following old IUCN categories) in the Norwegian Red List (Direktoratet for naturforvaltning, 1999). Status on the Swedish (Ga¨rdenfors, 2000) and Finnish Red Lists (Rytta¨ri, 2000) is also given (NT=Near Threatened, VU=Vulnerable, EN=Endangered, CR=Critically Endangered).

3.1. Abundance and species richness

3.2. Probability of occurrence of red-listed species

Neither substrate type (F1,39=0.09, P=0.76) nor degree of sun exposure, (F1,39=0.54, P=0.59) affected the total abundance of saproxylic species which averaged 34.5  25.6 (SD) individuals per sample. As indicated by the large standard deviation around mean abundance there was much extra variability (i.e. overdispersion) compared to the expected Poisson error (extra-dispersion scale parameter: 9.50 vs. the expected 1). Turning to species number, the random site effect model with a substrate type effect fitted the data quite well (extra-dispersion scale parameter=1.61; neither sun exposure nor the interaction between substrate type and sun exposure had any effect; P > 0.85). The estimated number of saproxylic species captured per substrate sample was significantly higher (F1,39=6.42, P=0.02) in snags (17.2 species, 95% CI: [15.3, 19.3]) than in logs (14.4 species, 95% CI: [12.7, 16.3]). The cumulative number of saproxylic species captured on snags was 169, while it was 156 on logs. The estimated proportion of saproxylic beetles of all beetles sampled was higher on snags (0.83, 95% CI: [0.79, 0.86]) than on logs (0.62, 95% CI: [0.58, 0.66]). There was a higher estimated number of non-saproxylic species per sample on logs (8.7 species, 95% CI: [7.3, 10.5]) than on snags (3.5 species, 95% CI: [2.7, 4.5]).

The mean number of red-listed species (0.86 0.95 SD) and individuals (1.54 2.57 [SD]) in the substrate samples was low so that it seemed most appropriate to analyse the occurrence of red-listed species as a binary response (i.e. presence/absence) with a logistic model. However, the numerical algorithm of the random site effect model did not converge when the interaction between substrate type and sun exposure was fitted. In a model with main effects only, both substrate type (F1,39=11.39, P=0.002) and degree of sun exposure (F1,39=5.51, P=0.008) were significant. There was a higher probability of presence of red-listed species in snags (0.77, 95% CI: [0.69, 0.88]) than in logs (0.38, 0.23, 0.57, while the probability of presence increased over the three categories of sun exposure (level 1: 0.27 [0.12, 0.51], level 2: 0.67, [0.40, 0.86] and level 3: 0.80, [0.59, 0.91]). However, an interactive effect between sun exposure and substrate type was indicated when the site effect was disregarded and a simple logistic model was fit to the proportions of samples with presence of redlisted species (w2= 8.03, df=3, P=0.05). The interaction was mainly due to the absence of red-listed species in logs at sites with least sun exposure (Fig. 1). Since one species, S. boreale, numerically dominated the sample of red-listed saproxylic species (Table 2), two additional analyses were conducted; one separate

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3.3. Community structure

Fig. 1. The proportion of samples at the substrate level with presence of red-listed species in relation to substrate type (snags and downed logs) and degree of sun exposure (three ordinal categories). Numbers above the bars gives number of sites with presence/absence.

analysis on presence/absence of S. boreale and one separate analysis on the 17 other much rarer red-listed species combined. Again, convergence by the numerical algorithm was not achieved when random site effect models were fitted with an interaction term. Models including main effects suggested a significant (F1,39=4.62, P=0.02) increase in the probability of presence of S. boreale with increasing sun exposure (level 1: 0.11 [0.03, 0.30], level 2: 0.40, [0.20, 0.64] and level 3: 0.53, [0.33, 0.72]). Substrate type was the only significant (F1,39=10.91, P=0.02) predictor of the probability of presence of the other red-listed species (snags: 0.55 [0.39, 0.70], logs: 0.18 [0.08, 0.33]. The interaction between substrate type and sun exposure which was indicated for all red-listed species combined, was no longer significant when the data was split on S. boreale (w2= 4.41, df=3, P=0.22) and other red-listed species (w2= 6.50, df=3, P=0.09).

The CCA on the entire assemblage of saproxylic species demonstrated a clear structuring effect of substrate type and sun exposure after one outlying species (Mycetochara flavipes Fabricius) of the total of 223 species was omitted. M. flavipes had an extremely aggregated distribution with 96% of the 108 individuals appearing in two samples. The two instrumental variables (i.e. sun exposure and substrate type) had the greatest explanatory power (11.6% of the variance) when specified in the CCA as an interaction (substrate type sun exposure). The ordination plot of substrate specific samples showed that logs and snags were generally very well separated irrespective of degree of sun exposure (Fig. 2A). The ordering of samples with respect to sun exposure was qualitatively the same for both substrate types. Especially, the two most extreme sun exposure categories (i.e. 1 and 3) were well separated. Sun exposure had a clearer structuring effect on the species assemblage in snags than in logs (Fig. 2A). The distribution of red-listed species in the ordination diagram (Fig. 2B) reflected the pattern revealed in the analysis of probability of presence; i.e. red-listed species occurred most frequently on snags, and were absent on the least sun exposed logs (Fig. 2A). Table 3 lists 15 saproxylic species (with at least 10 individuals in the total sample) that was associated with the three most distinct site and substrate characteristics evident from the CCA (Fig. 2A); i.e. snags on sites with little or much sun and logs on sites with little sun. The grouping of species was done by selecting the five species with highest scores on the x-axis (corresponding to little sun/logs), lowest scores on the x-axis (corresponding to much sun/snags) and the lowest scores on the yaxis of the ordination diagram (corresponding to little sun/snags), respectively (Fig. 2A). As we use a threshold of at least 10 individuals in the total sample, the species in Table 3 are relatively common. Many of them are known from a range of dead wood habitats, not only on aspen. Still it is evident from Table 3 that the species differentiate clearly between habitat categories of aspen dead wood. The species in the sun-exposed/snag category seemed to be the most specialised in terms of proportion of occurrence. These species were also fairly abundant. One of the species in this category, Ptilinus fuscus Geoffroy, is previously described as an aspen specialist in northern deciduous forest (Wikars, 1992; Martikainen, 2001). Species in the shaded/log category were both less abundant and specialised (Table 3). 3.4. Association between sun exposure and other environmental variables Degree of sun exposure was not correlated with other site variables (rsp < 0.14, n=40, P > 0.38) except for forest

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There were no systematic patterns in the trapping results that could be related to year of trapping. At the substrate level, degree of sun exposure was positively correlated with the diameter of snags (rsp=0.53, n=40, P=0.0003) and logs (rsp=0.33, n=40, P=0.04), and negatively with percentage bark on snags (rsp= 0.42, n=40, P=0.008; Fig. 3). None of the other substrate variables (HeigSnag, LengLog, Decay, ThicBark, LoosBark) covaried with sun exposure. The two significant substrate level covariates of sun exposure (i.e. percent bark and trunk diameter) were entered the models of species richness of saproxylic species and probability of presence of red-listed species. The random site effect had to be discarded from the model to achieve convergence by the numerical algorithm. Diameter did not improve any of the models of species richness or probability of presence of red-listed species as evaluated by the model selection criterion AIC (Burnham and Anderson, 1992); i.e. this variable did not have any effect independent of substrate type and sun exposure. However, there was a significant, partial effect of percent bark which indicated a significantly increased probability of presence of all redlisted species with increasing amount of bark on the trunk (estimate: 0.0241  0.0110, F1,75=4.77, P=0.03). The sun exposure effect remained significant in this model (F1,75=5.45, P=0.04). The covariates trunk diameter and percent bark were also entered the CCA with the effect of the interaction between sun exposure and substrate removed. It appeared that they had no clear independent structuring effect on the community of saproxylic species (only 2% of the variation was accounted for by trunk diameter and percent bark). Fig. 2. CCA ordination plots of (A) sample scores and (B) scores of saproxylic species on the two most influential axes from a CCA constrained by the interaction between substrate type and sun exposure. In the sample plot (A), the size of the symbols indicates sun-exposure category (ordinal scale: ‘‘1’’, ‘‘2’’ and ‘‘3’’; increasing size of symbol corresponding to increasing sun exposure). In the species plot (B), ‘‘Sb’’ denotes Scaphisoma boreale, ‘‘R’’ denotes other red-listed species, while ‘‘o’’ represents all other species.

cut class (rsp= 0.83, n=40, P < 0.0001) reflecting the fact that relascope sum was closely related to the forestry regime. The density of dead aspen in the surroundings did not show a consistent relationship with sun exposure: The estimated number of dead aspens within a radius of 100 m of the sampled trees was very similar in clearcuts (2.54 trees/snags, 95% CI: [2.00, 3.08]) and closed forest (2.19 trees/snags, 95% CI: [1.70, 2.67]), but it was lower around the sampled trees in semi-shade (1.00 trees/snags, 95% CI: [0.41, 1.59]).

4. Discussion The present study shows that aspen is an important element for the saproxylic beetle fauna in the boreal forest, because it harbours both a generally species-rich community and a high number of rare and threatened beetles (Table 2). The fact that more than 10% of the entire Norwegian beetle fauna was sampled from only 40 dead aspen trees clearly illustrates the rich beetle community hosted by dead aspen trees. A large number of single-individual occurrences in the sample (Table 2) precluded robust projections of the real number of saproxylic species on aspens in the study area (e.g. based on species accumulation curves, Colwell and Coddingston, 1995), but the real number is certainly much higher than that actually observed. The finding of the internationally endangered beetle Cucujus cinnaberinus (Baillie and Groombridge, 1996), found only a few times in Scandinavia in this century (Hansen, 1994),

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Table 3 Fifteen saproxylic species (with No. individuals>10) that according to scores on the two CCA axes (Fig. 2) could be grouped most distinctly with respect to site (sun exposure levels= 1 [shade], 2 [semi-shade] and 3 [sun-exposed]) and substrate type (snags or logs) CCA-grouping/speciesa

Snag

Log

Total No. of individuals

Shade

Semi-shade

Sun-exposed

Shade

Semi-shade

Sun-exposed

Shade/logs Epuraea pygmaea Gyllenhal Octotemnus glabriculus Gyllenhal Agathidium confusum Brisout Anisotoma castanea Herbst Arpidiphorus orbiculatus Gyllenhal

0.07 0 0 0 0.01

0.07 0 0 0 0.01

0 0 0.09 0 0.01

0.86 0.72 0.73 0.23 0.48

0 0.16 0.18 0.69 0.16

0 0.12 0 0.08 0.33

14 25 11 26 297

Shade/snags Triplax aenea Herbst Cryptophagus scanicus L. Glischrochilus quadripunctatus L. Quesius plagiatus Mannerheim Hylecoetus dermestoides L.

0.83 0.59 0.36 0.29 0.38

0.04 0.24 0.55 0.50 0.31

0 0.06 0 0.07 0.13

0 0.12 0.09 0.14 0.19

0 0 0 0 0

0.13 0 0 0 0

23 17 11 14 16

Sun exposed/snags Cis comptus Gyllenhal Ampedus tristis L. Ampedus baltustulata Latreille Dacne bipustulata Latrielle Ptilinus fuscus Geoffrey

0.03 0 0 0.02 0.02

0 0 0.11 0.11 0.18

0.89 0.88 0.84 0.80 0.75

0 0 0 0 0

0 0 0.03 0 0.03

0.08 0.12 0.03 0.07 0.02

38 41 38 44 61

a Shade/logs: five species with the most positive scores on the x-axis. Shade/snags: five species with the most negative scores on the y-axis. Sunexposure/snags: five species with the most negative scores on the x-axis. The proportion of individuals in each site/substrate combination out of the total number of individuals is shown.

further supports our conclusion concerning the importance of aspen habitat. Concerning the high number of S. borealis occurrences, it might indicate that this species is more common than previously thought and therefore should not be red-listed. The species is not red-listed in Sweden or Finland (Table 2). It is also possible, however, that the species is unusually frequent in this landscape because the density of dead and living aspen trees is rather high compared to boreal forest in other parts of south-eastern Norway, where mature aspen trees are rare (e.g. Ohlson and Tryterud, 1999; Sverdrup-Thygeson, 2001). The fact that density of dead aspen trees in the near surroundings (100 m radius) did not help to explain the diversity patterns, can be due to several factors. One can assume that the density of dead aspen in this landscape as a whole is above some unknown threshold value and the variation thus does not add to the explanation, or one can assume that the beetles adapted to this substrate is capable of finding this resource even though it is dispersed, and that resource density therefore is of secondary importance to resource quality. 4.1. Effects of sun exposure Sun exposure is clearly an important structuring factor for the community of saproxylic beetles in dead aspen. Even though species number and abundance is

rather similar across the gradient of sun exposure, our study shows that even among relatively common species there are clear habitat preferences concerning degree of sun-exposure in aspen CWD (Table 3). Among the rare species, S. boreale clearly preferred sun-exposed CWD, especially snags (Fig. 1B). Basal area of standing trees not only reflects sun exposure, but also the related factor, density of trees. If visual cues are important when searching for new habitat, it is likely that a dispersing beetle will more readily detect and colonize a snag or log in an open area, than similar CWD in closed, dense forest. Dispersal by wind will also favour CWD in open areas. Unfortunately, we know very little about the dispersal and search techniques of these beetle species. Beetle sampling by means of traps does not provide a random sample of the total pool of beetles, but reflects activity. As beetles are ectothermic animals, activity is dependent on ambient temperature. Thus there is a possible bias towards collecting higher numbers of individuals in the warm, sun-exposed sites than in the cooler, less sun-exposed sites. Notice, however, that there was no difference between sun-exposed and shaded sites in terms of number of trapped individuals. Thus we believe that the major qualitative difference in species composition revealed in this study between sites with different sun exposure is not an artefact due to a sampling bias.

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aspen CWD in boreal forest by showing that this result is also valid for another geographic and climatic region within the boreal forests in Fennoscandia. 4.2. Differences between snags and logs

Fig. 3. Relationship between degree of sun exposure versus percent bark and diameter of snags and downed logs.

These findings agree with those of Kaila et al. (1997), who compared standing dead birch (Betula spp.) trunks in clear-cut areas with similar trunks in mature forest. They found that median number of species or specimens caught did not differ between clear-cuts and closed forest, but individual beetle species occurred unevenly among the habitats. They concluded that dead birch trees left in clearings could host many specialist beetle species dependent on warm, sun-exposed environments, and that some of these species might not be able to survive in closed forest. Martikainen (2001) studied snags on four clearcuts with snags in two old-growth forest stands in Finland, and found that many of the species previously thought of as old-growth specialists actually preferred sun-exposed habitats. Ahnlund (1996) demonstrated that a high number of rare and threatened insects species (n=31) could be found on a single, sun-exposed aspen snag in south-central Sweden. Siitonen and Martikainen (1994) compared the fauna of beetles and flat bugs under bark of decaying aspen in Finnish and Russian Karelia, and suggested that a high abundance and continuity of large, dead sun-exposed aspen trees contributed to a considerably richer fauna of threatened insects in Russian Karelia. Our results further supports and strenghten importance of sun-exposed

There were also large differences in the faunal composition between upright snags and downed logs. Snags were more species-rich and also the probability of presence of red-listed species was higher in snags. Jonsell et al. (1998), in a review of Swedish research on the topic, also concluded that more red-listed saproxylic insects preferred snags than downed logs. Snags and logs differ in many aspects, most importantly in the temperature and the humidity of the wood (Hunter, 1990), which is a key factor explaining the fauna of saproxylic insects (Samuelsson et al., 1994). A snag will be raised above the soil and ground vegetation and into the wind, and will be drier than a downed log and less favourable for many decomposers, particularly many fungi. As we know that many wood-living invertebrates are dependent on fungal mycelium or spores for nutrition (Wheeler and Blackwell, 1984; Wilding et al., 1988), possible differences in fungal flora may explain the differences seen in the saproxylic beetles communities in snags versus downed logs. Closeness to the ground dampens variations in humidity in the decaying wood. This can explain why sun exposure had a stronger structuring effect on the beetle community in the snags than in downed logs (Fig. 2A). The interaction between substrate type (snag/log) and sun exposure was also seen in the probability of presence of red-listed beetles (Fig. 1). No specimens of any of the 18 redlisted species were sampled from logs in dense and dark forest. Also among the relatively more abundant species there seemed to be little preference for the shaded/log habitat category. In contrast, sun-exposed snags tended to harbour more specialised species (Table 3). As the logs in this study were the upper part of the trunk (above snag), the log diameter and bark thickness of logs systematically had lower values than snags. It is thus possible that logs created by windfall of intact trunks may differ from the logs in this study. Also, trap efficiency may be lower on logs than on snags, as flight close to the logs could be partly obstructed by ground vegetation. Note, however, while the number of saproxylic species increased from logs to snags, the number of other beetle species decreased, indicating that traps on logs were not generally less efficient. There is a negative correlation between sun exposure and bark percentage (Fig. 3). Still, as both sun exposure and bark percentage increases the probability of red-listed beetles being present, one can assume that if present, sun-exposed aspen snags with much bark remaining will be the optimal habitat for the red-listed beetles. The bark supplies nutrients and a range of

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microhabitats for saproxylic beetles, as well as a certain protection from predation and desiccation. The percentage of bark retained could be related to time since death of the tree, a variable that is hard to measure objectively in retrospect. Trees that have been dead for less than five years (and thus have much bark retained) host a higher number of red-listed insects than more decayed standing trees (Samuelsson and Ingelo¨g, 1996).

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Depending on site characteristics like soil depth and wind exposure, trees left in clearcuts might be unstable and easily topple over, thus creating a log only. In such areas, snags can be created artificially by cutting the tree some meters above ground. As aspen snags have more species and more red-listed species than logs, such means will probably benefit the local saproxylic beetle fauna.

4.3. Management consequences Acknowledgements In the production forest of Fennoscandia, managers have striven to eliminate aspen because it delays regeneration of the more valuable coniferous trees, and the present scarce distribution has caused concern (Siitonen and Martikainen, 1994; Kouki et al., 2001; Martikainen, 2001). As it is clear that aspen contributes significantly to the diversity of saproxylic beetles, as well as other species, more focus should be placed on this tree species in the conservation debate. In the long run, oldgrowth reserves will include few mature aspen trees and little CWD from aspen, because aspen is an early successor and is largely outcompeted in mature coniferous forest where large-scale natural disturbances are prevented (Linder et al., 1997). Therefore, rather than considering reserves, we must focus on the dynamic, managed landscape when considering appropriate management alternatives for the beetles dependent on aspen. In a recent study of beetles on retained aspen in Finland, Martikainen (2001) found that many of the species associated with aspen seemed to prefer sun-exposed habitats. Retaining aspen trees when clear-cutting will increase the abundance of sun-exposed, decaying wood in the landscape, and the present study confirms the value of such tree retention. Other species than beetles may also benefit from retained aspen trees. A study of lichens on retained aspen indicates that these trees can form biodiversity links during forest succession after final harvest (Hazell and Gustafsson, 1999). In addition to the retained aspen trees left to enrich reestablishing coniferous stands, a few regenerating stands should be left to develop through the entire deciduous-dominated succession phase that would naturally take place before the coniferous trees take over. This would create high-density patches of living and dead aspen; thus emulating the natural processes in the boreal forest landscape (Hansson, 1992; Angelstam, 1998; Landres et al., 1999). To aid the fauna of beetles dependent on aspen CWD, it is necessary to make sure that this substrate is available in habitats with different degrees of sun exposure. By leaving both dead and living aspen trees of various ages when clear-cutting, snags and logs with varying sun exposure can develop in the regenerating stand as time goes by. Leaving groups of aspen and not only solitary trees will also create variation in sun exposure and stages of decay.

We are grateful to Losby Bruk, represented by Erling Bergsaker, for access to study sites and for practical assistance. Sampling in the Rausjømarka nature reserve was done with permission from the proper authorities. Thanks are due to Randi and Kjetil Sverdrup-Thygeson for field assistance, to Sindre Ligaard who identified the beetles, to Mats Jonsell and Jogeir Stokland for providing data on beetle habitat preferences, to Nigel S. Yoccoz who provided excellent help with the CCA and to Tone Birkemoe, Lena Gustafson, Petri Martikainen, Jari Niemela¨, Dag Hjermann, Jari Kouki and an anonymous referee for valuable comments on the manuscript. This study is part of a co-operation between the Norwegian Forestry Association NORSKOG and the University of Oslo, Department of Zoology and received financial support from The Norwegian Research Council.

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