Exploring the “last biotic frontier”: Are temperate forest canopies special for saproxylic beetles?

Forest Ecology and Management 261 (2011) 211–220

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Exploring the “last biotic frontier”: Are temperate forest canopies special for saproxylic beetles? Christophe Bouget a,∗ , Antoine Brin b , Hervé Brustel b a b

Institute for Engineering in Agriculture and Environment (Cemagref), Research Unit ‘Forest ecosystems’, Domaine des Barres, F-45290 Nogent-sur-Vernisson, France Université de Toulouse, Ecole d’Ingénieurs de Purpan, 75 voie du T.O.E.C., BP 57611, F-31076 Toulouse Cedex 03, France

a r t i c l e

i n f o

Article history: Received 11 August 2010 Received in revised form 1 October 2010 Accepted 6 October 2010 Keywords: Insect Deadwood Biodiversity Stratification

a b s t r a c t Conserving saproxylic beetles in temperate forests will require a better understanding of habitat requirements. So far, quantitative community studies have rarely considered their vertical requirements. In comparison with the tropical forest canopy, it remains to be seen whether a comparably high level of beetle diversity exists in the temperate forest canopy. We compared saproxylic beetle assemblages at two vertical levels in three temperate French forests. Two datasets originated from emergence traps of pine and oak deadwood substrates (mid-canopy and forest floor branches) in lowland forests. The third compared flying beetle fauna at mid-canopy and understory levels using pairs of flight interception traps in beech-fir mountain forests. Our study provided contrasting results regarding the contribution of each stratum to biodiversity. Whereas higher abundance and species richness were apparent in understory samples in beech-fir stands and in oak branches, no difference for richness – or even the opposite pattern for abundance – was observed in pine branches. A significant inter-strata dissimilarity was revealed in all datasets. Each stratum harbored specialist taxa. Exclusive canopy species accounted for 20–40% of all species. In accordance with dissimilarity partitioning, arboreal saproxylic beetle communities were not just nested subsets of ground assemblages. It is likely that microhabitat requirements, food availability and other non-resource-based factors (microclimate preference, species interactions) drive the stratification of beetle assemblages. Our results lend support (i) to the recommendation of a multi-strata sampling strategy for forest insects and (ii) to management practices in favour of valuable canopy micro-habitats. © 2010 Elsevier B.V. All rights reserved.

1. Introduction European temperate forests face a number of continuing (timber harvesting, habitat fragmentation) and increasing (fuelwood production) threats to saproxylic organisms. Conserving saproxylic beetles in complex European landscapes will require a better understanding of saproxylic beetle habitat requirements. The specialised invertebrates that depend on dead wood constitute an exceptionally species-rich ecological group, but are also among the most rapidly declining parts of European biodiversity (Nieto and Alexander, 2010). The decline is usually attributed to an insufficient supply of dead wood in managed forests. It warrants serious concern, considering the great number of highly specialised European saproxylic species (Vodka et al., 2009).

∗ Corresponding author. Tel.: +33 2 38 95 05 42; fax: +33 2 38 95 03 59. E-mail addresses: [email protected] (C. Bouget), [email protected] (A. Brin), [email protected] (H. Brustel). 0378-1127/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2010.10.007

In the few studies that take into account the possible differences in substrate and habitat requirements of saproxylic species the deadwood stratum is one of the parameters used to describe saproxylic insect habitats (Hjältén et al., 2007). Our knowledge of insect communities in the upper layers of the forest is limited, however, because the canopy is difficult to access (Ozanne et al., 2003). Available studies often concern non-saproxylic arthropods (e.g. Ozanne, 1999; Su and Woods, 2001; Gruppe et al., 2008; Sobek et al., 2009). So far, quantitative studies have rarely considered the vertical requirements of saproxylic beetles, notably in temperate regions (but see Larkin and Elbourn, 1964; Jukes et al., 2002; Wermelinger et al., 2007; Vodka et al., 2009). It remains to be seen (i) whether a high level of biodiversity can be found in the canopy of temperate forests (in comparison with the well-known insect-rich tropical forest canopy; Erwin, 1983; Novotny and Basset, 2005), (ii) how much temperate forest canopies contribute to global species richness, and (iii) how specialised insect species are depending on vertical zones. Basset et al. (2003) suggested that vertical gradients may be less pronounced in temperate forests than in tropical forests, and

Maritime pine plantations (Private Landes Forest) 5 5 5 5 5 5 5 5 Small (3–5 cm)

Freshly dead Half decayed Freshly dead Half decayed 2006 Emergence traps (deadwood collection and beetle rearing) Maritime pine deadwood

Very small (1–2.5 cm)

2006–2007 Emergence traps (deadwood collection and beetle rearing)

Medium-sized (10–20 cm)

611 ind. 39 sp.

1535 ind. 201 sp. Lowland oak forests (Rambouillet State Forest) 5 5 5 5 Half decayed Highly decayed Half decayed Highly decayed

7 7 7 7

30 30

Understory/ ground-lying

Canopy/ suspended

Highland Beech-Fir forests French Pyrenees (Ariege)

Forest type and location Sample size Number of traps Plots—sampling design

5 sites, 6 trees per site 2 paired traps per tree (low 1.5 m height/canopy 15 m height) Small deadwood (5–10 cm) 2004

Oak deadwood

2.1.2. Canopy vs. ground saproxylic beetles in pine deadwood In different mature stands (30–40 years) in a large plantation of maritime pine Pinus pinaster in south-western France (Landes

Cross-vane windowflight traps (flying beetle trapping)

2.1.1. Canopy vs. understory flying saproxylic beetles in mountain beech-fir forests In five highland beech-fir forests in the French Pyrenees (Ariege), four with beech-dominated stands (Andronne, Col du Portillon, Monts d’Olmes and Castillon forests) and one with a fir-dominated stand (Bethmale forest), flying saproxylic beetles were sampled using paired cross-vane flight interception traps (one near the ground and a second suspended 15–20 m above in the canopy, spaced 50 m or more apart). The active insect fauna was collected from March to September in 2004 in a collecting jar attached underneath the funnel and the panes, and half filled with a salt mixture as a killing and preservative agent.

Beech-Fir stands

2.1. Study areas and sampling methods

Sampling year(s)

The purpose of this study was to compare the composition of saproxylic beetle assemblages at two vertical levels in several temperate forests. The study sites were chosen in mature forests in three temperate deciduous/mixed forest regions, and two sampling methods were used to compare the entomofauna of tree canopy and understory. Dataset composition and sampling design are described in Table 1.

Sampling method

2. Materials and methods

Dataset

Lowman et al. (1993) hypothesized that the stratum of peak insect diversity will generally be near the ground in temperate forests and in the canopy in tropical forests. For insects in general, Nielsen (1987), Le Corff and Marquis (1999), Preisser et al. (1998) and Ulyshen and Hanula (2007) have shown that the stratum with peak abundance or greatest diversity vary. The most likely explanation of the predominance of ground-based insects in temperate forests may relate (i) to the higher seasonal variation and (ii) to the lower number of niches in the temperate forest canopy than in the tropical forest canopy. In temperate forests, the environment of saproxylic beetles is stratified into distinct forest layers (forest floor/understory/midcanopy/tree top). This vertical gradient relates to microclimate conditions, distribution pattern of micro-habitats and species interactions. However, few community-level entomological studies have been carried out in temperate regions (but see Vance et al., 2003) and species composition per stratum is poorly documented. A better understanding of insect forest stratification is needed to inform conservation planning (Lowman and Wittman, 1996), but also to optimize sampling strategies; the value of current faunistic lists mainly based on ground sampling may be questionable. Would complementary canopy-based sampling help establish more realistic estimates of species diversity in temperate forests? Do attempts to assess the effects of silvicultural practices need to consider the entire vertical distribution of insect fauna in a stand? We tested the hypothesis of a significant vertical differentiation of saproxylic beetle assemblages among forest strata in terms of species composition and guild structure. In different French temperate forests, is the bulk of saproxylic beetle diversity near the ground? Are there characteristic species in each stratum? Are there canopy specialists among saproxylic beetles, as in nonbeetle (Bankowska, 1994) or non-saproxylic groups (Saure and Kielhorn, 1993; Ulyshen et al., 2010)? Or are canopy assemblages only nested subsets of understory assemblages? Alternatively, is there a uniform distribution of flying insects between the canopy and understory, resulting in an equal contribution of both strata to saproxylic beetle biodiversity (Hirao et al., 2009).

3325 ind. 158 sp.

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Table 1 Overview of sampling designs whose datasets were used in this study (ind.: individuals and sp.: species).

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de Gascogne), dead branches were cut in crowns of standing living trees, or lying logs were picked up on the ground, and put in emergence traps. Aerial branches were sawn off in recently felled trees (only some days after cutting), at a canopy height from 10 to 20 m. Each pine trap contained two pieces of deadwood for a total length of about 2 m (0.0006 m3 per bag for very small branches, 0.002 m3 per bag for small branches). 40 emergence bags were set up (20 of lying logs, 20 of attached dead branches). Samples covered a range of decay stages, from freshly dead to half-decayed, and deadwood diameter, but all decay and diameter classes were evenly represented within each stratum class to avoid any bias (Table 1). Highly decayed and medium-sized dead branches from pine crowns are missing from our samples (Table 1). Each bundle of dead branches was enclosed in fine polyethylene bags with a 500 ␮m × 600 ␮m mesh. Emerging insects were collected in a plastic bottle attached to the trap, half-filled with a preservative mixture. Rearing bags were kept in forest conditions, suspended or lying on the ground. Insects were given to emerge from deadwood sampling in April 2006 to October 2007. Saproxylic beetles were sorted, identified to species level according to the nomenclature of the Fauna Europaea Web Service (2004) and assigned to a trophic group according to the nomenclature proposed by Bouget et al. (2005). 2.1.3. Canopy vs. ground saproxylic beetles in oak deadwood Similarly, in different mature stands (100–120 years) in the sessile/pedunculate oak forest of Rambouillet, a 22,000-ha state forest in northern France, 50 km west of Paris, dead branches were cut in crowns of standing living trees (actually in recently felled trees), or lying logs picked up on the ground, and put in emergence bags. 48 emergence bags, coming from 19 forest plots, were set up (24 for lying logs, 24 for mid-canopy deadwood). The number of pieces (1 m long each) within each oak trap differed depending on the diameter class: 30 pieces for small branches (0.04 m3 per bag), 10 for medium-sized branches (0.05 m3 per bag). Oak bundles were made up of several branches, cut in the crown of several felled trees, at a canopy height from 10 to 20 m. Samples covered a range of decay stages, from half-decayed to highly-decayed, and deadwood diameter, but all decay and diameter classes were evenly represented within each stratum class to avoid any bias (Table 1). Very small dead sticks and freshly dead branches in living oak crowns are missing from our samples (Table 1). Sampling method and sorting protocol were the same as in the pine deadwood study. The main purpose of the study was to compare assemblages between stratum classes within a given tree species. Our sampling design was quite balanced for each tree species, but a comparison between tree species would reveal some discrepancies (see above and Table 1); some differences between oak and pine sampling designs mentioned above further weaken such a comparison. In addition, results based on active flying insect trapping in beech-fir stands and those based on larval beetle rearing in oak and pine logs obviously differ on principle (Sverdrup-Thygeson and Birkemoe, 2009). 2.2. Data analysis The main analytical objective was to compare two strata – canopy (or tree crowns) vs. understory (or ground level) – within a given species. No other major environmental variable was included in our analytical models. 2.2.1. Number of deadwood-associated species in canopy vs. understory Differences in mean number of individuals and species between canopy and understory assemblages were tested with:

213

- paired Wilcoxon signed-rank tests for the beech-fir forest paireddesign dataset, - multiple comparison of means (Tukey contrasts) in a Generalized Linear Model (GLM) with a Poisson structure (multcomp R package), for oak and pine emergence data. We figured the absolute and relative number of unique species for each stratum or species shared by the two strata. In the paired design, we considered the mean number per site in each stratum. This number may be over-estimated, since some species may be unique to a stratum in a site, but shared by the two strata over the all sites. In the two unpaired emergence designs, we considered the cumulated number per stratum over the whole sampling design. Cumulative species richness estimators [Mao Tau] were performed using EstimateS (v. 7.5, Colwell, 2005). Confidence intervals were calculated for interpolated values (100 runs, data including singletons). For the beech-fir forest paired-design dataset only, the exhaustiveness parameters of canopy and understory traps were calculated using the ComDyn4.0 software (order 1 jacknife method, closed M(h) model, Hines et al., 1999). The detection probability of saproxylic beetles in stratum j in site i was defined as the observed number of species in stratum j in site i divided by the estimated number of ‘trappable’ species in stratum j on site i, which reflects stratum exhaustiveness regarding the pool of ‘trappable’ species. 2.2.2. Species composition Similarity between strata in terms of species composition was analysed using Sorensen’s distance measure on presence–absence matrices without singletons. In the beech-fir paired dataset, we figured the mean of all pairwise intra-site similarities. The comparison was conducted on the whole assemblage and on simplified species assemblages restricted to each trophic group. ANOSIM tests (vegan R-package) enabled us to assess the significance of observed dissimilarities. Dissimilarity partitioning. Dissimilarity (or beta diversity) reflects two different phenomena: nestedness and spatial turnover (Baselga, 2010). Nestedness of species assemblages reflects a nonrandom process of species loss as a consequence of any factor that promotes the orderly disaggregation of assemblages. Contrary to nestedness, spatial turnover implies the replacement of some species by others as a consequence of environmental, spatial or historical constraints. Disentangling nestedness from turnover is crucial to improving our understanding of central conservation issues (Koleff et al., 2003). Baselga (2010) suggested the partitioning of the Sorensen dissimilarity index (␤sor) into the Simpson dissimilarity index (␤sim) describing spatial turnover without the influence of richness gradients, and the nestedness-resultant dissimilarity (␤nes). ␤nes is a measure of the dissimilarity of communities due to the effect of nestedness patterns. Distance matrices were computed using the R functions ‘beta-pairwise.R’ (Baselga, 2010). 2.2.3. Characteristic indicator species Species occurring in more than 3 samples with at least 20 individuals were tested for stratum preferences. Characteristic saproxylic beetle species were identified for each stratum using the indicator value method (Dufrêne and Legendre, 1997). This method combines measures of specificity (abundance) and fidelity (frequency of occurrence) and provides an indicator value (IndVal) for each species, as a percentage, as follows (Dufrêne and Legendre, 1997). Following Dufrêne and Legendre (1997), a random reallocation procedure of sites among site groups was used to test the significance of the IndVal measures for each species and a threshold level of 25% for the index was accepted.

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Table 2 Overview of the deadwood-associated species assemblages in canopy vs. understory: mean number of individuals and species, number of unique or shared species, cumulative species richness and exhaustiveness, canopy-understory Sorensen dissimilarity and dissimilarity partitioning. Dataset

Window-flight trapped beetles Beech-fir mountain forests

Reared beetles Oak branches

Reared beetles Pine branches

Variable

Canopy

Forest floor

Significance

Number of individuals Number of unique speciesa Mean species richness Interpolated cumulative species richness [Mao Tau] (n = 29) Detection probability Number of shared speciesa Mean Sorensen dissimilarity Dissimilarity partitioning

996 5.1 (24%) 12.9 97 (84.6–109.4)

2329 11.9 (58%) 21.2 126.4 (113.9–138.9)

**

Mean number of individuals Number of unique speciesb Mean species richness Interpolated cumulative species richness [Mao Tau] (n = 20) Number of shared speciesb Mean Sorensen dissimilarity Dissimilarity partitioning

23.9 42 (21%) incl. 14 singletons 12.8 106.0 (95.2–116.8)

Mean number of individuals Number of unique speciesb Mean species richness Interpolated cumulative species richness [Mao Tau] (n = 23) Number of shared speciesb Mean Sorensen dissimilarity Dissimilarity partitioning

14.5 17 (44%) incl. 8 singletons 2.5 20.8 (14.7–26.8)

0.4973

** *

0.6007 3.9 (18%) 0.63 Spatial turnover = 0.46 (73%) Nestedness = 0.17 (27%) 37.8 94 (47%) incl. 41 singletons 15.1 134.5 (121.2–147.9)

64 (32%) 0.85 Spatial turnover = 0.79 (93%) Nestedness = 0.06 (7%) 8.9 16 (41%) incl. 3 singletons 2.6 22.0 (17.6–26.4)

6 (15.4%) 0.88 Spatial turnover = 0.83 (94%) Nestedness = 0.05 (6%)

**

* *

R = 0.22**

**

ns ns

R = 0.27**

R: Anosim R-statistics of a 1000-run permutation test; n: number of traps for sample-based interpolation comparison of cumulative richness; between parentheses is the 95% confidence interval. a In this paired design, we figured the mean number of species in each stratum per site. b In this unpaired design, data are cumulated over the whole sampling design, throughout the studied forest. Significance: ns p > 0.05. * 0.05 < p < 0.01. ** p < 0.01.

2.2.4. Guild structure Differences between canopy and understory in the mean number of individuals and species of the four main saproxylic trophic groups were tested with the same method as the one used for the whole assemblage (paired Wilcoxon signed-rank tests or Tukey comparison of means in Generalized Linear Models). Analyses were carried out in R (R Development Core Team, 2008) or in Splus 7.0. 3. Results An overview of beetle samples is given in Table 1. 3.1. Canopy vs. understory flying saproxylic beetles in mountain beech-fir forests In beech-fir stands, the mean activity-abundance and the mean species richness per sample as well as the cumulative species richness (value interpolated by rarefaction) were greater in the understory than in the canopy. We also determined that detection probability was higher in understory samples (Table 2). The proportion of unique species in understory samples was more than twice as high as in canopy samples (Table 2). Though untestable, paired dissimilarity between canopy and understory for beetles trapped in beech-fir stands was high. Spatial turnover was the dom-

inant underlying process in the community divergence between understory and canopy – not nestedness (Table 2). The nestedness component was low. Therefore, species-poor canopy assemblages were not nested subsets of species-rich understory assemblages; on the contrary, they harbored specialist taxa. This result agrees with the limited overlap of shared species (18% of the observed species). Nonetheless, in accordance with the lower proportion of unique species in the canopy (24%), understory samples harbored more indicator species than canopy (Table 3). From IndVal results, only Xestobium plumbeum significantly preferred the canopy. No species showed changes in stratum preference according to the season in our dataset. The comparison of understory and canopy samples for each trophic group showed significant differences in guild structure (Fig. 1). More mycetophagous and xylophagous beetle individuals and species were caught in the understory. Similarly, predator beetles were more species-rich in understory samples. The number of saproxylophagous species and individuals was the same in canopy and understory samples. 3.2. Canopy vs. ground saproxylic beetles in pine deadwood Canopy pine limbs provided more beetle individuals than ground-lying pine branches, but an equal species richness per trap and an equal cumulative richness were observed in canopy and understory (Table 2). Only 15% of the species were shared by both strata, and assemblage composition differed significantly between

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Table 3 Characteristic species, determined by the IndVal approach. Only species significant at both permutation tests, with an indicator value higher than 25%, sampled in more than 3 traps and with more than 10 individuals were selected. Canopy

Forest floor

a

a

Xestobium plumbeum (Ill.) – Anobiidae

Cartodere nodifer (Westwood) – Latridiidae Enicmus testaceus (Stephens) – Latridiidae a Grynobius planus (F.) – Anobiidae a Hemicoelus costatus (Aragona) – Anobiidae a Idolus picipennis (Bach) – Elateridae a Mycetina cruciata (Schaller) – Endomychidae a Ptilinus pectinicornis (L.) – Anobiidae a Rhinosimus ruficollis (L.) – Salpingidae a Taphrorychus bicolor (Hbst) – Scolytinae a Xylophilus corticalis (Paykull) – Eucnemidae a

Window-flight trapped beetles Beech-fir mountain forests

Reared beetles Oak branches

Reared beetles Pine branches a

Aspidiphorus orbiculatus (Gyll.) – Sphindidae Bryaxis curtisii (Leach) – Pselaphinae Ennearthron cornutum (Gyll.) – Ciidae a Orchesia undulata Kraatz – Melandryidae Orthocis festivus (Panzer) – Ciidae a Proteinus brachypterus (F.) – Staphylinidae Rhizophagus bipustulatus (F.) – Monotomidae Trypodendron signatum (F.) – Scolytinae Xyleborinus saxesenii (Ratzeburg) – Scolytinae Xyleborus dryographus (Ratzeburg) – Scolytinae

Dromaeolus barnabita (Villa) – Eucnemidae a Anaspis humeralis (F.) – Scraptiidae a Cartodere nodifer (Westwood) – Latridiidae a Cryptolestes duplicatus (Waltl) – Laemophloeidae Cryptophagus dentatus Hbst – Cryptophagidae a Dasytes aeratus Stephens – Melyridae Phymatodes testaceus (L.) – Cerambycidae

a

a

a

Orthotomicus erosus (Wollaston) – Scolytinae Pityogenes trepanatus (Nördlinger) – Scolytinae Pityogenes bidentatus (Hbst) – Scolytinae

Atheta amicula (Steph.) – Staphylinidae

a

IndVal combining fidelity (frequency of occurrence) and specificity (abundance); other species: IndVal based upon specificity (abundance) only.

canopy and understory (Table 2). Since spatial turnover was the major underlying process in the community divergence between understory and canopy, canopy assemblages were not nested subsets of understory assemblages; on the contrary, they harbored specialist taxa (Table 2). Canopy and understory data showed the same proportion of unique species (around 40%). Slightly more indicator species were detected in pine limbs in tree crowns than in ground-lying branches. Nonetheless only three scolytid species significantly preferred the canopy (Table 3). We demonstrated significant differences in abundance but not in species richness for trophic guilds between understory and canopy samples (Fig. 1). More mycetophagous beetle individuals were caught in the understory whereas xylophagous beetles were slightly more abundant in canopy deadwood. Pine data did not show any differences for zoophagous and saproxylophagous beetles.

3.3. Canopy vs. ground saproxylic beetles in oak deadwood In oak branches, both the highest cumulative species richness and the highest abundance were observed in ground samples (Table 2). The mean species richness per sample was slightly lower in the canopy than in the understory. Despite a high proportion of shared species between canopy and understory (31%; Table 2), assemblage composition differed significantly between canopy and understory (Table 2). Canopy assemblages were not nested subsets of understory assemblages, and they showed seven IndVal characteristic species. Exclusive canopy species accounted for 21% of the species. However the proportion of unique species in understory samples was more than twice as high as in canopy samples (Table 2). In agreement with this result, understory samples harbored more indicator species than canopy (Table 3). The comparison of understory and canopy samples for each feeding guild showed significant differences (Fig. 1). More mycetophagous beetle individuals and species were caught in the understory. Similarly, predator beetles were slightly more abundant in understory oak samples. Inversely more saproxylophagous (but not xylophagous) species and individuals were caught in canopy samples.

3.3.1. Variability in species preferences IndVal results evidenced the variability in species preferences (Table 3). Indeed, Cartodere nodifer was significantly characteristic of understory deadwood in beech-fir stands, but of canopy deadwood in the oak data. In a broader perspective, among the 35 species collected in more than one of the three datasets (including singletons), 74% had a similar (but untested) stratum preference in samples. Among the canopy-preferring species were Anaspis maculata, Anaspis humeralis, Abdera biflexuosa, Calambus bipustulatus, Dasytes aeratus, Litargus connexus. The following species showed divergent preferences in the two datasets concerning deciduous tree species: Melasis buprestoides and Corticarina fuscula were canopy-preferring in beech window-flight trap data, but groundpreferring in oak emergence traps, whereas Cerylon ferrugineum, Dacne bipustulata, C. nodifer, Enicmus rugosus, Anaspis garneysi, Anaspis lurida and Leiopus nebulosus were ground-preferring in beech data, but canopy-preferring in oak data. No divergence in preference was observed between broadleaf and conifer data. 4. Discussion 4.1. Is the bulk of saproxylic beetle diversity mainly supported by one stratum? Our study provided contrasting results regarding the contribution of each stratum to forest biodiversity. Whereas higher abundance, cumulative and mean richness were apparent in understory samples in beech-fir stands and in oak branches, no differences for species richness – or even the opposite pattern for abundances – were observed in pine branches. Nevertheless, we demonstrated in beech-fir stands that the detection probability was lower for canopy than for understory data. Biodiversity may therefore be underestimated in the canopy. For insects in general, and saproxylic beetles in particular, we summarize the published findings on the density of insect individuals or species in understory vs. canopy in temperate or boreal forests in Table 4. Actually, the literature related to standing deadwood and saproxylic beetles is mainly composed of studies dealing with high stumps (e.g. Jonsell

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Fig. 1. Guild structure: differences in mean number of individuals and species of the four main saproxylic trophic groups between canopy (C) and understory (U). Differences were statistically tested using paired Wilcoxon signed-rank test for beech-fir data, and multiple comparison of means (Tukey contrasts) in a Generalized Linear Model with a Poisson structure. From top to bottom: abundance (left) and richness (right) of saproxylic beetle trophic groups in: (a) beech-fir forests, (b) oak branches, (c) pine branches. Myc: xylo-mycetophagous, saproxylo: saproxylophagous, xyl: xylophagous, zoo: predator. Saproxylophagous beetle abundance and richness in pine branches was not testable. Box plots show the spread of data, with upper and lower extremes (max-min), and 2 areas filled with black or grey above and below the median line for upper and lower quartiles.

and Weslien, 2003) or the lower parts of snags and standing dead trees (Jacobs et al., 2007). We have to be aware that beetle sampling at the upper level was generally operated at breast height (e.g. 1.5 m, sometimes 2 m). If these studies referred to vertical comparisons, they were limited to a ground-understory comparison. In order to be coherent, we decided to allude here mainly to studies concerning a stratum comparison with upper vertical levels above the breast height (entire snags, entire dead trees, crown part of tall snags, etc.; Hammond et al., 2004; Hedgren and Schroeder, 2004; Kappes and Topp, 2004; Ulyshen and Hanula, 2009; Foit, 2010). Results from recent literature are very disparate, depending on forest type, insect group or even sampling method. The highest abundance occurred in the elevated stratum in Hirao et al. (2009) and Hammond et al. (2004), near the ground in Preisser et al. (1998) and Manak (2007) or was comparable in Ulyshen and Hanula (2007). What is more, species richness peaked in the canopy for Schroeder et al. (2009) and Kappes and Topp (2004), at low levels for Hammond et al. (2004), Vodka et al. (2009), Ulyshen and Hanula (2009) and Foit (2010) and was equivalent in the two strata

for Ulyshen and Hanula (2007) and Hirao et al. (2009). Notwithstanding forest type or insect group, no obvious trend could be inferred. From a conservation viewpoint, some European studies showed a higher number of read-listed species in upper than lower vertical levels (Jonsell and Weslien, 2003; Kappes and Topp, 2004; Sverdrup-Thygeson and Ims, 2002). 4.2. Are canopy assemblages only nested subsets of understory assemblages? The effect of vertical stratification on assemblage composition was significant in oak and pine branches, as well as in beech-fir stands. Nonetheless, contrasting responses were found in the literature for community divergence between canopy and forest floor (Table 4). A significant inter-strata dissimilarity was revealed for beetles (Ulyshen and Hanula, 2007), saproxylic beetles (Hammond et al., 2004; Schroeder et al., 2009; Foit, 2010), bugs (Goßner, 2009) and parasitic wasps (Pucci, 2008). However, Müller and Goßner (2010) demonstrated a low beta diversity of saproxylic beetles

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Table 4 Bibliographic compilation of results comparing the density of insect individuals or species and the species composition in understory vs. canopy in boreal or temperate forests. Parameter

Abundance

Understory/ground vs. canopy

Insect group

Temperate forest type

References

Understory < canopy

Saproxylic Buprestidae Saproxylic beetles Beetles Saproxylic Buprestid Agrilus planipennis Saproxylic beetles (Scolytinae) Beetles

Pine, spruce and deciduous forests (Switzerland) Boreal aspen forests (western Canada) Cool-temperate deciduous forest (Japan) Ash woodland (USA)

Wermelinger et al. (2007) Hammond et al. (2004) Hirao et al. (2009) Francese et al. (2008)

Pine, spruce and deciduous forests (Switzerland)

Wermelinger et al. (2007)

Understory = canopy

Deciduous forest (USA)

Ulyshen and Hanula (2007)

Understory > canopy

Saproxylic beetles Saproxylic Cerambycidae Saproxylic Cerambycidae

Norway spruce forest (Sweden) Maple and pine forest (Canada) Pine, spruce and deciduous forests (Switzerland)

Manak (2007) Vance et al. (2003) Wermelinger et al. (2007)

Understory < canopy

Saproxylic Buprestidae Saproxylic beetles Flying beetles

Pine, spruce and deciduous forests (Switzerland) Broadleaved forest (central Europe) Beech-maple forest (Canada)

Wermelinger et al. (2007) Kappes and Topp (2004) Schroeder et al. (2009)

Understory = canopy

Saproxylic Cerambycidae Saproxylic beetles (Scolytinae) Beetles Beetles

Maple and pine forest (Canada) Pine, spruce and deciduous forests (Switzerland)

Vance et al. (2003) Wermelinger et al. (2007)

Deciduous forest (USA) Cool-temperate deciduous forest (Japan)

Ulyshen and Hanula (2007) Hirao et al. (2009)

Saproxylic beetles Saproxylic beetles Saproxylic beetles

Manak (2007) Hammond et al. (2004) Ulyshen and Hanula (2009)

Xylophagous beetles Xylophagous beetles Beetles Saproxylic Cerambycidae

Norway spruce forest (Sweden) Boreal aspen forests (western Canada) Pine-dominated and bottomland hardwood forests (southeastern USA) Oak woodland (Czech republic) Scots pine forest (Czech republic) Norway spruce plantation (Denmark) Pine, spruce and deciduous forests (Switzerland)

Beetles

Deciduous forest (USA)

Ulyshen and Hanula (2007)

Xylophagous beetles Saproxylic beetles Saproxylic beetles

Scots pine forest (Czech republic) Boreal aspen forests (western Canada) Beech-maple forest (Canada)

Foit (2010) Hammond et al. (2004) Schroeder et al. (2009)

Low Beta diversity among vertical strata

Saproxylic beetles

Various ecological forest types in southern Germany

Müller and Goßner (2010)

40% 24%

Beetles Saproxylic Cerambycidae

Deciduous forest (USA) Maple and pine forest (Canada)

Ulyshen and Hanula (2007) Vance et al. (2003)

Canopy = 29% Ground = 31%

Beetles

Deciduous forest (USA)

Ulyshen and Hanula (2007)

Canopy = 30% Ground = 46%

Saproxylic Cerambycidae

Maple and pine forest (Canada)

Vance et al. (2003)

Species richness Understory > canopy

Significant inter-strata dissimilarity Species composition

Shared species

Unique species

among vertical strata. They concluded that, for most species, movement from the ground to the canopy, by flying or by climbing the stems, is not limited. Regarding this point, divergence in community response may be partly caused by the sampling method. In our results, canopy–ground dissimilarity was lower in trap data than in emergence data. Indeed, window-flight traps sample dispersing individuals, which may be flying far away from their larval substrate. However, in our data, each stratum harbored specialist taxa, and canopy assemblages were not nested subsets of species-richer ground assemblages. The dissimilarity partitioning and the amount of unique canopy species suggest that the arboreal saproxylic beetle community is not just a random subset of the forest floor assemblage. In previous studies dealing with exclusive canopy species, we did not find any statistical results on nestedness. In addition to strong canopy–ground differences in beetle species composition, there were some canopy–ground differences among feeding guilds. But similarly to Hammond et al. (2004), our study found no strong consistent evidence for the vertical strat-

Vodka et al. (2009) Foit (2010) Reddersen and Jensen (2003) Wermelinger et al. (2007)

ification of beetle feeding guild assemblages. Our guild groupings may have been too coarse to detect fine-scale differences. Resource differences between the canopy and the ground are subtle, and therefore are only detectable for fine-scale autecological data (feeding guild and substrate preference). Nonetheless, saproxylophagous beetles were more species-rich and abundant in canopy samples for oak, but not beech or pine. In Swedish oakwoods, Franc (2007) also found fewer secondary wood boring species on lying logs than on standing deadwood (at breast height). In agreement with data from Hammond et al. (2004) in Canadian aspen forests, predator abundance tended to be slightly higher in our understory oak samples than in canopy samples. Besides more mycetophagous beetle individuals and species were detected in the understory (except in pine samples for species richness). Similarly, traps on lying oak deadwood, compared to traps on standing dead wood, had more fungivores species in southern Sweden (Franc, 2007). Distribution patterns of host substrate play a crucial role for mycetophagous beetles. With respect to temperature and relative humidity, marked differences in fungal

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communities exist between forest floor and upper canopy layers (Unterseher and Tal, 2006). Specific fungi (Boddy and Rayner, 1982) are linked with drier and more slowly decaying deadwood on attached branches (Jomura et al., 2008). 4.3. Stratum specialists, canopy-preferring species and canopy–ground environmental contrasts In accordance with the higher proportion of unique species at low level, understory samples harbored more indicator species than canopy ones (except for pine data). However, some beetle taxa were consistently restricted to the higher traps in our pine, oak and beech-fir samples. Overall, exclusive canopy species accounted for 20–40% of all species. This slight variation in the proportion of species exclusive to canopy in our three datasets is consistent with values in the existing literature (Table 4). In North American forests, Vance et al. (2003) and Ulyshen and Hanula (2007) found that about 30% of the beetle species were unique to canopy traps. Moreover several studies also found characteristic species in upper vertical levels (Hammond et al., 2004), e.g. in the crown section of snags (Kappes and Topp, 2004; Ulyshen and Hanula, 2009). The habitat preferences reported here may be driven by particular microhabitat requirements and availability of food resources (Basset et al., 2003), and/or by other non-resource-based factors, such as microclimate preferences, competition and predator avoidance (Grimbacher and Stork, 2007). First, the canopy–ground habitat dissimilarity obviously relates to the distribution pattern of deadwood micro-habitats. In the canopy, a large variety of resources associated to tree age and architecture are available to saproxylic insects in the form of decaying wood in the top of standing dead or moribund trees, snag tops, attached dead branches resulting from crown retrenchment, windstorm damage, snow break, pest attacks in the top of living trees, high tree holes formed in branch crotches in which debris accumulate and compost (with or without vertebrate nests). The forest floor also harbors specific deadwood features, such as stumps, uprooted trees, ground lying boles and logs, low cavities with mould, specific fungi and epiphytes associated to sheltered and humid deadwood and very rotten wood (absent in the canopy). Since many saproxylic beetles are closely connected to a specific micro-habitat, these disparities should deeply impact the vertical stratification of the saproxylic fauna (Alexander, 2008). Secondly, microclimate shows vertical stratification within temperate forests, since the canopy is exposed to more solar radiation, experiences much stronger wind velocities and temperature extremes, and is consequently much more unstable and less humid than the ground (Parker, 1995). Such vertical gradients in temperate forests depend on tree species (Canham et al., 1994) and could partly explain a tree-dependent variation in canopy–ground contrasts. Such abiotic gradients select for species that prefer open conditions (Manak, 2007), that need higher subcortical temperatures for larval development or that have greater desiccation resistance in the canopy. Differences between species in flying height are known to be influenced by wind speed gradients. Microclimate also impacts the vertical distribution pattern of fungi (see above) and flowers, a complementary resource for many saproxylic insect adults. Thirdly, species interactions may also have structuring effects. On the one hand, zoophagous saproxylic beetles depend on the distribution pattern of their potential prey, e.g. insect larvae or mites whose arboreal assemblages are distinct from those on the forest floor (Lindo and Winchester, 2006). On the other hand, the pressure of predators (spiders, birds) and parasitoids on saproxylic species may be distinct between canopy and understory. Concerning spiders, Larrivée and Buddle (2009), Hövemeyer and Stippich

(2000) demonstrated that the composition of canopy and understorey assemblages differed significantly. Earlier studies suggest a significant top-down impact of vertebrate predators on arboreal arthropods in canopy food webs (Gunnarsson and Hake, 1999). As far as we know, distinct parasitoid wasp species assemblages may have a driving pressure on their host assemblage (Vance et al., 2007; Pucci, 2008). Moreover beetle preferences also reflect competitive interactions among species. For example, Safranyik et al. (2000) demonstrated height segregation among five bark beetle species in lodgepole pines. 4.4. Consistency of species preferences The response of some indicator canopy species was consistent with the preference reported in recent ecological studies in Western and Central Europe; Phymatodes testaceus and A. humeralis (Alexander, 2002), D. aeratus (Stork et al., 2001) are known to develop in the dead branches of various broad-leaved trees. What is more, untested canopy-preferring species A. maculata (oak, beech and pine) and A. biflexuosa (oak and pine) generally develop on lower dead oak branches which have been shaded out by the tree’s own canopy (Stork et al., 2001; Alexander, 2002, respectively). IndVal results also highlighted the variability of species preferences and their ecological plasticity. Indeed, not many species had a significant stratum preference. Common species, known as canopy-taxa in the literature, such as Agrilus sp. (Alexander, 2002), Malthinus sp., Malthodes sp. (Paviour-Smith and Elbourn, 1993; Simandl, 1995), Mesosa nebulosa (Alexander, 2008) were not detected in our study. Moreover, some had divergent preferences among our datasets (e.g. C. nodifer), or responses unconsistent with the ecological literature; Orchesia undulata, Ptilinus pectinicornis, Taphrorychus bicolor are canopy-associated taxa in the literature (Alexander, 2002; Wermelinger et al., 2007, respectively), but characteristic of the forest floor in our broadleaf data. C. nodifer may possibly be a species with a multi-stratum ecology, i.e. larval development in the canopy and adult understory flight. A famous reverse example is the longhorn beetle Akimerus schaefferi, whose adults are known to have canopy habits, whereas larvae develop in the ground (Büssler, 2000). Nevertheless, in a broader perspective, 3/4 of the species collected in more than one of our three datasets had a similar (but untested) stratum preference. Obviously, some insects permanently inhabit the canopy, whereas other species are only temporarily arboreal during certain phases of their life cycle, for hibernation or foraging, for example (Barnard et al., 1986; Thunes et al., 2003). 5. Conclusion As a conclusion, our analysis of species richness and assemblage composition reveals significant between-strata differences. Lowman’s hypothesis of the predominance of ground-based assemblages in temperate forests was validated for saproxylic beetles in oak and beech-fir forests. For beetle assemblages associated to pine branches, the hypothesis of an equal contribution of ground and canopy strata (Hirao et al., 2009) cannot be rejected, since canopy samples harbored as many indicator and exclusive species as ground samples. Nonetheless, in our study on oak deadwood, stratum was the describing factor of deadwood pieces with the lowest contribution to global inertia of ordinated assemblages, in contrast with size or decay class (unpubl. data). Previous studies also demonstrated that vertical stratification is a less important factor for the local saproxylic beetle diversity than sun exposure (Vodka et al., 2009) or horizontal distribution of microhabitats (Müller and Goßner, 2010),

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for example. Even though it is not the main driver, the “suspended, standing or fallen” characteristic of timber makes a significant difference for saproxylic beetles (see Jonsell and Weslien, 2003). Moreover, it is known as a conditioning factor in the occurence of some specialist species (Ulyshen and Hanula, 2009). Our results confirmed that suspended dead branches cannot provide an alternative breeding substrate for all the species that reproduce in small and mid-size logs. They constitute a significantly different substrate than lying logs. In case of intensive log harvesting (for fuelwood for instance), many of the species will not have an alternative substrate in aerial deadwood. Our results also support temperate forest management practices which increase suspended deadwood and micro-habitats inside tree crowns. Several studies have evidenced quite lower quantities of deadwood in the canopy than on the forest floor (Norden et al., 2004). On 60 plots in both managed and unmanaged oak-hornbeam stands in the lowland state forest of Rambouillet (France), we calculated that perched deadwood (diameter > 10 cm) in large oak trees (DBH > 40 cm) represented 7% of the deadwood volume on average (mean = 4.3 ± 2.5 m3 /ha; unpublished data). As aerial deadwood is valuable habitat, its removal should only be specified where a threat to tree stability or public safety occurs. Second, our results lend support to the recommendation of a multi-strata sampling strategy when studying forest insect fauna (Su and Woods, 2001). To measure the effects of local management within sites, it could be very important to consider the canopy, because canopy composition differs from lower strata (Müller and Goßner, 2010), especially in forests with varied vertical structures. How forest management affects canopy assemblages remains largely unknown (Bail and Schmidl, 2008). Finally, oversimplifications and limitations in our sampling design must be pointed out. Further factors should be investigated: (i) more detailed vertical stratification (Goßner, 2009), (ii) stand density, since it impacts the flying strategy inside the canopy (Su and Woods, 2001), (iii) stand maturity, since tree ageing induces fundamental changes in tree micro-habitats in the canopy (no overmature stands were included in our study design), (iv) focused sampling on specific micro-habitats within the canopy, and (v) despite our non-significant preliminary results, seasonal migrations from canopy to ground, and reciprocally (Ulyshen and Hanula, 2007; Schmidl and Bussler, 2008). Ecological research in temperate forest canopies is recent and still mainly descriptive. As the methods for canopy access improve, more rigorous hypotheses-driven field studies will remain a priority of this new discipline (Lowman and Wittman, 1996). Canopy–ground relationships regarding substrate colonisation may be an interesting field of research, along with top-down processes, e.g. the influence of the initial decay of dead branches in the canopy on the colonization of fallen deadwood by saproxylophagous species (Fonte and Schowalter, 2004). Erwin (1983).

Acknowledgments We thank Benoit Nusillard, Carl Moliard, Lionel Valladares, Xavier Pineau, Charles Ricou, Eric Guilbert and Guilhaume Gautier for their technical assistance, Hervé Jactel for his advice, Heinz Büssler and Jiri Schlaghamersky for helpful discussion, and Victoria Moore for checking the English language. We are also deeply grateful to two anonymous reviewers whose relevant comments helped to improve an earlier version of the manuscript. This research was supported by grant no. CV050000150 from the French GIP Ecofor. Considerable technical assistance was provided by the staff of the National Forest Office at the Rambouillet State Forest.

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