Effects of Habitat Structure and Lid Transparency on Pitfall ... - BioOne

SAMPLING

Effects of Habitat Structure and Lid Transparency on Pitfall Catches IAIN D. PHILLIPS1

AND

TYLER P. COBB2

Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E3, Canada

Environ. Entomol. 34(4): 875Ð882 (2005)

ABSTRACT We present a methodological study that aims to help placate some of the criticism surrounding the use of pitfall trapping for carabid beetles in ecological studies. Because pitfall trap catches are dependent on the activity of carabids and not solely on density, characteristics of the trap construction may inßuence the success of the trap in different habitat types. SpeciÞcally, traditional opaque wooden lids may change the temperature and sun exposure of a trap relative to its surroundings. These abiotic factors may vary with the vegetation structure present around the trap. Thus, traditional opaque lids may offer a shade refuge in low vegetation habitats. We hypothesized that a change in microclimate associated with lid transparency would alter the behavior of ground beetles and thereby lead to a bias in trap catch results. To test this hypothesis, we performed a replicated, two-factor experiment manipulating lid transparency (opaque, partially transparent, and completely transparent) and vegetation height (⬎2, 1, ⬍0.5 m) around 27 pitfall traps. Soil temperatures beneath each lid varied signiÞcantly with lid transparency and vegetation height. There was no effect of either treatment on carabid species richness, whereas species assemblages varied signiÞcantly with respect to vegetation height but not lid transparency. However, total carabid catch rates and overall carabid species composition varied signiÞcantly with vegetation height but not lid transparency. Therefore, our results show that lid transparency does not bias carabid beetle catch and lend support to the use of pitfall trapping to assess the effects of habitat change on epigaeic communities. KEY WORDS pitfall traps, carabid beetles, sampling methods, boreal forest

AS ANTHROPOGENIC DEMANDS FOR natural resources continue to pressure boreal forests, a sound method of determining the ecological impact of such activities is of crucial importance. Arthropods are commonly used as ecological indicators because they comprise ⬎80% of the worldÕs species richness (Wilson 1992) and they respond quickly to habitat changes because of short generation times (see Work et al. 2002) and microclimate sensitivity (Niemela¨ 1997). Furthermore, several arthropod taxa, especially beetles and spiders, have been shown to be useful indicators in studies aimed at improved understanding of the ecological effects of forest harvesting (Niemela¨ et al. 1993, Buddle et al. 2000). Ground beetles (Coleoptera: Carabidae) are perhaps the most widely used arthropod group for this sort of research because they are diverse (⬇40,000 spp.), abundant in virtually all terrestrial habitats, well known taxonomically, and seem highly sensitive to habitat changes (Refseth 1980, Niemela¨ et al. 1988, 1990, 1992, 1993, Niemela¨ 1990, 1997). However, widespread use of carabids as indicators of ecological impact hinges on the ability of researchers to accurately sample and compare their populations across a range of varying habitat conditions. 1

Corresponding author, e-mail: [email protected]. Department of Renewable Resources, University of Alberta, Edmonton, Alberta T6G 2E3, Canada. 2

One of the principal methods for sampling carabid communities is with pitfall traps. Pitfall traps are typically open containers dug into the ground, ßush with the surface of the substrate they are sampling, and generally possess an opaque lid designed to keep debris, larger vertebrates, and excess rainwater from entering the trap (Spence and Niemela¨ 1994). Because of their simplicity, pitfall traps are inexpensive to construct and can be easily deployed in almost any terrestrial habitat. Furthermore, these traps generally yield large catches of carabids that provide data sets large enough for rigorous statistical analysis. Numerous studies have investigated the virtues of sampling ground-dwelling arthropods with pitfall traps (see Greenslade 1964, Luff 1975, Adis 1979, Southwood 1994) and suggest that a variety of factors must be taken into consideration when interpreting the data they generate. In general, the efÞciency of this sampling method depends on population density (Baars 1979, Work et al. 2002), arthropod activity (determined to a large extent by climatic conditions and habitat structure; Mitchell 1963, Greenslade 1964), and trap design characteristics (e.g., Spence and Niemela¨ 1994, Vennila and Rajagopal 2000, Work et al. 2002). Most studies of pitfall trap design have focused on trap diameter (Abensperg-Traun and Steven 1995, Work et al. 2002, Koivula et al. 2003), construction material (Luff 1975, Waage 1985), pre-

0046-225X/05/0875Ð0882$04.00/0 䉷 2005 Entomological Society of America

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servative (Lemieux and Lindgren 1999, Waage 1985, Koivula et al. 2003), or the type of trap used (Luff 1975, Curtis 1980, Bostanian et al. 1983, Halsall and Wratten 1988, Spence and Niemela¨ 1994, Buddle and Hammond 2003). Work et al. (2002) compared the effect of varying lid and trap sizes on catches of beetles and spiders and found that the differing lid sizes had no signiÞcant difference in carabid catch rate or species richness. Other than lid size, however, characteristics of the lid such as transparency have been largely ignored. Comparisons of community parameters between habitats are difÞcult to make unless one can account for certain site- and trap-speciÞc factors that may bias or otherwise inßuence the catch. Most studies attempt to avoid this criticism by taking care to deploy identical traps in all study sites. However, for studies to compare trap catches in locations with differing habitat characteristics (as is the case in most studies), a critical assumption is that the biases are the same between those habitats (Melbourne 1999). Under this assumption, there would be no difference in sampling efÞciency between traps in open locations relative to those in vegetated habitats. Presumably there are inherent differences in the abundance, species richness, and species composition of carabid communities between two habitats that have a distinct contrast in epigaeic habitat structure; however, it is important that the differences in data collected are in fact representative of the true community and not an artifact of trap characteristics under the conditions of the habitat treatment. For example, the presence of an opaque lid may offer a shade refuge for carabids in habitats with increased exposure and thereby bias trap catch results in studies aimed at comparing carabid communities between open (e.g., clear-cut harvested forest) and more closed (e.g., unharvested forest) habitats. Because pitfall trapping is one of the principal methods for carabid data collection in boreal forest habitat studies of Western Canada (e.g., Holliday 1991, 1992, Niemela¨ et al. 1993, Spence et al. 1996, Buddle et al. 2000), it is important that we understand where biases in this method of sampling may exist to correct our interpretation of the data or perhaps control for these problems. Here we studied the inßuence of lid characteristics and vegetation structure on carabid samples obtained by pitfall trapping in a disturbed boreal forest setting. SpeciÞcally, we assessed the effect of lid transparency and vegetation height on overall carabid abundance, species richness, and species composition to test the hypothesis that a change in microclimate associated with lid transparency in varying habitats would alter the activity of ground beetles and thereby lead to a bias in pitfall trap catch results. Materials and Methods Site Description. This experiment was conducted during the summer of 2003 ⬃300 km northwest of Edmonton, Alberta, Canada. The site (55⬚06⬘ N, 114⬚18⬘ W) was a former white-spruce [Picea glauca

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(Moench) Voss.]Ðtrembling aspen (Populus tremuloides Michx.) mixedwood boreal forest stand that was clear-cut harvested in 1998 and subsequently burned during a large-scale (⬃120,000 ha) wildÞre that occurred during the spring of 2001. Devoid of most debris, the soil cover is primarily successional vegetation consisting largely of regenerating trembling aspen along with patches of raspberry (Rubus idaeus L.) and various grasses. The site was selected on the basis of little variation in slope and relatively uniform vegetation height. At the time of the experiment (i.e., 2 yr after the Þre), regenerating trembling aspen had reached a height of ⬇2 m. Sampling Protocol and Experimental Design. Carabids were sampled with pitfall traps constructed from 1-liter clear yogurt tubs, with a tight Þtting inner cup, identical to those used in other boreal forest arthropod studies (Niemela¨ et al. 1986, 1988, 1990, 1992, 1993, Holliday 1991, 1992, Spence and Niemela¨ 1994, Digweed et al. 1995, Niemela¨ and Spence 1999, Buddle et al. 2000, Gandhi et al. 2001, 2004, Buddle and Hammond 2003, Work et al. 2004). Traps were embedded in the ground so the lip of the trap remained ßush with the substrate surface. Traps were Þlled with 2Ð3 cm of silicate-free ethylene glycol (GM Dex-Cool, Oshawa, Ontario, Canada) as preservative and covered with a 15 by 15-cm lid (described below) elevated 2Ð5 cm above the trap by two nails placed in opposite corners. Lids are necessary to reduce ßooding and accumulation of leaves and litter in the preservative (Work et al. 2002). We compared the performance of three different degrees of transparency of lids over pitfall traps operating under three levels of vegetation height. Degrees of lid transparency were established as follows: opaque (15 by 15-cm piece of plywood that is the lid type used in most studies), partially transparent (15 by 15-cm piece of plywood with holes allowing 50% transmittance of light and covered with a piece of Plexiglas), and transparent (a 15 by 15-cm piece of Plexiglas). Vegetation cover was manipulated based on the experiment of Melbourne (1999), which involved three levels of habitat structure (high, medium, low), each created by modifying (or not modifying) the height of the vegetation. In a 2.5-m radius plot surrounding each trap, levels of vegetation height were maintained at ⬇2 (high), 1 (medium), and ⬍0.1 m (low). For the medium and low treatments, vegetation was cut to the desired height using a weed whacker at the beginning of the experiment and maintained by hand picking. The resulting nine lid transparencyÐvegetation height combinations were replicated three times and randomly assigned to 1 of 27 positions in a grid (Fig. 1). Each of the 27 traps in this grid was separated from a neighboring trap by 20 m to improve independence (Digweed et al. 1995). Carabids were sampled continuously for a total of 73 d (7 June to 19 August 2003), and each trap was emptied and recharged during four separate visits (⬇18-d intervals). Soil Temperature. To determine if lid transparency and habitat structure were having an effect on the

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PHILLIPS AND COBB: PITFALL TRAPPING

877

Fig. 1. Design of pitfall trap placement in the study area.

microclimate immediately surrounding the trap, we measured soil temperature at 1 cm depth beneath each lid immediately adjacent to the trap using pocket digital probe thermometer (Thermor Elco Brandt, Rueil Malmaison Cedex, France). Soil temperature measurements were recorded on three separate cloudless

days between 1200 and 1400 hours. No measurements were taken if the trap or lid had been disturbed. Species Identification. Pitfall samples were sorted in the laboratory, and all carabids were removed and subsequently identiÞed to species using Lindroth (1969). In total, 1,216 carabids representing 26 species

Table 1. Summary of ANOVA results for the effects of vegetation height (VEG) and lid transparency (LID) on mean soil temperature, Carabid catch rate, S. quadripunctata (DeGeer), and P. adstrictus Eschscholtz measured on 3 d Species Sericoda quadripunctata (DeGeer) Pterostichus adstrictus Eschscholtz Calathus advena (LeConte) Calathus ingratus Dejean Agonum cupreum Dejean Amara obesa (Say) Amara lunicollis Schiødte Syntomus americanus (Dejean) Harpalus laevipes Zetterstedt Bembidion mutatum Gemminger and Harold Calosoma calidum (Fabricius) Platynus decentis (Say) Bembidion grapii Gyllenhal Stereocerus haematopus (Dejean) Amara patruelis Dejean Harpalus somnulentus Dejean Agonum gratiosum (Mannerheim) Amara torrida (Panzer) Harpalus fulvilabris Mannerheim Agonum retractum LeConte Bembidion bimaculatum (Kirby) Cymindis cribricollis Dejean Synuchus impunctatus (Say) Amara littoralis Mannerheim Agonum placidum (Say) Amara quenseli (Scho¨ nherr) Total species Total abundance

High

Medium

Low

O

PT

T

O

PT

T

O

PT

T

20 16 6 4 0 0 0 0 1 1 0 2 3 1 0 0 0 0 2 1 0 0 0 0 0 0 11 57

11 19 10 4 0 0 0 0 0 0 1 4 1 2 1 0 0 0 0 1 0 0 0 0 0 0 10 54

19 33 10 18 1 0 1 0 3 0 0 1 1 1 0 2 4 0 0 0 0 1 0 0 0 0 13 95

50 42 7 1 1 1 1 0 0 1 1 0 1 0 0 2 0 0 0 0 0 0 0 0 0 0 11 108

84 84 3 2 0 3 0 3 0 0 2 0 1 1 4 0 0 0 0 0 0 0 0 0 0 0 10 187

35 60 6 1 2 0 3 0 0 1 0 0 0 1 1 1 0 0 0 0 0 0 0 0 0 1 11 112

175 49 8 0 10 1 0 0 0 5 0 0 1 0 2 0 0 2 0 0 0 0 1 0 0 0 10 254

111 39 8 0 2 2 5 1 1 0 2 0 0 2 0 0 0 0 0 0 1 0 0 1 1 0 13 176

70 54 9 1 7 15 1 6 5 1 2 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 13 173

Total 575 396 67 31 23 22 11 10 10 9 8 8 8 8 8 5 4 3 2 2 1 1 1 1 1 1 26 1216

Data were log10-transformed before analysis to meet the assumptions of normality (Kolmogorov-Smirnov) and homoscedasticity (LeveneÕs test).

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Fig. 3. Mean carabid catch rate ⫾ SE (n ⫽ 3) in each lid transparency and vegetation height category. Fig. 2. Mean soil temperature ⫾ SE (n ⫽ 3) in each lid transparency and vegetation height category.

were collected over the course of the experiment (Table 1). Voucher specimens from this study are deposited in the Strickland Entomological Museum (University of Alberta) located in Edmonton, Alberta, Canada. Data Analyses. Two-factor analysis of variance (ANOVA) was used to test the effects of lid type and vegetation height on soil temperature, carabid catch rates (total individuals/trap-day), and species richness (SYSTAT v.9.0). Where necessary, data were log10-transformed before analysis to meet the assumptions of normality (K-S test) and homoscedasticity (LeveneÕs test). Nonmetric multidimensional scaling (NMS) was performed using the software package PCOrd (McCune and Medford 1999) to simultaneously examine the effects of lid transparency and vegetation height on carabid species composition. This analysis was performed using the “slow and thorough” autopilot feature in the software and the Sorensen (Bray-Curtis) distance measure. Table 2.

Results Soil Temperature. The treatment objective of changing the microclimate through varying lid transparency and vegetation structure was successful because soil temperatures measured at 1 cm depth beneath each lid varied signiÞcantly with both lid transparency and vegetation height (Fig. 2; Table 2). In general, areas with greater vegetation height had lower soil temperatures. However, in more open areas (low vegetation height), soil temperatures increased signiÞcantly with increasing lid transparency (Fig. 2; Table 2). Carabid Community. Although there seems to be a general trend of greater overall catch rates of carabids in traps with opaque lids in open areas (Fig. 3), this effect was not statistically signiÞcant (Table 2). Analyses of mean carabid catch rate data showed that there were greater mean catch rates of carabids in open areas (signiÞcant vegetation effect), but that this effect was not dependent on lid transparency (no signiÞcant lid type effect or vegetation X lid interaction; Table 2).

Total catch of carabid species by vegetation height treatment (high, medium, low) and pitfall trap lid transparency Variable

Soil temperature (1 cm depth)

Catch rate of carabid beetles (individuals/d)

Catch rate of S. quadripunctata (DeGeer) (individuals/d) Catch rate of P. adstrictus Eschscholtz (individuals/d)

O, opaque; PT, partially transparent; T, transparent.

Source of variation

df

MS

F

P

VEG LID VEG ⫻ LID Error VEG LID VEG ⫻ LID Error VEG LID VEG ⫻ LID Error VEG LID VEG ⫻ LID Error

2 2 4 70 2 2 4 18 2 2 4 18 2 2 4 18

0.07 0.012 0.005 0.002 0.606 0.007 0.083 0.061 0.963 0.102 0.048

29.82 5.3 2.27

⬍0.0001 0.0072 0.0697

9.98 0.12 1.37

0.0012 0.8907 0.2834

16.36 1.74 0.83

0.0001 0.2062 0.5292

0.491 0.031 0.052

12.3 0.78 1.29

0.0004 0.4748 0.3094

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Fig. 4. NMS ordination of trap level carabid beetle catch rates coded for vegetation height (a) and lid transparency (b).

Results of NMS ordination analyses of the effects of vegetation height (Fig. 4a) and lid transparency (Fig. 4b) on carabid species composition was similar to the effect on overall carabid catch rates (Fig. 3). Using species counts standardized for sampling effort (number of beetles per trap-day), NMS resulted in a two-dimensional solution (Þnal stress, 7.88) that explained 91% of the total variance. This analysis showed that, although there was considerable overlap in carabid species composition between the low and medium vegetation height treatments, areas with high vegetation supported a distinct assemblage. Also, there was little or no separation in species composition between opaque, transparent, and partially transparent lid types. These analyses suggest that vegetation structure alters carabid species composition, but that this effect is not dependent on the transparency of the lid above the pitfall trap. Finally, there was no effect of vegetation height or lid transparency on carabid species

richness as evident in the consistent carabid species catch across treatments (Table 1). Carabid Species Response. Sericoda quadripunctata (DeGeer) was the most abundant species, with 575 individuals (comprising 47% of the sample), whereas Pterostichus adstrictus Eschscholtz followed as the second most abundant species with 396 individuals (comprising 33% of the sample). Because these two species comprised the majority of the total catch of carabids and appeared to show some effect in their total catch (Table 1), we separated them out for further analysis (Fig. 5). However, they too had no signiÞcant response as a result of the type of lid used (Table 2). Discussion Carabids have been used extensively in biodiversity studies, and many of these studies have used pitfall traps to compare populations between different hab-

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Fig. 5. Mean catch rate ⫾ SE (n ⫽ 3) for the two most abundant carabid species in each lid transparency and vegetation height category.

itat types (see Holliday 1991, 1992, Niemela¨ et al. 1993, Beaudry et al. 1997, Hammond 1997, Buddle et al. 2000, Helio¨ la¨ et al. 2001, Cook and Holt 2005). Because the degree of exposure differs between habitat types, it is important to determine if this inherently inßuences the pitfall catch regardless of the treatment under study. For example, Niemela¨ et al. (1993) studied the effects of clear-cut forest harvesting on carabid community parameters using traditional pitfall trapping methods. Sites used in their study included Þve age categories since harvest. The regenerating sites were generally drier and more open than the shaded, structured, regenerated sites. Eighteen species of Amara, Bembidion, and Harpalus showed a marked increase in abundance after logging. Similar results that show a marked increase in carabids have been found after logging in Finland (Niemela¨ et al. 1988), Russia (Arnoldi and Matveev 1973), Poland (Szyszko 1983), and the United States (Jennings et al. 1986). One common criticism of these sorts of Þndings has been that increased catch of some species may have resulted from a bias related to the efÞciency of the pitfall trap and not a true representation of habitat preference. Our results lend additional support to these earlier Þndings because we found that vegetation height altered trap catch results regardless of lid transparency.

The ability to measure carabid community parameters using pitfall traps has been criticized in the past because of the seemingly innumerable variables that can alter the activity of the beetles and hence the number caught. Catches reßect the abundance of carabids in the habitat under study, their activity on the ground surface, and the capture efÞciency of the trap (Greenslade 1964, Kowalski 1975, Luff 1975, Uetz and Unzicker 1976, Curtis 1980, Topping and Sunderland 1992, Brennan et al. 1999). Despite the limitations of this method, pitfall traps also possess many favorable attributes such as continuous sampling, large sample sizes, little maintenance, and simultaneous sampling at numerous locations (Baars 1979, Topping and Sunderland 1992, Spence and Niemela¨ 1994, Brennan et al. 1999). Furthermore, no sampling method is completely without bias, and no trap has been developed that is as efÞcient and inexpensive as pitfall traps. Spence and Niemela¨ (1994) accurately pointed out that much of the knowledge compiled about carabid populations has come from the analysis of pitfall trap data. To completely discount pitfall trapping as a direct method of information gathering in population studies would be to remove a very simple and useful tool. Therefore, it is important that the variables biasing pitfall trap catches be understood and the in-

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terpretation of that data be adjusted for those variables. We sought to determine if opaque lids above pitfall traps offered a shade refuge when traps are placed in open areas (e.g., clear-cuts), thereby biasing pitfall trap catches in studies aimed at using pitfall traps to investigate the effects of vegetation structure on carabid beetles. In general, the data do not support this hypothesis. Although vegetation height and pitfall trap lid transparency altered soil temperature around pitfall traps, mean catch rates of carabid beetles and carabid species composition seem to be only affected by vegetation height. Furthermore, despite appearing to be inßuenced by lid type in their total catch (Table 1), the two most abundant species in the study (Sericoda quadripunctata (DeGeer) and Pterostichus adstrictus Eschscholtz) had no signiÞcant affect on their catch rate by the manipulation of lid type (Fig. 5). The data lend support to the use of pitfall trapping to monitor the effects of vegetation structure on ground beetles by showing that lid transparency does not bias carabid catch rates or species composition.

Acknowledgments We thank A. De´ cheˆ ne for Þeld assistance, G. E. Ball for taxonomic expertise, and J. R. Spence and W. H. Cook for numerous valuable comments and suggestions. Funding for this study was provided by the Foothills model Forest Chisholm-Dogrib Fire Research Initiative, Alberta Conservation Association supported Biodiversity Challenge Grant, and the Natural Science and Engineering Research Council.

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