Leaf-Litter Arthropod Community Structure and Abundance in a Recently Burned Montane Longleaf Pine Ridge
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1 Leaf-Litter Arthropod Community Structure and Abundance in a Recently Burned Montane Longleaf Pine Ridge Amy M. Waananen 1 and Grant L. Gentry 2, Ph.D. 1 St. Olaf College, Northfield, MN 55057; waananen@stolaf.edu 2 Department of Biology and Environmental Science, Samford University, Birmingham, AL 35229; ggentry@samford.edu ABSTRACT Arthropod populations relationship with fire is poorly understood due to highly variable responses in different ecosystems and conditions. The objectives of this study were to 1) evaluate the short-term impacts of prescribed burning on leaf litter arthropods in a longleaf pine ecosystem and 2) to determine the relative importance of environmental factors such as litter depth, moisture, or slope aspect on arthropod communities in areas that have undergone a prescribed burn. The study was carried out at Oak Mountain State Park in Pelham, AL where a section of historic longleaf pine forest had been burned three months prior. Pitfall traps and Berlese funnels were used to sample leaf-litter arthropods. Overall faunal, predatory, and detritivore population abundances were significantly higher in the unburned plots. Leaf litter depth and moisture covaried and were greater in the unburned plots. This evidence corroborates previous studies that suggest bottom-up limitation in detritus-based food webs impacts all trophic levels (Chen and Wise 1999) and other studies that shows decreased abundance after prescribed burning (Ferrenberg et al. 2006, Castano-Meneses and Palacios-Vargas 2002, Wikars and Schimmel). Further study is suggested to evaluate prescribed burning s impact on the arthropod biodiversity and to better understand fire dynamics in an infrequently burned system. Keywords: community ecology, leaf-litter arthropods, longleaf pine, prescribed fire INTRODUCTION Recent interest in restoring the longleaf pine ecosystem in Alabama has led to more discussion of using prescribed burning to maintain the species diversity unique to this ecosystem. The effect of fire on arthropod communities has been studied in a variety of contexts with conflicting results. This issue is particularly relevant in the endangered longleaf pine ecosystem of the Southeastern U.S. where the forests naturally undergo frequent low-intensity fires, but in the past century have been managed under a policy of fire suppression. The longleaf pine ecosystem is maintained by frequent surface fires (Abrams 1992, Brockway and Lewis 1996), where burning facilitates the success of the flame-resilient longleaf pine and wiregrass. Fire changes the structure and moisture of the leaf litter layer, decreasing organic material which serves as a resource for saprophagous animals. The availability of detritus has been shown to have bottom-up effects on organisms in higher trophic levels, such as Centipedes (Chilopoda), Pseudoscorpions (Pseudoscorpiones), and Spiders (Araneae) (Chen and Wise 1999). Thus, the scarcity of detritus after a burn may have limiting effects on the abundances of organisms in many trophic levels. Soil and litter arthropods play an important role in the regulation of soil nutrients in forest ecosystems through decomposition. Because the leaf-litter fauna influence the distribution of soil organic matter, aeration, and porosity of the soil, they affect forest productivity. This makes leaf-
2 litter arthropods useful as bioindicators of forest health, as demonstrated in studies on rainforest restoration (Nakamura et al. 2003), plantation forests (Bird et al. 1999, Maleque et al. 2009), urbanization (Gibb and Hochuli 2001), agriculture (Paoletti and Hassal 1999, Paoletti et al. 2007) and response to different fire regimes (Orgeas and Andersen 2001, Buddle et al. 2005, Andrew et al. 2000). Monitoring arthropod abundance is a useful measure in the evaluation of the impact of silvicultural techniques and the efficacy of forest restoration efforts such as prescribed burns. This study seeks to clarify how prescribed fire interacts with arthropod communities in longleaf pine ecosystems and to evaluate the impact of recent conservation efforts. The objectives of this study were to 1) evaluate the short-term impacts of prescribed burning on leaf litter arthropods in a longleaf pine ecosystem and 2) to determine the relative importance of environmental factors such as litter depth, moisture, or slope aspect on arthropod communities in areas that have undergone a prescribed burn. MATERIALS AND METHODS Study Site The study was carried out at Oak Mountain State Park in Pelham, AL on a recently burned ridge ( N, W) and an adjacent unburned ridge ( N, W). Both ridges are home to longleaf pine (Pinus palustris) stands mixed with several other species of pine and deciduous hardwood trees including the loblolly pine (Pinus taeda), shortleaf pine (Pinus echinata), American sweetgum (Liquidambar styraciflua), and several species of oak (Quercus). On both ridges, leaf litter consists of a mixture of pine straw and deciduous leaf matter, although the burn treatment left several patches of bare mineral soil. The ridges run from northwest to southeast, with the southeastern slope receiving more sunlight than the northwestern slope (Sheffield 2013). The burn site had undergone a prescribed burn on March 14, 2013 and previously in Invertebrate Sampling Methods Samples were taken from 4 randomly selected transects running over the top of the ridges in adjacent burned and unburned sites. Pitfall traps and Berlese funnels were used to sample the invertebrate leaf litter community of each study area. Previous studies have found these to be complementary sampling methods for invertebrate studies (Jimenez-Valverde and Lobo 2005, Sabu et al. 2009). Pitfall traps consisted of a cup with a 15 cm diameter containing 30 ml ethylene glycol buried such that the lip of the cup was flush with the ground. The cups were fitted with a funnel with a diameter of 15 cm at the top and 3.5 cm at the bottom. The traps were covered with a plastic rain cover, elevated 10 cm above the top of the cup. Pitfall traps were set out for three weeks. For the four randomly selected transects, six traps were placed every 15m along 90 m measured perpendicular to each side of the ridge at both the burned and unburned sites. Arthropods collected were identified to family or order and then sorted into trophic guild. Samples of arthropods were also collected using a Berlese funnel. Leaf litter samples were obtained by raking 0.5 m 2 plots from three evenly spaced locations on both sides of the ridge from the same transects selected for the pitfall traps. The Berlese funnels consisted of incandescent shop-lights above 5 gallon buckets fitted with a large funnel at the bottom. Foil was attached from the lamps to the buckets to direct heat into the leaf litter. A jar containing 3 cm of isopropyl alcohol was placed beneath the funnel to kill and preserve the specimen. Before placing the leaf litter samples in the Berlese funnels, the samples were sifted over a coarse mesh 166
3 (openings 2 cm 2 ). The small particles that fell through were returned to the top of the leaf litter, reducing the problem of having excess soil and debris falling into the collection jar. Specimens collected were sorted by order or family and into trophic guilds. Because orders such as Coleoptera and Diptera occupy several trophic levels, these were identified to family and then sorted accordingly to trophic level. The trophic levels included were macropredators (Araneae, Coleoptera: Carabidae, Histeridae, and Staphylinidae, Chilopoda, Diptera: Asilidae and Tachinidae, Formicidae, Scorpiones, Pseudoscorpiones, and Opiliones), detritivores (Acari, Blattodea, Collembola, Coleoptera: Silphidae and Scarabaeidae, Diptera: Mycetophilidae and Phoridae, and Orthoptera), and herbivores (Coleoptera:Chrysomelidae, Curculionidae, Elateridae, and Tenebrionidae, Diplopoda, Hemiptera: Cicadellidae, Hymenoptera: Apidae and Formicidae, Lepidoptera, Thripidae, and Thysanura). Acari and Collembola were only counted for the first two transects collected from pitfall traps. Thus, a separate macrodetritivore trophic grouping was also created, including the same orders and families as the detritivore category, but excluding Acari and Collembola. Note that ants, as generalist omnivores, are counted in both the predatory and herbivorous groups. Abiotic Factors Data on litter moisture, litter depth, and ridge aspect was collected at each sample site. Litter moisture was measured by taking 10 cm x 10 cm plots of leaf-litter sample directly adjacent to the 0.5 m x 0.5 m plots collected for sampling via Berlese funnels and at the locations of the pitfall traps. The litter obtained from the 10 cm x 10 cm plots was weighed, and then dried in an incubator overnight at 70 degrees Celsius. Moisture content was obtained from the difference in weight before and after drying in the oven. The litter depth of each sample site was measured at the four corners of the 0.5 m x 0.5 m plot and then averaged to give a reasonable estimate of overall litter depth. Ridge aspect was determined using a compass at each site. Statistical Analyses The data collected was analyzed using SPSS statistical software to perform univariate analysis of variance (ANOVA) to determine the relationship between burned and unburned and aspect (northwest-facing versus southeast-facing) with the overall abundance of the leaf-litter arthropods and of the abundance of specific orders. Ridge aspect, distance from the top of the ridge, and fire regime were fixed factors of the model and litter depth and moisture were included as covariates. Simple linear regression was used to determine the relationship between leaf litter depth and leaf litter moisture. RESULTS We collected 15,426 individual arthropods. The majority were Diptera (26.5%), Collembola (25.0%), Coleoptera (15.7%), Hymenoptera (13.5%), Acari (9.2%), Araneae (5.3%), and Orthoptera (4.5%). Several orders each made up ~1% of the total (Diplopoda (1.7%), Thysanura (1.4%), Hemiptera (1.2%), Chilopoda (0.8%)). A number of other orders were found in very small numbers (Blattodea, Mantodea, Psocoptera, Thripidae, Scorpiones, Pseudoscorpiones). The most abundant orders were analyzed if the counts satisfied parametric assumptions. Orders that satisfied these qualifications were: Acari, Araneae, Non-Predatory Coleoptera, Predatory Coleoptera, Collembola, Diptera, Hemiptera, Orthoptera, and Thysanura. 167
4 Abiotic Factors The unburned site s leaf litter had greater moisture content than the burned site (P < ). From 300 samples taken over the course of one month, the burn site s average moisture content was (SD ) while the unburned site s was (SD ). The unburned site also had deeper leaf litter than the burned site (P < ), where the average depth in the burn site was (SD ) and (SD 1.346). Leaf litter moisture and depth were positively correlated (R 2 = ) (Figure 1). Arthropod Abundance Arthropod abundance was higher in the unburned site than the burned site for overall fauna, macropredators, macrodetritivores, and four of the major orders studied (Acari, Collembola, Hemiptera, and Thysanura) (Table 1). This is illustrated by comparing the proportion of the major orders found in the burned site to those found in the unburned site (Figure 2). One deviation from this trend was seen in the Coleoptera, where 57.8% of all beetles were found in the burned site. Closer inspection of the order indicates that the Scarabaeidae family is responsible for the greater abundance of Coleoptera found in the burned site than the unburned (Figure 3). The overall trend that the proportion of individuals found was higher in the unburned carries over into categorizing the individuals by trophic level (Figure 4), where the proportion of all major trophic groups studied was higher in the unburned site than the burned. Although overall faunal abundance was not related to litter depth, individuals of several specific trophic groups and orders (Non-predatory Coleoptera, Collembola, Orthoptera, Macropredators), were found in greater numbers in deeper litter (Table 2). Macrodetritivores and Thysanura were more abundant in greater litter moisture (Table 3). Although Diptera abundance was not related to burn treatment, litter depth, or litter moisture, their populations were greater as the distance from the top of the ridge increased (ANOVA, 5 d.f., F = 2.406, P = 0.009) (Table 4). Total fauna collected from Berlese funnels (ANOVA, 11 d.f., F = 2.222, P = 0.048), macrodetritivores (ANOVA, 17 d.f., F = 2.075, P = 0.042), and macro non-predators (ANOVA, 17 d.f., F = 2.375, P = 0.02) also followed the trend of having increased abundance at increased distance from the top of the ridge (Table 4). DISCUSSION Results clearly show decreased abundance of total arthropod populations and most orders and trophic groups under the burned treatment, with notable exceptions including herbivores (Figure 3). Herbivores may deviate from the trend because of their indirect relationship to leaf litter for food. Detritivores depend directly on leaf litter and it s nutritive properties, while predators are similarly dependent, possibly for reasons of bottom-up control (Chen and Wise 1999) or structural complexity benefiting their hunting ability (Uetz 1976). Overall fauna, predators and detritivores were more abundant under the unburned fire regime, corroborating the evidence of many other studies on arthropod response to prescribed fire (Ferrenberg et al. 2006, Castano-Meneses and Palacios-Vargas 2002, Wikars and Schimmel). Litter moisture covaried with leaf litter depth (r 2 = 0.543). This follows results from previous studies that found that arthropod abundance is positively correlated with leaf-litter moisture (Schimel et al. 1999, Kaspari and Weiser 2000, Rainio and Niemela 2002). Litter complexity is also correlated with many species of arthropod abundance such as mites (Hansen and Coleman 1996), ants (Lassau and Hochuli 2004), and predatory macroinvertebrates such as spiders (Uetz 1976), due to having more access to hiding locations or points to build webs from 168
5 (Reichert and Gillespie 1986). Such studies suggest that as a result of fire s leaf litter removal one would see decreased population sizes of all trophic levels of leaf litter arthropods. This may suggest some explanation for the increased faunal abundance in the unburned site, which had deeper and moister leaf litter but is not sufficient to account for all of the observed variation. Although this study was not designed in such a way that allows for explicit differentiation of the nutritional properties and structural complexity of leaf litter, some inferences can be made. Leaf litter depth was related to both litter moisture and predator abundance, particularly for micropredators. This suggests that some combination of bottom-up resource abundance and structural availability of hunting and hiding locations led to greater abundance of predators. Leaf litter accumulation on the forest floor is important to arthropods for the structural complexity it provides as well as the resources of organic material and moisture. The data support that deeper leaf litter is correlated with greater leaf litter moisture. This relationship is particularly critical to detritivores and fungivores, whose relative benefit from the food resource is greater than that of predators. Thus, our results showing increased detritivore abundance in the unburned sites support the bottom-up relationship between availability of detritus with the abundance of higher trophic levels as asserted by Chen and Wise (Chen and Wise 1999). Although decreased arthropod abundance may be a useful indicator of disturbance in an ecosystem, it is important to note that this change is not necessarily positive or negative from an ecological standpoint. This study was not designed to assess arthropod diversity and thus lacks a measure of biodiversity that is critical in assessing whether silvicultural treatment benefited or harmed the arthropod community. Further studies are suggested to determine the level of diversity in the burned plot and also to see how the community abundance and structure changes over time. ACKNOWLEDGMENTS We would like to thank the National Science Foundation for funding this research opportunity and Oak Mountain State Park for hosting our study. This project would not have been possible without the help of Dan Proud and Malia Fincher, whose advice and problem solving were essential. We also greatly appreciate Pete Van Zandt s contribution through his statistical consultations and the bug sorting aide provided by Chase. Because of Sarah Clardy of the U.S. Fish and Wildlife Service, we were able to see exceptional examples of mountain longleaf forests at the Mountain Longleaf NWR. Thanks also go out to Emma Sheffield, a great field buddy who was kind enough to share both data and snacks. LITERATURE CITED Abrams, M.D Fire and the development of oak forests. BioScience 42: Andersen, A.N., B.D. Hoffmann, W.J. Muller, A.D. Griffiths Using ants as bioindicators in land management: simplifying assessment of ant community responses. Journal of Applied Ecology 39: Andrew, N., L. Rodgerson, A. York Frequent fuel reduction burning: the role of logs and associated leaf litter in the conservation of ant biodiversity. Austral Ecology 25: Bird, S., R.N. Coulson, D.A. Crossley Jr Impacts of silvicultural practices on soil and litter arthropod diversity in a Texas pine plantation. Forest Ecology and Management 13:
6 Brockway, D.G. and C.E. Lewis Long-term effects of dormant-season prescribed fire on plant community diversity, structure and productivity in a longleaf pine wiregrass ecosystem. Forest Ecology and Management 96: Brockway, D.G., K.W. Outcalt, D.J. Tomczak, E.E. Johnson. Restoring longleaf pine forest ecosystems in the southern U.S. Pages in:j.a. Santurf and P. Madsen (eds.) Restoration of Boreal and Temperate Forests. CRC Press, Boca Raton, Florida. Buddle, C.M., J.R. Spence, and D.W. Langor Succession of boreal forest spider assemblages following wildfire and harvesting. Ecography 23: Buddle, C.M., D.W. Langor, G.R. Pohl, J.R. Spence Arthropod responses to harvesting and wildfire: Implications for emulation of natural disturbance in forest management. Biological Conservation 128: Chen, B. and D.H. Wise. Bottom-up limitation of predaceous arthropods in a detritus-based terrestrial food web. Ecology 80: Castano-Meneses, G., J.G. Palacios-Vargas Effects of fire and agricultural practices on neotropical ant communities. Biodiversity and Conservation 12: Drever, C.R., G. Peterson, C. Messier, Y. Bergeron, and M. Flannigan Can forest management based on natural disturbances maintain ecological resilience? Canadian Journal of Forest Restoration 36: Ferrenberg S.M., D.W. Schwilk, E.E. Knapp, E. Groth, J.E. Keeley Fire decreases arthropod abundance but increases diversity: early and late season prescribed fire effects in a Sierra Nevada mixed-conifer forest. Fire Ecology 2: Gibb, H. and D.F. Hochuli Habitat fragmentation in an urban environment: large and small fragments support different arthropod assemblages. Biological Conservation 106: Hansen, R.A. and D.C. Coleman Litter complexity and composition are determinants of the diversity and species composition of oribatid mites (Acari: Oribatida) in litterbags. Applied Soil Ecology 9: Jimenez-Valverde, A. and J.M. Lobo Determining a combined sampling procedure for a reliable estimation of araneidae and thomisidae assemblages (Arachnida, Araneae). The Journal of Arachnology 33: Kaspari, M. and M.D. Weiser Ant activity along moisture gradients in a neotropical forest. Biotropica 32: Laussau, S.A. and D.F. Hochuli Effects of habitat complexity on ant assemblages. Ecography 27: Maleque, M.A., K. Maetq, H.T. Ishii Arthropods as bioindicators of sustainable forest management, with a focus on plantation forests. Applied Entomological Zoology 1:1-11. Moretti, M., M.K. Obrist, P. Duelli Arthropod biodiversity after forest fires: winners and losers in the winter fire regime of the southern Alps. Ecography 27: Nakamura, A. H. Proctor, C.P. Catterall Using soil and litter arthropods to assess the state of rainforest restoration. Ecological Management and Restoration 4: Niwa, C.G. and R.W. Peck Influence of prescribed fire on carabid beetle (Carabidae) and Spider (Araneae) assemblage in forest litter in southwestern Oregon. Community and Ecosystem Ecology 31: Orgeas J. and A.N. Andersen Fire and biodiversity: responses of grass-layer beetles to experimental fire regimes in an Australian tropical savanna. Journal of Applied Ecology 38:
7 Paoletti, M.G., G.H. Osler, A. Kinnear, D.G. Black, L.J. Thomson, A. Tsitsilas, D. Sharley, S. Judd, P. Neville, A. D Inca Detritivores as indicators of landscape stress and soil degradation. Australian Journal of Experimental Agriculture 47: Paoletti, M.G. and M. Hassal Woodlice (Isopoda: Oniscidea): their potential for assessing sustainability and use as bioindicators. Agriculture, Ecosystems and Environment 74: Rainio, J and J. Niemela Ground beetles (Coleoptera:Carabidae) as bioindicators. Biodiversity and Conservation 12: Reichert, S.E. and R.M. Gillespie Habitat choice and utilization in web-building spiders. Pages in: Shear, W.A (ed). Spiders: Webs, Behaviors and Evolution. Stanford University Press, Palo Alto, California. Sabu, T.K., R.T. Shiju, K.N. Vinod, S. Nithya. A comparison of the pitfall trap, Winkler extractor, and Berlese funnel for sampling ground-dwelling arthropods in tropical montane cloud forests. Journal of Insect Science 11:1-19. Spence, J.R., C.M. Buddle, K.J. Gandhi, D.W. Langor, W.J. Volney, H.E. Hammond, G.R. Pohl Invertebrate biodiversity, forestry and emulation of natural disturbance: a down-toearth perspective. United States Department of Agriculture Forest Service General Technical Report: Uetz, G.W. and J.D. Unzicker Pitfall trapping in ecological studies of wandering spiders. Journal of Arachnology 3: Wikars L.O. and J. Schimmel Immediate effects of fire-severity on soil invertebrates in cut and uncut pine forests. Forest Ecology and Management 141:
8 Table 1: Analysis of variance of abundance of major arthropod orders or trophic groups between burned and unburned sites. Significant results (P < 0.05) are marked with an *. Order/Trophic Group n df F P Acari * Araneae Non-Predatory Coleoptera Predatory Coleoptera Collembola * Diptera Hemiptera * Hymenoptera Orthoptera Thysanura * Macro Predators * Herbivores Macro Detritivores * Macro Non Predators Total Fauna (Pitfall) * Total Fauna (Berlese) * 172
9 Table 2: Analysis of variance of major arthropod orders and trophic group s abundance in varying leaf litter depths. Significant results (P < 0.05) are marked with an *. Litter Depth Order/Trophic Group n df F P Acari Araneae Non-Predatory Coleoptera * Predatory Coleoptera Collembola * Diptera * Hemiptera Hymenoptera Orthoptera * Thysanura Macro Predators * Herbivores Macro Detritivores Macro Non Predators Total Fauna (Pitfall) Total Fauna (Berlese)
10 Table 3: Analysis of variance of major arthropod orders and trophic group s abundance from varying leaf litter moisture content. Significant results (P < 0.05) are marked with an *. Litter Moisture Order/Trophic Group n df F P Acari Araneae Non-Predatory Coleoptera Predatory Coleoptera Collembola Diptera Hemiptera Hymenoptera Orthoptera Thysanura * Macro Predators Herbivores Macro Detritivores * Macro Non Predators Total Fauna (Pitfall) Total Fauna (Berlese)
11 Table 4: Analysis of variance of major arthropod orders and trophic group s abundance from varying leaf litter moisture content. Significant results (P < 0.05) are marked with an *. Distance from Ridge Order/Trophic Group n df F P Acari Araneae Non-Predatory Coleoptera Predatory Coleoptera Collembola Diptera * Hemiptera Hymenoptera Orthoptera Thysanura Macro Predators Herbivores Macro Detritivores * Macro Non Predators * Total Fauna (Pitfall) Total Fauna (Berlese) * 175
12 Moisture Content y = x Depth (cm) Burne d Unbur ned Figure 1: Moisture content versus litter depth obtained from 300 samples taken from the burned and unburned sites. 176
13 Figure 2: Comparison of the proportion of individuals from a major order found in the burned or unburned sites. 177
14 Figure 3: Comparison of the major Coleoptera families proportion of individuals found in the burned site versus the unburned site. 178
15 Proportion Burned Unburned Trophic Group Figure 4: Proportion of major trophic groups collected from the burned and unburned sites. 179
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