Warming reverses top-down effects of predators on belowground ecosystem function in Arctic tundra Amanda M. Koltza,b,1, Aimée T. Classenc,d, and Justin P. Wrightb aDepartment of Biology, Washington University in St. Louis, St. Louis, MO 63130; bDepartment of Biology, Duke University, Durham, NC 27708; cThe Rubenstein School of Environment & Natural Resources, University of Vermont, Burlington, VT 05405; and dThe Gund Institute for Environment, University of Vermont, Burlington, VT 05405 Edited by Alan Hastings, University of California, Davis, CA, and approved June 12, 2018 (received for review May 21, 2018) Predators can disproportionately impact the structure and func- the rate of global climate change (9). Prior studies have assessed tion of ecosystems relative to their biomass. These effects may be the feedbacks between the Arctic terrestrial ecosystem and cli- exacerbated under warming in ecosystems like the Arctic, where mate change by measuring the balance between plant community the number and diversity of predators are low and small shifts in and microbial responses to warmer temperatures (reviewed in community interactions can alter carbon cycle feedbacks. Here, we ref. 10). The extent to which these responses may be affected by show that warming alters the effects of wolf spiders, a dominant interactions with organisms at other trophic levels, which are also tundra predator, on belowground litter decomposition. Specifi- responding to warming (e.g., detritivores, herbivores, pollinators, cally, while high densities of wolf spiders result in faster litter predators), has been largely overlooked (but see refs. 11–13 for decomposition under ambient temperatures, they result, instead, discussion of effects of vertebrate herbivores on plant commu- in slower decomposition under warming. Higher spider densities nities under warming). In particular, there has been little con- are also associated with elevated levels of available soil nitrogen, sideration of how changes in trophic interactions between potentially benefiting plant production. Changes in decomposition belowground microbes and their associated consumers, which rates under increased wolf spider densities are accompanied by are both sensitive to warming (14–19), will affect ecosystem trends toward fewer fungivorous Collembola under ambient functioning in the Arctic (but see refs. 14, 20). temperatures and more Collembola under warming, suggesting The composition and activity of microbial communities are that Collembola mediate the indirect effects of wolf spiders on often modified by soil micro- and macroinvertebrates (5), which decomposition. The unexpected reversal of wolf spider effects on are themselves regulated by higher level predators, such as Collembola and decomposition suggest that in some cases, warm- surface-dwelling spiders (21). At our study site in the Alaskan ing does not simply alter the strength of top-down effects but, Arctic, wolf spiders are extremely abundant at the soil surface instead, induces a different trophic cascade altogether. Our results (22, 23) and outweigh larger mammalian predators, such as indicate that climate change-induced effects on predators can wolves, by several orders of magnitude (SI Appendix), making cascade through other trophic levels, alter critical ecosystem them one of the dominant predators of the tundra community. In functions, and potentially lead to climate feedbacks with impor- temperate forests and agroecosystems, wolf spider predation has tant global implications. Moreover, given the expected increase in wolf spider densities with climate change, our findings suggest indirect effects on key ecosystem processes, including plant productivity (24), nutrient cycling (25, 26), and decomposition that the observed cascading effects of this common predator on – detrital processes could potentially buffer concurrent changes in (27 29). As in temperate systems, Arctic wolf spiders are gen- decomposition rates. eralist feeders that prey upon herbivores, detritivores, and other Arctic | predator | decomposition | aboveground–belowground | Significance trophic interactions Organisms’ responses to climate change can result in altered espite general agreement that species interactions will be species interactions, with cascading effects on communities Daffected by climate change (1, 2), surprisingly few studies and ecosystems. Understanding these processes is especially have explored the ways in which climate-modified trophic cas- relevant in the rapidly warming Arctic, where faster decom- cades might affect ecosystem functioning (reviewed in ref. 3). position of stored soil carbon is expected to result in positive Individual and population-level responses to altered climatic carbon feedbacks to the atmosphere. We provide evidence that conditions could have cascading effects that either amplify or warmer temperatures alter the cascading effects of wolf spiders, an abundant and widespread predator, on ecosystem func- dampen the impacts of existing trophic cascades on ecosystems. tioning. Specifically, we find that warming tends to reverse the However, interactive effects between climate change and these effect of high spider densities on fungal-feeding Collembola population-level responses could also lead to completely new and ultimately leads to slower decomposition rates. Our work community structures with subsequent impacts on function. It is demonstrates that climate change can alter the nature of increasingly apparent that changes in community-scale dynamics predator effects on decomposition, resulting in unexpected can influence important ecosystem processes, such as pro- changes in ecosystem function with potentially important ductivity, nutrient cycling, and decomposition (4, 5). Thus, un- global implications. derstanding how global change will shape both community interactions and function is important when predicting the ef- Author contributions: A.M.K. and J.P.W. designed research; A.M.K. performed research; fects of future climate change. A.M.K. analyzed data; and A.M.K., A.T.C., and J.P.W. wrote the paper. Shifts in aboveground–belowground trophic interactions due The authors declare no conflict of interest. to climate change are particularly relevant in the Arctic, a region This article is a PNAS Direct Submission. that is warming rapidly (6) and stores a large amount of soil Published under the PNAS license. organic carbon (C) (7, 8). Rapid warming is facilitating increased 1To whom correspondence should be addressed. Email: [email protected]. belowground microbial respiration from thawing permafrost This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. ECOLOGY more than it is increasing plant uptake of C, thereby causing the 1073/pnas.1808754115/-/DCSupplemental. Arctic to become a source of atmospheric C and accelerating Published online July 23, 2018. www.pnas.org/cgi/doi/10.1073/pnas.1808754115 PNAS | vol. 115 | no. 32 | E7541–E7549 Downloaded by guest on October 4, 2021 predators (30–32), suggesting that they could indirectly influence Wolf spider density treatments included low density, control these processes in the Arctic as well. While experimental work density, and high density; high-density treatments had approxi- has failed to detect changes in plant performance due to Arctic mately twice the densities of the average early season densities wolf spider predation on herbivores (33), more recent work from the control treatments. Warming treatments were either suggests that these predators may obtain the majority of their ambient temperature or warmed. energy from detritivorous prey [e.g., Collembola (22)], and Given the pace at which the Arctic is warming and the fact that therefore are more likely to have measurable indirect effects on wolf spider densities may be higher in the future, our primary processes such as decomposition and nutrient cycling. Currently, interest for this experiment was in capturing potential interac- Arctic wolf spiders are responding to earlier snowmelt dates tions between the wolf spider density and warming treatments. brought on by climate change by becoming larger (34) and hence We used a series of mixed effects models to investigate these more fecund (35). Because bigger and more abundant spiders potential interactive treatment effects on belowground commu- could exert stronger predation pressure on belowground prey, nity structure and function. In each model, either average soil these changes could have important consequences for microbial moisture or litter moisture content was included as a fixed effect activity and nutrient cycling in the tundra. and experimental block was included as a random effect. Post Arctic wolf spiders and the food web to which they belong hoc tests (e.g., Tukey) are not available for general linear mixed provide us with an ideal system to study how trophic interactions models with interaction terms; thus, for those models that might alter the predicted effects of climate change on ecosystem showed significant interactive effects on the response variable, functioning. Here, we explore the role of Arctic wolf spiders in we split the models by ambient temperature and warming mediating the response of the belowground community to treatments to investigate pairwise differences under the three warming. Specifically, using a fully factorial experimental design, spider density treatments (low, control, or high). we investigated the extent to which warming and the expected associated increase in wolf spider