Higher Trophic Levels Overwhelm Climate Change Impacts on Terrestrial Ecosystem Functioning

RESEARCH ARTICLE Higher Trophic Levels Overwhelm Climate Change Impacts on Terrestrial Ecosystem Functioning Shannon L. Pelini1, Audrey M. Maran1, Angus R. Chen2¤a, Justine Kaseman1,2¤b, Thomas W. Crowther3* a11111 1 Department of Biological Sciences, Bowling Green State University, Bowling Green, OH, 43403, United States of America, 2 Harvard Forest, Harvard University, Petersham, MA, 01366, United States of America, 3 School of Forestry and Environmental Studies, Yale University, New Haven, CT, 06511, United States of America ¤a Current address: US Geological Survey, Dededo, 96912, Guam ¤b Current address: Freelance writing, Brooklyn, NY, 11233, USA * OPEN ACCESS Citation: Pelini SL, Maran AM, Chen AR, Kaseman J, Crowther TW (2015) Higher Trophic Levels Overwhelm Climate Change Impacts on Terrestrial Ecosystem Functioning. PLoS ONE 10(8): e0136344. doi:10.1371/journal.pone.0136344 Editor: Andrea Belgrano, Swedish University of Agricultural Sciences, SWEDEN Received: May 22, 2015 Accepted: July 31, 2015 Published: August 20, 2015 Copyright: © 2015 Pelini et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Data are available on the Harvard Forest data archive (accession number hf113) at http://harvardforest.fas.harvard.edu/harvardforest-data-archive and on the Long Term Ecological Research Network, doi:10.6073/pasta/ be0b964a5caedb3f9c89006eba29cbf7. Funding: Funding was provided by United States National Science Foundation Long Term Ecological Research (DBI 10-03938) and Research Experiences for Undergraduates (DBI 1459519) awards to Harvard Forest. SLP received funds from the Building Strength Program at Bowling Green State University. TWC received funds from Yale University's Climate Abstract Forest floor food webs play pivotal roles in carbon cycling, but they are rarely considered in models of carbon fluxes, including soil carbon dioxide emissions (respiration), under climatic warming. The indirect effects of invertebrates on heterotrophic (microbial and invertebrate) respiration through interactions with microbial communities are significant and will be altered by warming. However, the interactive effects of invertebrates and warming on heterotrophic respiration in the field are poorly understood. In this study we combined field and common garden laboratory approaches to examine relationships between warming, forest floor food web structure, and heterotrophic respiration. We found that soil animals can overwhelm the effects of warming (to 5 degrees Celsius above ambient) on heterotrophic respiration. In particular, the presence of higher trophic levels and burrowing detritivores strongly determined heterotrophic respiration rates in temperate forest soils. These effects were, however, context-dependent, with greater effects in a lower-latitude site. Without isolating and including the significant impact of invertebrates, climate models will be incomplete, hindering well-informed policy decisions. Introduction There is a critical need to improve estimates of future soil CO2 emissions (soil respiration, RS), which are 10 × greater than those generated by the burning of fossil fuels [1], and the potential feedbacks of the emissions to climate change. The impacts of increasing temperatures on microbes, which, along with plant roots are the primary contributors to RS, are included in determination of soil-climate change feedbacks [2–5]. While the direct contribution of other soil and litter-dwelling organisms (e.g., invertebrate detritivores, vertebrate predators) to the heterotrophic component of RS (i.e., RH) is presumed to be small relative to that of microbes, PLOS ONE | DOI:10.1371/journal.pone.0136344 August 20, 2015 1 / 10 Soil Macroinvertebrates Drive Carbon Release and Energy Institute and the British Ecological Society. The authors thank Rob Dunn, Aaron Ellison, Nick Gotelli, and Nate Sanders for allowing use of the warming chambers, funded by United States Department of Energy Program for Ecosystem Research (DE-FG02-08ER64510). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. the indirect effects of climate change on RH through animal-microbe interactions have not been sufficiently explored. Indeed, the absence of soil animals, particularly invertebrates, has been highlighted as a major limitation to current climate and carbon cycling models and management practices [6–10]. Soil food webs are dominated by invertebrates, which govern decomposition rates and soil structure via their interactions with microbial communities [11–17]. Direct trophic effects of invertebrates can regulate microbial activity in some regions [18,19], but the indirect effects generally enhance microbial growth and respiration. That is, by shredding litter [15,17,20,21] and moving soil [11,12,22,23], invertebrate engineers have the potential to stimulate microbial growth and nutrient mineralization [24]. Temperate forests harbor a variety of organisms that also have the capacity to drive cascading effects on microbial activity. However, there is mixed support for top-down trophic cascades on RH via invertebrate predation [25,26]. Best and Welsh [27] demonstrated that salamanders affect forest leaf litter retention by regulating invertebrate populations, but the impacts on microbes and RH remain unknown. The potential for cascading effects on RH needs to be explored further because multiple studies have shown that warming strengthens the effects of predators on lower trophic levels and nutrient cycling in other food webs [21,28,29]. Invertebrates are highly responsive to climatic change [reviewed in 30]. Because invertebrates are ectotherms, the rates and magnitudes of predation and engineering should increase with temperature, at least until thermal thresholds are exceeded or competitive interactions shift [31]. The effects of warming on invertebrate activity may be magnified if soil invertebrates increase movement throughout the soil [32]. Based on this pattern, our understanding of RH responses to warming remains incomplete until we consider the indirect effects of warming mediated through invertebrates. In this study we examined relationships between warming, forest floor food web structure, and RH. We combined field and common garden laboratory experiments to separate indirect from direct and individual from community structure responses to warming on RH. More specifically, using open-top warming chambers at Harvard Forest and Duke Forest, we evaluated the effects of (1) warming on food web structure-RH interactions, (2) macroinvertebrate communities shaped by different warming scenarios on RH, a (...truncated)