Large Inter- and Intraspecific Variation in Heat Tolerance Across Trophic Levels of a Soil Arthropod Community

CORE Metadata, citation and similar papers at core.ac.uk Provided by University of Groningen University of Groningen Heated communities Franken, Oscar; Huizinga, Milou; Ellers, Jacintha; Berg, Matty P. Published in: Oecologia DOI: 10.1007/s00442-017-4032-z IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2018 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Franken, O., Huizinga, M., Ellers, J., & Berg, M. P. (2018). Heated communities: Large inter- and intraspecific variation in heat tolerance across trophic levels of a soil arthropod community. Oecologia, 186(2), 311-322. https://doi.org/10.1007/s00442-017-4032-z Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 13-11-2019 Oecologia (2018) 186:311–322 https://doi.org/10.1007/s00442-017-4032-z HIGHLIGHTED STUDENT RESEARCH Heated communities: large inter‑ and intraspecifc variation in heat tolerance across trophic levels of a soil arthropod community Oscar Franken1 · Milou Huizinga1 · Jacintha Ellers1 · Matty P. Berg1,2 Received: 2 August 2017 / Accepted: 29 November 2017 / Published online: 9 December 2017 © The Author(s) 2017. This article is an open access publication Abstract Temperature extremes are predicted to increase in frequency, intensity and duration under global warming and are believed to signifcantly afect community composition and functioning. However, the efect of extreme climatic events on communities remains difcult to predict, especially because species can show dissimilar responses to abiotic changes, which may afect the outcome of species interactions. To anticipate community responses we need knowledge on within and among species variation in stress tolerance. We exposed a soil arthropod community to experimental heat waves in the feld and measured heat tolerance of species of diferent trophic levels from heated and control plots. We measured the critical thermal maximum (CTmax) of individuals to estimate inter- and intraspecifc variation in heat tolerance in this community, and how this was afected by experimental heat waves. We found interspecifc variation in heat tolerance, with the most abundant prey species, the springtail Isotoma riparia, being more sensitive to high temperatures than its predators (various spider species). Moreover, intraspecifc variation in CT max was substantial, suggesting that individuals within a single species were unequally afected by heat extremes. However, heat tolerance of species did not increase after being exposed to an experimental heat wave. We conclude that interspecifc variation in tolerance traits potentially causes trophic mismatches during extreme events, but that intraspecifc variation could lessen these efects by enabling partial survival of populations. Therefore, ecophysiological traits can provide a better understanding of abiotic efects on communities, not only within taxonomic or functional groups, but also when comparing diferent trophic levels. Keywords Critical thermal maximum (CTmax) · Extreme event · Heat wave · Functional trait · Thermal stress Introduction Communicated by Sylvain Pincebourde. Most terrestrial ecosystems irregularly experience sudden and severe changes in environmental conditions, for We expanded the use of trait-based approaches to include example, due to extreme weather events, such as heat multiple taxa within a soil arthropod community in the feld. This provides new insights on how diferences in tolerance can waves, drought spells, and floods. Such extreme events shape communities. have recently received increasing experimental attention (e.g., De Boeck et al. 2011; Krab et al. 2013; Kayler et al. Electronic supplementary material The online version of this 2015), but their impact on the community relative to more article (https://doi.org/10.1007/s00442-017-4032-z) contains supplementary material, which is available to authorized users. gradual changes in abiotic conditions remains hard to assess. Whereas, extreme events occur infrequently and usually last * Oscar Franken for a short period of time, they impose more extreme con- [email protected]; [email protected] ditions on organisms and the sudden onset of these events 1 Section of Animal Ecology, Department of Ecological leaves little time for adaptation. Moreover, current climate Science, Vrije Universiteit, Amsterdam, De Boelelaan 1085, change scenarios predict an increase in frequency, intensity 1081 HV Amsterdam, The Netherlands and duration of extreme weather events (Easterling et al. 2 Groningen Institute for Evolutionary Life Sciences, 2000a, b; Beniston et al. 2007; Rahmstorf and Coumou Community and Conservation Ecology Group, University 2011), which may amplify their ecological impact (Guts- of Groningen, PO Box 11103, 9700 CC Groningen, chick and BassiriRad 2003; Jentsch et al. 2007). The Netherlands Vol.:(0123456789)1 3 312 Oecologia (2018) 186:311–322 A major challenge in community ecology is to predict through reduced prey density) or lower trophic levels (e.g., the efects of such extreme weather events on community through reduced predation pressure). Another important structure and composition (Gilman et al. 2010; Sutherland source of intraspecifc variation in trait values is pheno- et al. 2013). The main difculty in anticipating a community typic plasticity (DeWitt and Scheiner 2004), by which pre- response is that diferent species within the community can vious exposure to stressful conditions may lead to a rapid show dissimilar responses to abiotic stress, which may be increase in tolerance to subsequent exposures, which may due to diferences in physiological tolerances or behavioural even act across generations (e.g., Bateson et al. 2014; Ziz- strategies and microhabitat use to avoid stress. In addition, zari et al. 2016). Moreover, if species difer in the degree the variation among species in their responses to environ- to which they adjust their physiology to extreme condi- mental change may result in altered trophic, competitive or tions, this may diferentially afect species’ survival when facilitative interactions and interaction strengths (Tylianakis exposed to extreme events, thereby afecting the inter- et al. 2008; Walther 2010; Berg et al. 2010). To anticipate action strength between the species. Understanding the community responses we need knowledge on interspecifc causes and consequences of intraspecifc variation can and intraspecifc variation in responses of species to abiotic provide valuable insight in the efects of extreme events stress, which can be investigated using functional traits that at the population level, and subsequently on the interac- relate to species tolerance. tions with other species in the community. Trait-based approaches have been advocated as a more In this paper we investigate the extent of inter- and mechanistic approach to foresee how communities are intraspecifc variation in heat tolerance of several species afected by environmental change (McGill et al. 2006; Lang- from a soil arthropod community that was exposed to experi- lands et al. 2011; Dias et al. 2013). Multiple studies have mental heat waves. These heat waves were induced by plac- related variation in tolerance traits and their environmental ing small plastic greenhouses with heat emitters in the feld. drivers to spatial distribution of species (Dias et al. 2013; We focus on a thermal trait that is related to temperature van Dooremalen et al. 2013), (dis)assembly processes (Lindo extremes: the critical thermal maximum (CT max), which et al. 2012; Bartlett et al. 2016), and community composition refects the heat tolerance of an individual when exposed (Bokhorst et al. 2012). However, trait studies have mainly to a gradually increasing temperature (Lutterschmidt and been carried out within single functional groups or trophic Hutchison 1997; Terblanche et al. 2007; Mitchell and Hof- levels (e.g., Dias et al. 2013; van Dooremalen et al. 2013), mann 2010). As CTmax is measured at the individual level, rather than across trophic levels within a single community this tolerance proxy allowed us to measure intraspecifc (but see Sentis et al. 2013; Puentes et al. 2015). Moreover, variation in heat tolerance and link this to body size efects. studies have predominantly used mean trait values of species Using species from a single arthropod community, we maxi- to characterize interspecifc variation in tolerance, ignoring mize the likelihood that they have previously experienced the fact that trait distributions between species may overlap the same climatic conditions, although the actual habitat due to intraspecifc variation of trait values (Albert et al. mean temperature and variance that individuals have expe- 2011; Violle et al. 2012). Intraspecifc

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