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19 September 2017 Warming Strengthens the Ecological Role of Intraspecific Variation in a Predator
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Abstract

Recent work shows communities and ecosystems can be shaped by predator intraspecific variation, but it is unclear whether the magnitude and direction of these influences are context-dependent. Temperature is an environmental context of strong ecological influence and widespread relevance given global warming trends. Warming should increase per capita predator effects on prey through increases in predator metabolic rate, potentially exacerbating intraspecific differences in ecological effects. Here, we used two populations of the potent pelagic freshwater predator, Western Mosquitofish (Gambusia affinis), to test how experimental pond temperature mediates the differences between their ecological impacts. Mosquitofish introduction induced a strong pelagic trophic cascade, causing a large reduction of crustacean zooplankton biomass, an increase in phytoplankton biomass, and changes to ecosystem-level response variables. Warming ( 2°C above unwarmed treatments) exacerbated fish-induced reduction of zooplankton biomass, but moderated the cascade to phytoplankton, primary productivity, and nutrient concentrations. Effects of intraspecific variation were apparent only on zooplankton, and only at warmed environmental temperatures. The traits underlying this divergence may be related to the population source thermal environments. Overall, results show that warming may increase the ecological importance of predator intraspecific variation. In general, extrinsic environmental drivers, such as those associated with climate change, may reshape the effects of intraspecific trait variation on ecosystems.

INTRASPECIFIC trait variation in ecologically important species is becoming a widely recognized potential driver of community—and ecosystem—level characteristics and processes (reviewed in Whitham et al., 2003; Hairston et al., 2005; Fussmann et al., 2007; Bailey et al., 2009a; Post and Palkovacs, 2009; Bolnick et al., 2011; Matthews et al., 2011; Schoener, 2011). Intraspecific effects can be strong even contrasted with traditional ecological factors like presence of a dominant species (Bailey et al., 2009b; Palkovacs et al., 2015; Gómez et al., 2016) and habitat size (Farkas et al., 2013). A typical study design is a “common gardening” experiment (sensu Matthews et al., 2011), in which one tests the ecological impacts of intraspecific trait variants in a common environmental context (e.g., Schweitzer et al., 2004; Palkovacs and Post, 2009; Ingram et al., 2011; Lundsgaard-Hansen et al., 2014; Fryxell et al., 2015; Rudman and Schluter, 2016). However, the role of environmental context in determining the strength and direction of intraspecific effects is not well known. Some studies find intraspecific effects depend on biotic context (i.e., presence of another species or another species' particular phenotype; Palkovacs et al., 2009; Ingram et al., 2012; Rudman et al., 2015), but few studies evaluate how intraspecific effects may depend on the abiotic environment, especially in animals (but see El-Sabaawi et al., 2015; Lajoie and Vellend, 2015; Tuckett et al., this volume, 2017). Because abiotic context strongly shapes ecological interactions (Chamberlain et al., 2014), impacts of intraspecific variation likely also depend on abiotic context.

Temperature is an abiotic variable with profound impacts across levels of biological organization. The ecological influence of temperature is fundamental in that it shapes organismal metabolism (Gillooly et al., 2001; Brown et al., 2004), which itself may help explain higher-level ecological patterns such as biodiversity and carbon-flow through ecosystems (Allen et al., 2002; Schramski et al., 2015). Temperature is highly variable across space and through time, and has been increasing rapidly on average across the globe in recent history (IPCC, 2014). Because of its pervasive ecological role and immediate relevance, it is important to understand how temperature may mediate the ecological role of intraspecific variation.

Metabolism increases exponentially with temperature within the range of temperatures typically encountered by an organism (Gillooly et al., 2001), so small increases in body temperature can greatly increase metabolic demand. This increased demand must be met by increased ingestion rates at the individual level (Rall et al., 2012), which, in consumers and predators, could contribute to the widely observed warming-induced strengthening of top-down effects on ecosystems (Sanford, 1999; Barton and Schmitz, 2009; Barton et al., 2009; O'Connor et al., 2009; Hoekman, 2010; Harley, 2011; Kratina et al., 2012; Shurin et al., 2012). If feeding-related trait variation occurs among populations, warming-induced increases in per capita feeding rates could increase the ecological effects differences between populations of ectotherm predators.

Here, we test the prediction that predator intraspecific differences have stronger effects for freshwater communities in a warmed versus an unwarmed environment. We test this prediction using Western Mosquitofish, Gambusia affinis, which prey heavily upon crustacean zooplankton in the pelagic zone of ponds (Hurlbert and Mulla, 1981; Pyke, 2005), causing trophic cascades whereby producer biomass increases, primary productivity increases, and nutrient concentrations decline (Hurlbert et al., 1972; Fryxell et al., 2016). Mosquitofish have been spread globally (Pyke, 2008) and today inhabit a wide diversity of environments to which they have acclimated and adapted (Pyke, 2005). There is considerable trait variation within and among Mosquitofish populations. Body size variation and sex ratio variation are common and can mediate a population's ecological effects. An increasing proportion of females, which are generally larger, can induce stronger trophic cascades (Fryxell et al., 2015). Morphological differences among Mosquitofish populations can emerge via evolutionary responses to predation pressure (Langerhans et al., 2004). Mosquitofish are also known to exhibit rapid evolution of life history traits in response to habitat size variation (Stearns, 1983) and temperature (Stockwell and Weeks, 1999). Such contemporary trait change might also have community and ecosystem effects.

In this experiment, we used wild-caught Mosquitofish from two recently divergent populations of different thermal environment. We crossed three fish treatments (fishless, cool-source, warm-source) with two ecosystem temperature treatments (unwarmed, warmed) to test our predictions that 1) warming exacerbates top-down effects of fish introduction and 2) warming exacerbates the ecological differences between warm- and cool-source fish. Specifically, we expect 1) fish will more strongly suppress zooplankton at warmed versus unwarmed temperatures, which should cascade to affect phytoplankton, productivity, and nutrients, and 2) the ecological differences between populations for these same response variables will be larger at warmed versus unwarmed temperatures. Our use of recently divergent wild-caught fish from populations of different source temperatures may additionally allow us to address how