Warming reinforces nonconsumptive predator effects on prey growth, physiology, and body stoichiometry

Abstract

While nonconsumptive effects of predators may strongly affect prey populations, little is known how future warming will modulate these effects. Such information would be especially relevant with regard to prey physiology and resulting changes in prey stoichiometry. We investigated in Enallagma cyathigerum damselfly larvae the effects of a 4°C warming (20°C vs. 24°C) and predation risk on growth rate, physiology and body stoichiometry, for the first time including all key mechanisms suggested by the general stress paradigm (GSP) on how stressors shape changes in body stoichiometry. Growth rate and energy storage were higher at 24°C. Based on thermodynamic principles and the growth rate hypothesis, we could demonstrate predictable reductions in body C:P under warming and link these to the increase in P-rich RNA; the associated warming-induced decrease in C:N may be explained by the increased synthesis of N-rich proteins. Yet, under predation risk, growth rate instead decreased with warming and the warming-induced decreases in C:N and C:P disappeared. As predicted by the GSP, larvae increased body C:N and C:P at 24°C under predation risk. Notably, we did not detect the assumed GSP-mechanisms driving these changes: despite an increased metabolic rate there was neither an increase of C-rich biomolecules (instead fat and sugar contents decreased under predation risk), nor a decrease of N-rich proteins. We hypothesize that the higher C:N and N:P under predation risk are caused by a higher investment in morphological defense. This may also explain the stronger predator-induced increase in C:N under warming. The expected higher C:P under predation risk was only present under warming and matched the observed growth reduction and associated reduction in P-rich RNA. Our integrated mechanistic approach unraveled novel pathways of how warming and predation risk shape body stoichiometry. Key findings that (1) warming effects on elemental stoichiometry were predictable and only present in the absence of predation risk and that (2) warming reinforced the predator-induced effects on C:N:P, are pivotal in understanding how nonconsumptive predator effects under global warming will shape prey populations.

Energy storage and fecundity explain deviations from ecological stoichiometry predictions under global warming and size‐selective predation

“…While several recent studies found both stressors to interact (e.g. Touchon & Warkentin ; Culler, McPeek & Ayres ; Miller, Matassa & Trussell ; Janssens, Van Dievel & Stoks ), Chu et al . () showed no significant overlap in the transcriptomic responses to predation risk and thermal stress in the snail Nucella lapillus , indicating both stressors may impose distinct and potentially additive challenges.…”

“…They claimed this was because predator‐induced increases of C‐rich sugars were accompanied by increases in N‐rich proteins due to the increased production of tail muscles. Notably, the few studies that showed the predicted increase in body C : N under the GSP, either did not explicitly test for the assumed underlying GSP mechanisms (Hawlena & Schmitz ) or demonstrated the pattern could not be explained by GSP mechanisms (Janssens, Van Dievel & Stoks ). Taken together, this suggests that while predation risk can indeed affect the C : N ratio of the prey, a more general mechanistic framework is needed that reconciles the contrasting patterns.…”

The Temperature Dependence of Predation Stress and Prey Nutritional Stoichiometry

“…Several studies experimentally examining the interplay between temperature and predation risk have provided mixed support for the original idea that rising temperature should exacerbate predation stress causing prey to consume more C (Jansens et al, 2015;Kirschman et al, 2016;Van Dievel et al, 2016;Zhang et al, 2016). These studies used 2 × 2 factorial designs that crossed a temperature treatment with a perceived predation risk treatment.…”

“…These shifts in nutrient intake should also be reflected in body element stoichiometry, with stressed prey having higher carbon [C]:nitrogen [N] ratios than non-stressed prey (Hawlena and Schmitz, 2010a). Some experiments have shown that such shifts in nutrient intake and body stoichiometry can indeed occur between conditions with and without perceived predation risk (McPeek et al, 2001;Hawlena and Schmitz, 2010b;Jansens et al, 2015). Other experiments have, however, shown that the predicted responses do not occur (Costello and Michel, 2013;Dalton and Flecker, 2014;Kaplan et al, 2014;Guariento et al, 2015;Kirschman et al, 2016;Van Dievel et al, 2016;Zhang et al, 2016), thereby calling into question the generality of the predicted stress response.…”

Fear and below-ground food-webs

“…Prey can also allocate resources to develop and support new defense morphologies (e.g., larger tail muscles, and shell or exoskeleton fortifications; Tollrian and Harvell, 1999). Both physiological and morphological defenses can alter the nutritional composition of prey body and waste materials (e.g., Hawlena and Schmitz, 2010a;Dalton and Flecker, 2014;Guariento et al, 2015;Janssens et al, 2015). When decomposed, carcasses and waste materials of stressed animals may affect the SFW differently from those of non-stressed prey (Fig.…”