Climate Change Enhances the Negative Effects of Predation Risk on an Intermediate Consumer

Predators are a major source of stress in natural systems because their prey must balance the benefits of feeding with the risk of being eaten. Although this \u27fear\u27 of being eaten often drives the organization and dynamics of many natural systems, we know little about how such risk effects will be altered by climate change. Here, we examined the interactive consequences of predator avoidance and projected climate warming in a three-level rocky intertidal food chain. We found that both predation risk and increased air and sea temperatures suppressed the foraging of prey in the middle trophic level, suggesting that warming may further enhance the top-down control of predators on communities. Prey growth efficiency, which measures the efficiency of energy transfer between trophic levels, became negative when prey were subjected to predation risk and warming. Thus, the combined effects of these stressors may represent an important tipping point for individual fitness and the efficiency of energy transfer in natural food chains. In contrast, we detected no adverse effects of warming on the top predator and the basal resources. Hence, the consequences of projected warming may be particularly challenging for intermediate consumers residing in food chains where risk dominates predator-prey interactions

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Data from: Prey state shapes the effects of temporal variation in predation risk

The ecological impacts of predation risk are influenced by how prey allocate foraging effort across periods of safety and danger. Foraging decisions depend on current danger, but also on the larger temporal, spatial or energetic context in which prey manage their risks of predation and starvation. Using a rocky intertidal food chain, we examined the responses of starved and fed prey (Nucella lapillus dogwhelks) to different temporal patterns of risk from predatory crabs (Carcinus maenas). Prey foraging activity declined during periods of danger, but as dangerous periods became longer, prey state altered the magnitude of risk effects on prey foraging and growth, with likely consequences for community structure (trait-mediated indirect effects on basal resources, Mytilus edulis mussels), prey fitness and trophic energy transfer. Because risk is inherently variable over time and space, our results suggest that non-consumptive predator effects may be most pronounced in productive systems where prey can build energy reserves during periods of safety and then burn these reserves as ‘trophic heat’ during extended periods of danger. Understanding the interaction between behavioural (energy gain) and physiological (energy use) responses to risk may illuminate the context dependency of trait-mediated trophic cascades and help explain variation in food chain length

Appendix A. Description of techniques used to map and monitor barnacles and tables of statistical results.

Description of techniques used to map and monitor barnacles and tables of statistical results

All data

matassa&trussell_1-7.zip contains 7 consecutively numbered csv files which contain all of the data presented in the manuscript and its appendice

Data from: Cascading effects of a top predator on intraspecific competition at intermediate and basal trophic levels

1. Predators can impact competition among prey by altering prey density via consumption or by causing prey to modify their traits or foraging behavior. Yet, differences between these two mechanisms may lead to different cascading impacts on lower trophic levels. 2. Using a crab-snail-barnacle rocky intertidal food chain, we tested the effects of predation risk from crabs (top predators) on intraspecific competition among snails (intermediate consumers) and emergent indirect effects on the density of and competition between barnacles (basal resources). 3. The per capita foraging and growth rates of snails declined with high conspecific density. Predation risk from crabs, which caused even larger reductions in snail foraging and growth, weakened competition among snails, whereas a 45% increase in barnacle density had no detectable effect on snail competition. 4. Intraspecific competition between barnacles, however, depended on the interactive effects of barnacle density, snail density, and crab predation risk. Barnacles developed hummocking morphologies as they grew and competed for space. Hummock formation (a proxy for competition) increased as a result of either greater initial barnacle density or reduced snail foraging pressure, but these effects depended on predation risk. 5. The effects of crab predation risk on snail foraging behavior weakened an otherwise strong relationship between barnacle density and hummock development: hummocking increased with barnacle density in the absence of crabs but remained relatively high when crabs were present. In communities with similar final barnacle densities, hummocking was more common in those with crabs than those without crabs. 6. The extent to which predators can drive trophic cascades by suppressing the foraging rates of their prey is highly context-dependent: the positive trait-mediated indirect effect of predators on basal resource abundance is stronger when many prey respond simultaneously to the threat of predation. However, our results demonstrate that top predators can also enhance competition among basal resources even when their indirect effect on resource abundance is relatively weak. Hence, the cascading effects of predators on competition within lower trophic levels may play an important but underappreciated role in the dynamics of basal resource populations and the communities they support

Data from: Moving beyond linear food chains: trait-mediated indirect interactions in a rocky intertidal food web

In simple, linear food chains, top predators can have positive indirect effects on basal resources by causing changes in the traits (e.g. behaviour, feeding rates) of intermediate consumers. Although less is known about trait-mediated indirect interactions (TMIIs) in more complex food webs, it has been suggested that such complexity dampens trophic cascades. We examined TMIIs between a predatory crab (Carcinus maenas) and two ecologically important basal resources, fucoid algae (Ascophyllum nodosum) and barnacles (Semibalanus balanoides), which are consumed by herbivorous (Littorina littorea) and carnivorous (Nucella lapillus) snails, respectively. Because crab predation risk suppresses snail feeding rates, we hypothesized that crabs would also shape direct and indirect interactions among the multiple consumers and resources. We found that the magnitude of TMIIs between the crab and each resource depended on the suite of intermediate consumers present in the food web. Carnivorous snails (Nucella) transmitted TMIIs between crabs and barnacles. However, crab–algae TMIIs were transmitted by both herbivorous (Littorina) and carnivorous (Nucella) snails, and these TMIIs were additive. By causing Nucella to consume fewer barnacles, crab predation risk allowed fucoids that had settled on or between barnacles to remain in the community. Hence, positive interactions between barnacles and algae caused crab–algae TMIIs to be strongest when both consumers were present. Studies of TMIIs in more realistic, reticulate food webs will be necessary for a more complete understanding of how predation risk shapes community dynamics

Data from: Resource levels and prey state influence antipredator behavior and the strength of nonconsumptive predator effects

The risk of predation can drive trophic cascades by causing prey to engage in antipredator behavior (e.g. reduced feeding), but these behaviors can be energetically costly for prey. The effects of predation risk on prey (nonconsumptive effects, NCEs) and emergent indirect effects on basal resources should therefore depend on the ecological context (e.g. resource abundance, prey state) in which prey manage growth/predation risk tradeoffs. Despite an abundance of behavioral research and theory examining state-dependent responses to risk, there is a lack of empirical data on state-dependent NCEs and their impact on community-level processes. We used a rocky intertidal food chain to test model predictions for how resources levels and prey state (age/size) shape the magnitude of NCEs. Risk cues from predatory crabs (Carcinus maenas) caused juvenile and sub-adult snails (Nucella lapillus) to increase their use of refuge habitats and decrease their growth and per capita foraging rates on barnacles (Semibalanus balanoides). Increasing resource levels (high barnacle density) and prey state (sub-adults) enhanced the strength of NCEs. Our results support predictions that NCEs will be stronger in resource-rich systems that enhance prey state and suggest that the demographic composition of prey populations will influence the role of NCEs in trophic cascades. Contrary to theory, however, we found that resources and prey state had little to no effect on snails in the presence of predation risk. Rather, increases in NCE strength arose because of the strong positive effects of resources and prey state on prey foraging rates in the absence of risk. Hence, a common approach to estimating NCE strength – integrating measurements of prey traits with and without predation risk into a single metric – may mask the underlying mechanisms driving variation in the strength and relative importance of NCEs in ecological communities

Appendix A. Five tables showing the ANOVA results of Nucella present on barncales or mussels, and of the number of barnacles and mussels consumed, the amount of energy acquired by Nucella, the amount of tissue produced by Nucella, and the growth efficiency of Nucella, all in the presence and absence of predation risk and different levels of snail removal.

Five tables showing the ANOVA results of Nucella present on barncales or mussels, and of the number of barnacles and mussels consumed, the amount of energy acquired by Nucella, the amount of tissue produced by Nucella, and the growth efficiency of Nucella, all in the presence and absence of predation risk and different levels of snail removal