Local adaptation in trait-mediated trophic cascades.

Predator-induced changes in prey foraging can influence community dynamics by increasing the abundance of basal resources via a trait-mediated trophic cascade. The strength of these cascades may be altered by eco-evolutionary relationships between predators and prey, but the role of basal resources has received limited attention. We hypothesized that trait-mediated trophic cascade strength may be shaped by selection from trophic levels above and below prey. Field and laboratory experiments used snails (Nucella lapillus) from two regions in the Gulf of Maine (GoM) that vary in basal resource availability (e.g. mussels), seawater temperature, and contact history with the invasive green crab, Carcinus maenas. In field and laboratory experiments, Nucella from both regions foraged on mussels in the presence or absence of green crab risk cues. In the field, Nucella from the northern GoM, where mussels are scarce, were less responsive to risk cues and more responsive to seawater temperature than southern Nucella. In the lab, however, northern Nucella foraged and grew more than southern snails in the presence of risk, but foraging and growth were similar in the absence of risk. We suggest that adaptation to basal resource availability may shape geographical variation in the strength of trait-mediated trophic cascades.

Local and regional geographic variation in inducible defenses.

Invasive predators can cause substantial evolutionary change in native prey populations. Although invasions by predators typically occur over large scales, their distributions are usually characterized by substantial spatiotemporal heterogeneity that can lead to patchiness in the response of native prey species. Our ability to understand how local variation shapes patterns of inducible defense expression has thus far been limited by insufficient replication of populations within regions. Here, we examined local and regional variation in the inducible defenses of 12 native marine snail (Littorina obtusata) populations within two geographic regions in the Gulf of Maine that are characterized by vastly different contact histories with the invasive predatory green crab (Carcinus maenas). When exposed in the field to waterborne risk cues from the green crab for 90 days, snails expressed plastic increases in shell thickness that reduced their vulnerability to this shell-crushing predator. Despite significant differences in contact history with this invasive predator, snail populations from both regions produced similar levels of shell thickness and shell thickness plasticity in response to risk cues. Such phenotypic similarity emerged even though there were substantial geographic differences in the shell thickness of juvenile snails at the beginning of the experiment, and we suggest that it may reflect the effects of warming ocean temperatures and countergradient variation. Consistent with plasticity theory, a trend in our results suggests that southern snail populations, which have a longer contact history with the green crab, paid less in the form of reduced tissue mass for thicker shells than northern populations.

A novel analytical framework to quantify co-gradient and countergradient variation.

Spatial covariance between genotypic and environmental influences on phenotypes (CovGE ) can result in the nonrandom distribution of genotypes across environmental gradients and is a potentially important factor driving local adaptation. However, a framework to quantify the magnitude and significance of CovGE has been lacking. We develop a novel quantitative/analytical approach to estimate and test the significance of CovGE from reciprocal transplant or common garden experiments, which we validate using simulated data. We demonstrate how power to detect CovGE changes over a range of experimental designs. We confirm an inverse relationship between gene-by-environment interactions (GxE) and CovGE , as predicted by first principles, but show how phenotypes can be influenced by both. The metric provides a way to measure how phenotypic plasticity covaries with genetic differentiation and highlights the importance of understanding the dual influences of CovGE and GxE on phenotypes in studies of local adaptation and species' responses to environmental change.

Effects of a non-native cyanobacterium on bay scallops (Argopecten irradians) in a New England seagrass ecosystem.

Bay scallops (Argopecten irradians) are an economically valuable species whose populations have declined in recent decades due in part to harmful algal and cyanobacterial blooms. Nantucket, Massachusetts hosts one of the last remaining bay scallop fisheries in the U.S., but recently documented the occurrence of a non-native cyanobacterium (Hydrocoleum sp.). Hydrocoleum can form dense mats in seagrass beds, the primary habitat of scallops, but is also diazotrophic, potentially augmenting bioavailable nitrogen to primary producers and fueling secondary production. We conducted surveys to explore the relationships between Hydrocoleum and scallop condition, reproductive potential, and density in eelgrass beds in Nantucket Harbor as well as effects of other habitat characteristics (e.g., eelgrass cover) on these same scallop traits. We found low Hydrocoleum cover during our sampling, but found fewer large scallops in plots with Hydrocoleum, suggesting that this size class may be especially vulnerable to negative effects of Hydrocoleum. Contrary to expectation, we found a positive correlation between Hydrocoleum cover and scallop condition. These patterns suggest that Hydrocoleum may enhance scallop condition, but also affect habitat use, highlighting the need for manipulative experiments to clarify mechanisms driving these relationships. Understanding how non-native species such as Hydrocoleum impact fishery species will help advance conservation and resource management efforts.

Parental and embryonic experiences with predation risk affect prey offspring behaviour and performance.

Because phenotypic plasticity can operate both within and between generations, phenotypic outcomes are often shaped by a complex history of environmental signals. For example, parental and embryonic experiences with predation risk can both independently and interactively influence prey offspring traits early in their life. Parental and embryonic risk experiences can also independently shape offspring phenotypes throughout an offspring's ontogeny, but the persistence of their interactive effects throughout offspring ontogeny is unknown. We examined the effects of parental and embryonic experiences with predation risk on the response of 1-year-old prey (the carnivorous snail, Nucella lapillus) offspring to current predation risk. We found that parental and embryonic risk experiences had largely independent effects on offspring performance and that these effects were context dependent. Parental experience with risk had strong impacts on multiple offspring traits in the presence of current risk that generally improved offspring performance under risk, but embryonic risk experience had relatively weaker effects and only operated in the absence of current risk to reduce offspring growth. These results illustrate that past environmental experiences can dynamically shape organism phenotypes across ontogeny and that attention to these effects is key to a better understanding of predator/prey dynamics in natural systems.

Synergistic effects of parental and embryonic exposure to predation risk on prey offspring size at emergence.

Cues signaling predation risk can strongly influence prey phenotypes both within and between generations. Parental and embryonic effects have been shown to operate independently in response to predation risk, but how they interact to shape offspring life history traits remains largely unknown. Here, we conducted experiments to examine the synergistic impacts of parental and embryonic experiences with predation risk on offspring size at emergence in the snail, Nucella lapillus, which is an ecologically important intermediate consumer on rocky intertidal shores. We found that when embryos were exposed to predation risk, the offspring of risk-experienced parents emerged larger than those of parents that had no risk experience. This response was not the result of increased development time, greater resource availability, or fewer emerging offspring, but may have occurred because both parental and embryonic experiences with risk increased growth efficiency, perhaps by reducing embryonic respiration rates under risk. Our results highlight the potential for organisms to be influenced by a complex history of environmental signals with important consequences for individual fitness and predator-prey interactions.

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.

Spatial scale mediates the effects of biodiversity on marine primary producers.

Most studies evaluating the effects of biodiversity on ecosystem functioning are conducted at a single location, limiting our understanding of how diversity-function relationships may change when measured across different spatial scales. We conducted a species-removal experiment at three sites nested in each of three regions along the rocky intertidal coastline of the Gulf of Maine, USA, to evaluate the potential for scale-dependent effects of species loss on the biomass of intertidal seaweed assemblages. We randomly assigned 50 plots in the mid-intertidal zone at each site to one of five treatments (n = 10 plots each): an unmanipulated control, a polyculture plot that contained our three target seaweed species, and three monoculture plots. We manipulated diversity by removing all non-target species from monoculture and polyculture plots, then removing additional biomass from polyculture plots, proportionate to species' relative abundances, so that the average amount removed from monoculture and polyculture plots was equivalent at each site. At the largest spatial scale, all sites considered together, after accounting for region and site nested within region seaweed diversity had consistent, positive effects on seaweed cover. Diverse polyculture plots always had higher cover than was predicted by the average performance of the component seaweed species and usually had higher cover than even the best-performing component species. Diversity effects weakened and became less consistent at smaller spatial scales, so that at the scale of individual sites, diverse polycultures only performed better than the average of monocultures ~40% of the time. Hence, our results indicate that weak and/or inconsistent biodiversity effects at the level of individual sites may scale up to stronger, more consistent effects at larger spatial scales. Quantitative summaries of biodiversity experiments conducted at the scale of individual sites do not capture this spatial aspect of biodiversity effects and may therefore underestimate the functional consequences of biodiversity loss.

Refuge quality impacts the strength of nonconsumptive effects on prey.

Prey often retreat into the safety of refuges for protection from predators. This shift into refuge can reduce foraging opportunities, escalating the costs of risk and the strength of nonconsumptive effects. Such costs, however, may be shaped by the variation in resources that refuges harbor for prey foraging (i.e., refuge quality), and change dynamically via impacts on prey state. Despite its potential importance, we lack an explicit understanding of how refuge quality impacts prey performance under risk. Using a rocky intertidal food chain, we examined the interaction between predation risk and the amount of resources available for prey in refuge. We found that refuges with more resources greatly reduce the costs of refuge use, and that nonconsumptive effects are thereby weakened by as much as one-half, with especially strong impacts on prey growth and growth efficiency. These results suggest that failure to consider refuge quality could result in overestimation of the negative effects associated with prey refuge use.

Parental effects enhance risk tolerance and performance in offspring.

Predation risk can strongly influence community dynamics through its effects on prey foraging decisions that often involve habitat shifts (i.e., from risky to refuge habitats). Although the within-generation effects of risk on prey are well appreciated, the effects of parental experience with risk on offspring decision-making and growth are poorly understood. The capacity of parents to prepare their offspring for potential risk exposure may be adaptive when the likelihood of eventual risk exposure is high and be instrumental in shaping how offspring allocate their foraging effort and habitat use. Using a simple rocky intertidal food chain, we examined the influence of parental exposure to predator risk cues on the behavior, foraging, and tissue maintenance of offspring exposed to the presence and absence of risk. We found that offspring of risk-experienced parents were bolder. When confronted with risk, these offspring spent more time out of refuge habitat, foraged more, and maintained more tissue than offspring of risk-free parents. Thus, parental experience with risk was most important when offspring were exposed to risk. These results suggest that the effects of parental experience with predation risk on offspring traits strongly shape the transmission of risk effects in ecological communities.

Effects of predation risk across a latitudinal temperature gradient.

The nonconsumptive effects (NCEs) of predators on prey behavior and physiology can influence the structure and function of ecological communities. However, the strength of NCEs should depend on the physiological and environmental contexts in which prey must choose between food and safety. For ectotherms, temperature effects on metabolism and foraging rates may shape these choices, thereby altering NCE strength. We examined NCEs in a rocky intertidal food chain across a latitudinal sea surface temperature gradient within the Gulf of Maine. The NCEs of green crabs (Carcinus maenas) on the foraging, growth, and growth efficiency of prey snails (Nucella lapillus) were consistent across a broad (~8.5 °C) temperature range, even though snails that were transplanted south consumed twice as many mussels (Mytilus edulis) and grew twice as much as snails that were transplanted north. The positive effects of warmer temperatures in the south allowed snails under high risk to perform similarly to or better than snails under low risk at cooler temperatures. Our results suggest that for prey populations residing at temperatures below their thermal optimum, the positive effects of future warming may offset the negative effects of predation risk. Such effects may be favorable to prey populations facing increased predation rates due to warmer temperatures associated with climate change. Attention to the direct and indirect effects of temperature on species interactions should improve our ability to predict the effects of climate change on ecological communities.

Thermal stress and predation risk trigger distinct transcriptomic responses in the intertidal snail Nucella lapillus.

Thermal stress and predation risk have profound effects on rocky shore organisms, triggering changes in their feeding behaviour, morphology and metabolism. Studies of thermal stress have shown that underpinning such changes in several intertidal species are specific shifts in gene and protein expression (e.g. upregulation of heat-shock proteins). But relatively few studies have examined genetic responses to predation risk. Here, we use next-generation RNA sequencing (RNA-seq) to examine the transcriptomic (mRNA) response of the snail Nucella lapillus to thermal stress and predation risk. We found that like other intertidal species, N. lapillus displays a pronounced genetic response to thermal stress by upregulating many heat-shock proteins and other molecular chaperones. In contrast, the presence of a crab predator (Carcinus maenas) triggered few significant changes in gene expression in our experiment, and this response showed no significant overlap with the snail's response to thermal stress. These different gene expression profiles suggest that thermal stress and predation risk could pose distinct and potentially additive challenges for N. lapillus and that genetic responses to biotic stresses such as predation risk might be more complex and less uniform across species than genetic responses to abiotic stresses such as thermal stress.

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.

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 'fear' 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.

Phylogenomic analyses reveal latitudinal population structure and polymorphisms in heat stress genes in the North Atlantic snail Nucella lapillus.

North Atlantic rocky intertidal species have been shaped by repeated glaciations and strong latitudinal temperature gradients, making them an excellent system to study postglacial phylogeography and thermal tolerance. Population genetics data from northwestern Atlantic species, however, often show patterns inconsistent with the prediction that high dispersal should generate weaker genetic structure among populations. Here, we used next-generation sequencing restriction-associated DNA tags (RAD-seq) and a transcriptome assembled from RNA-seq data to analyse the genetic structure of northwestern Atlantic populations of the low-dispersal intertidal snail Nucella lapillus. Although previous studies in this region have detected almost no genetic structure in N. lapillus, our phylogenomic approach identified a well-supported split between northern and southern clades. By comparing RAD-seq data and our transcriptome assembly, we identified thousands of fixed single-nucleotide polymorphisms (SNPs) between these latitudinal clades that map to protein-coding genes, including genes associated with heat stress tolerance. These fixed SNPs might represent loci under selection for different thermal regimes in the northwestern Atlantic.

Non-linear interactions between consumers and flow determine the probability of plant community dominance on Maine rocky shores.

Although consumers can strongly influence community recovery from disturbance, few studies have explored the effects of consumer identity and density and how they may vary across abiotic gradients. On rocky shores in Maine, recent experiments suggest that recovery of plant- or animal- dominated community states is governed by rates of water movement and consumer pressure. To further elucidate the mechanisms of consumer control, we examined the species-specific and density-dependent effects of rocky shore consumers (crabs and snails) on community recovery under both high (mussel dominated) and low flow (plant dominated) conditions. By partitioning the direct impacts of predators (crabs) and grazers (snails) on community recovery across a flow gradient, we found that grazers, but not predators, are likely the primary agent of consumer control and that their impact is highly non-linear. Manipulating snail densities revealed that herbivorous and bull-dozing snails (Littorina littorea) alone can control recovery of high and low flow communities. After ∼1.5 years of recovery, snail density explained a significant amount of the variation in macroalgal coverage at low flow sites and also mussel recovery at high flow sites. These density-dependent grazer effects were were both non-linear and flow-dependent, with low abundance thresholds needed to suppress plant community recovery, and much higher levels needed to control mussel bed development. Our study suggests that consumer density and identity are key in regulating both plant and animal community recovery and that physical conditions can determine the functional forms of these consumer effects.

The cost of safety: refuges increase the impact of predation risk in aquatic systems.

Although use of refuge habitats by prey can reduce their risk of predation, refuge use may also involve costs such as increased within-refuge competition for resources. Despite the ubiquity of refuge use by prey, it is unknown whether predator-induced use of refuges has widespread, negative nonconsumptive effects on prey growth, survival, and fecundity. We performed a meta-analysis of 204 studies of aquatic taxa containing data on 271 distinct predator--prey pairs and found strong evidence that the negative effect of predation risk on prey activity, growth, and fecundity increases when prey have access to refuge habitats. Moreover, the effect of refuge habitats on growth and activity depends upon whether the refuge provides partial or total protection from predators. These results suggest that prey choosing whether to use refuges face a trade-off between lowering the immediate risk of being consumed and increased nonconsumptive costs of refuge use. Our results suggest that changes in nonconsumptive effects in the presence of refuge habitats may alter prey population dynamics, coexistence, and metapopulation dynamics. Moreover, our results reveal key pragmatic considerations: the magnitude and direction of nonconsumptive effects may depend on the presence of refuge habitat and whether the refuge provides partial or total protection from predators.

How the informational environment shapes how prey estimate predation risk and the resulting indirect effects of predators.

Prey often behaviorally respond to changes in the intensity of predation risk, and these responses can often significantly shape community dynamics, but flexible responses to changes in predation risk require that prey have accurate and timely estimates of predation risk. We present a model of how a prey's environment should shape the cognitive rules they use to assess predation risk and present how these rules shape the effects predators have on prey and the prey's resources. In the model, prey can rely on a combination of a fixed estimate of predation risk and a flexible estimate of predation risk shaped by their recent experience. Prey relied more on their experience to estimate predation risk when predator cues were more reliable and when predator densities were lower. In addition, when the prey cognitive rules favored a greater use of their experience to estimate predation risk, the presence of predators caused larger nonconsumptive effects and generally smaller consumptive effects on prey and the prey's resources. These differences in prey cognition also altered the effects that alterations of cue reliability and predator densities had on prey and their resources.

Costs of predator-induced phenotypic plasticity: a graphical model for predicting the contribution of nonconsumptive and consumptive effects of predators on prey.

Defensive modifications in prey traits that reduce predation risk can also have negative effects on prey fitness. Such nonconsumptive effects (NCEs) of predators are common, often quite strong, and can even dominate the net effect of predators. We develop an intuitive graphical model to identify and explore the conditions promoting strong NCEs. The model illustrates two conditions necessary and sufficient for large NCEs: (1) trait change has a large cost, and (2) the benefit of reduced predation outweighs the costs, such as reduced growth rate. A corollary condition is that potential predation in the absence of trait change must be large. In fact, the sum total of the consumptive effects (CEs) and NCEs may be any value bounded by the magnitude of the predation rate in the absence of the trait change. The model further illustrates how, depending on the effect of increased trait change on resulting costs and benefits, any combination of strong and weak NCEs and CEs is possible. The model can also be used to examine how changes in environmental factors (e.g., refuge safety) or variation among predator-prey systems (e.g., different benefits of a prey trait change) affect NCEs. Results indicate that simple rules of thumb may not apply; factors that increase the cost of trait change or that increase the degree to which an animal changes a trait, can actually cause smaller (rather than larger) NCEs. We provide examples of how this graphical model can provide important insights for empirical studies from two natural systems. Implementation of this approach will improve our understanding of how and when NCEs are expected to dominate the total effect of predators. Further, application of the models will likely promote a better linkage between experimental and theoretical studies of NCEs, and foster synthesis across systems.