Common fear molecules induce defensive responses in marine prey across trophic levels.

Predator-prey interactions are a key feature of ecosystems and often chemically mediated, whereby individuals detect molecules in their environment that inform whether they should attack or defend. These molecules are largely unidentified, and their discovery is important for determining their ecological role in complex trophic systems. Homarine and trigonelline are two previously identified blue crab (Callinectes sapidus) urinary metabolites that cause mud crabs (Panopeus herbstii) to seek refuge, but it was unknown whether these molecules influence other species within this oyster reef system. In the current study, homarine, trigonelline, and blue crab urine were tested on juvenile oysters (Crassostrea virginica) to ascertain if the same molecules known to alter mud crab behavior also affect juvenile oyster morphology, thus mediating interactions between a generalist predator, a mesopredator, and a basal prey species. Oyster juveniles strengthened their shells in response to blue crab urine and when exposed to homarine and trigonelline in combination, especially at higher concentrations. This study builds upon previous work to pinpoint specific molecules from a generalist predator's urine that induce defensive responses in two marine prey from different taxa and trophic levels, supporting the hypothesis that common fear molecules exist in ecological systems.

Induced defenses as a management tool: Shaping individuals to their environment.

Many prey species can adjust morphology to reduce predation risk in response to predator cues. Enhancing prey defenses using predator cues may improve survival of cultivated species and enhance species restoration efforts, but assessment of such benefits at industrially relevant scales is needed. We examined how raising a model foundation species, oysters (Crassostrea virginica), under commercial hatchery conditions with cues from two common predator species can improve survival across a variety of predator regimes and environmental conditions. Oysters responded to predators by growing stronger shells than controls, but had subtle variations in shell characteristics depending on the predator species. Predator-induced changes significantly increased oyster survival up to 600% and survivorship was maximized when cue source was matched with local predator regime. Overall, our findings demonstrate the utility of using predator cues to enhance the survival of target species across landscapes and highlight the opportunity to employ nontoxic methods to control pest-based mortality.

Barnacles as biological flow indicators.

Hydrodynamic stress shapes the flora and fauna that exist in wave-swept environments, alters species interactions, and can become the primary community structuring agent. Yet, hydrodynamics can be difficult to quantify because instrumentation is expensive, some methods are unreliable, and accurately measuring spatial and temporal differences can be difficult. Here, we explored the utility of barnacles as potential biological flow-indicators. Barnacles, nearly ubiquitous within estuarine environments, have demonstrated notable phenotypic plasticity in the dimensions of their feeding appendages (cirri) and genitalia in response to flow. In high flow, barnacles have shorter, stockier cirri with shorter setae; in low flow, barnacles have longer, thinner cirri with longer setae. By measuring the relative differences in cirral dimensions, comparative differences in flow among locations can be quantified. We tested our hypothesis that ivory barnacles (Amphibalanus eburneus) could be useful biological flow indicators in two experiments. First, we performed reciprocal transplants of A. eburneus between wave protected and wave exposed areas to assess changes in morphology over 4 weeks as well as if changes dissipated when barnacles were relocated to a different wave habitat. Then, in a second study, we transplanted barnacles into low (<5 cm/s) and high flow (>25 cm/s) environments that were largely free of waves and shielded half of the transplanted barnacles to lessen flow speed. In both experiments, barnacles had significant differences in cirral morphologies across high and low flow sites. Transplanting barnacles revealed phenotypic changes occur within two weeks and can be reversed. Further, ameliorating flow within sites did not affect barnacle morphologies in low flow but had pronounced effects in high flow environments, suggesting that flow velocity was the primary driver of barnacle morphology in our experiment. These results highlight the utility of barnacles as cheap, accessible, and biologically relevant indicators of flow that can be useful for relative comparisons of flow differences among sites.

Predator signaling of multiple prey on different trophic levels structures trophic cascades.

The capacity of an apex predator to produce nonconsumptive effects (NCEs) in multiple prey trophic levels can create considerable complexity in nonconsumptive cascading interactions, but these effects are poorly studied. We examined such effects in a model food web where the apex predator (blue crabs) releases chemical cues in urine that affect both the intermediate consumer (mud crabs seek shelter) and the basal prey (oysters are induced to grow stronger shells). Shelter availability and predator presence were manipulated in a laboratory experiment to identify patterns in species interactions. Then, experimentally induced and uninduced oysters were planted across high-quality and low-quality habitats with varying levels of shelter availability and habitat heterogeneity to determine the consistency of these patterns in the field. Oyster shell thickening in response to blue crab chemical cues generally protected oysters from mud crab predation in both the laboratory and in field environments that differed in predation intensity, structural complexity, habitat heterogeneity, and predator composition. However, NCEs on the intermediate predator (greater use of refugia) opposed the NCEs on oyster prey in the interior of oyster reefs while still providing survival advantages to basal prey on reef edges and bare substrates. Thus, the combined effects of changing movement patterns of intermediate predators and morphological defenses of basal prey create complex, but predictable, patterns of NCEs across landscapes and ecotones that vary in structural complexity. Generalist predators that feed on multiple trophic levels are ubiquitous, and their potential effects on NCEs propagating simultaneously to different trophic levels must be quantified to understand the role of NCEs in food webs.

Drift macroalgal distribution in northern Gulf of Mexico seagrass meadows.

Drift macroalgae, often found in clumps or mats adjacent to or within seagrass beds, can increase the value of seagrass beds as habitat for nekton via added food resources and structural complexity. But, as algal biomass increases, it can also decrease light availability, inhibit faunal movements, smother benthic communities, and contribute to hypoxia, all of which can reduce nekton abundance. We quantified the abundance and distribution of drift macroalgae within seagrass meadows dominated by turtle grass Thalassia testudinum across the northern Gulf of Mexico and compared seagrass characteristics to macroalgal biomass and distribution. Drift macroalgae were most abundant in areas with higher seagrass shoot densities and intermediate canopy heights. We did not find significant relationships between algal biomass and point measures of salinity, temperature, or depth. The macroalgal genera Laurencia and Gracilaria were present across the study region, Agardhiella and Digenia were collected in the western Gulf of Mexico, and Acanthophora was collected in the eastern Gulf of Mexico. Our survey revealed drift algae to be abundant and widespread throughout seagrass meadows in the northern Gulf of Mexico, which likely influences the habitat value of seagrass ecosystems.

Storms promote ecosystem resilience by alleviating fishing.

Marine ecosystems face numerous challenges from natural and anthropogenic sources. For example, excessive rainfall from storms rapidly lowers salinity, which can destroy coastal foundation species and their associated fauna [1], while fishing can alter coastal food webs, reduce biodiversity, and lower ecosystem resilience [2]. Concurrently, mass disruptions to fishing activity are common following disasters such as hurricanes, oil spills, and tsunamis, which may lead to increased populations of harvested species [3]. However, our understanding of how these disturbances interact to affect communities remains limited. We examined effects on estuarine communities following fishing disruptions and salinity changes caused by a tropical cyclone. Our results indicate that recreational fishing had large effects on fish populations that cascaded down the food web. Further, although destructive, hurricanes and other disturbances that simultaneously curtail human activities may promote recovery. VIDEO ABSTRACT.

Personality interacts with habitat quality to govern individual mortality and dispersal patterns.

Individual phenotypic differences are increasingly recognized as key drivers of ecological processes. However, studies examining the relative importance of these differences in comparison with environmental factors or how individual phenotype interacts across different environmental contexts remain lacking. We performed two field experiments to assess the concurrent roles of personality differences and habitat quality in mediating individual mortality and dispersal. We quantified the predator avoidance response of mud crabs, Panopeus herbstii, collected from low- and high-quality oyster reefs and measured crab loss in a caging experiment. We simultaneously measured the distance crabs traveled as well as the stability of personalities across reef quality in a separate reciprocal transplant experiment. Habitat quality was the primary determinant of crab loss, although the distance crabs traveled was governed by personality which interacted with habitat quality to control the fate of crabs. Here, crabs on low-quality reefs rapidly emigrated, starting with the boldest individuals, and experienced modest levels of predation regardless of personality. In contrast, both bold and shy crabs would remain on high-quality reefs for months where bolder individuals experienced higher predation risk. These findings suggest that personalities could produce vastly different population dynamics across habitat quality and govern community responses to habitat degradation.

Habitat quality mediates personality through differences in social context.

Assessing the stability of animal personalities has become a major goal of behavioral ecologists. Most personality studies have utilized solitary individuals, but little is known on the extent that individuals retain their personality across ecologically relevant group settings. We conducted a field survey which determined that mud crabs, Panopeus herbstii, remain scattered as isolated individuals on degraded oyster reefs while high quality reefs can sustain high crab densities (>10 m-2). We examined the impact of these differences in social context on personality by quantifying the boldness of the same individual crabs when in isolation and in natural cohorts. Crabs were also exposed to either a treatment of predator cues or a control of no cue throughout the experiment to assess the strength of this behavioral reaction norm. Crabs were significantly bolder when in groups than as solitary individuals with predator cue treatments exhibiting severally reduced crab activity levels in comparison to corresponding treatments with no predator cues. Behavioral plasticity depended on the individual and was strongest in the presence of predator cues. While bold crabs largely maintained their personality in isolation and group settings, shy crabs would become substantially bolder when among conspecifics. These results imply that the shifts in crab boldness were a response to changes in perceived predation risk, and provide a mechanism for explaining variation in behavioral plasticity. Such findings suggest that habitat degradation may produce subpopulations with different behavioral patterns because of differing social interactions between individual animals.

Predator-prey interactions mediated by prey personality and predator hunting mode.

Predator-prey interactions are important drivers in structuring ecological communities. However, despite widespread acknowledgement that individual behaviours and predator species regulate ecological processes, studies have yet to incorporate individual behavioural variations in a multipredator system. We quantified a prevalent predator avoidance behaviour to examine the simultaneous roles of prey personality and predator hunting mode in governing predator-prey interactions. Mud crabs, Panopeus herbstii, reduce their activity levels and increase their refuge use in the presence of predator cues. We measured mud crab mortality and consistent individual variations in the strength of this predator avoidance behaviour in the presence of predatory blue crabs, Callinectes sapidus, and toadfish, Opsanus tau We found that prey personality and predator species significantly interacted to affect mortality with blue crabs primarily consuming bold mud crabs and toadfish preferentially selecting shy crabs. Additionally, the strength of the predator avoidance behaviour depended upon the predation risk from the predator species. Consequently, the personality composition of populations and predator hunting mode may be valuable predictors of both direct and indirect predator-prey interaction strength. These findings support theories postulating mechanisms for maintaining intraspecies diversity and have broad implications for community dynamics.

The Influence of Diet Composition on Fitness of the Blue Crab, Callinectes sapidus.

The physiological condition and fecundity of an organism is frequently controlled by diet. As changes in environmental conditions often cause organisms to alter their foraging behavior, a comprehensive understanding of how diet influences the fitness of an individual is central to predicting the effect of environmental change on population dynamics. We experimentally manipulated the diet of the economically and ecologically important blue crab, Callinectes sapidus, to approximate the effects of a dietary shift from primarily animal to plant tissue, a phenomenon commonly documented in crabs. Crabs whose diet consisted exclusively of animal tissue had markedly lower mortality and consumed substantially more food than crabs whose diet consisted exclusively of seaweed. The quantity of food consumed had a significant positive influence on reproductive effort and long-term energy stores. Additionally, seaweed diets produced a three-fold decrease in hepatopancreas lipid content and a simultaneous two-fold increase in crab aggression when compared to an animal diet. Our results reveal that the consumption of animal tissue substantially enhanced C. sapidus fitness, and suggest that a dietary shift to plant tissue may reduce crab population growth by decreasing fecundity as well as increasing mortality. This study has implications for C. sapidus fisheries.