skip to main content

Title: Environmental forcing and predator consumption outweigh the nonconsumptive effects of multiple predators on oyster reefs

The ability to predict how predators structure ecosystems has been shown to depend on identifying both consumptive effects (CEs) and nonconsumptive effects (NCEs) of predators on prey fitness. Prey populations may also be affected by interactions between multiple predators across life stages of the prey and by environmental factors such as disturbance. However, the intersection of these multiple drivers of prey dynamics has yet to be empirically evaluated. We addressed this knowledge gap using eastern oysters (Crassostrea virginica), a species known to suffer NCEs, as the focal prey. Over 4 months, we manipulated orthogonally the life stage (none, juvenile, adult, or both) at which oysters experienced simulated predation (CE) and exposure to olfactory cues of a juvenile oyster predator (crab), adult predator (conch), sequentially the crab and then the conch, or none. We replicated this experiment at three sites along an environmental gradient in a Florida (USA) estuary. For both juvenile and adult oysters, survival was reduced solely by CEs, and variation in growth was best explained by among‐site variation in water flow, with a much smaller and negative effect of predator cue. Adults exposed to conch cue exhibited reduced growth (an NCE), but this effect was outweighed by more » a positive CE on growth: Surviving oysters grew faster at lower densities. Finally, conch cue reduced larval settlement (another NCE), but this was swamped by among‐site variation in larval supply. This research highlights how strong environmental gradients and predator CEs may outweigh the influence of NCEs, even in prey known to respond to predator cues. These findings serve as a cautionary tale for the importance of evaluating NCE processes over temporal scales and across environmental gradients relevant to prey demography.

« less
 ;  ;  
Award ID(s):
1820540 1736943
Publication Date:
Journal Name:
Wiley Blackwell (John Wiley & Sons)
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    When prey alter behavioral or morphological traits to reduce predation risk, they often incur fitness costs through reduced growth and reproduction as well as increased mortality that are known as nonconsumptive effects (NCEs). Environmental context and trophic structure can individually alter the strength of NCEs, yet the interactive influence of these contexts in natural settings is less understood. At six sites across 1000 km of the Southeastern Atlantic Bight (SAB), we constructed oyster reefs with one, two, or three trophic levels and evaluated the traits of focal juvenile oysters exposed to predation risk cues. We monitored environmental variables (water flow velocity, microalgal resources, and oyster larval recruitment) that may have altered how oysters respond to risk, and we also assessed the cost of trait changes to oyster mortality and growth when they were protected from direct predatory loss. Regardless of trophic structure, we found that oyster shell strength and natural oyster recruitment peaked at the center of the region. This high recruitment negated the potential for NCEs by smothering and killing the focal oysters. Also independent of trophic structure, focal oysters grew the most at the northernmost site. In contrast to, and perhaps because of, these strong environmental effects, themore »oyster traits of condition index and larval recruitment were only suppressed by the trophic treatment with a full complement of risk cues from intermediate and top predators at just the southernmost site. But at this same site, statistically significant NCEs on oyster growth and mortality were not detected. More strikingly, our study demonstrated environmental gradients that differentially influence oysters throughout the SAB. In particular, the results of our trophic manipulation experiment across these gradients suggest that in the absence of predation, environmental differences among sites may overwhelm the influence of NCEs on prey traits and population dynamics.

    « less
  2. Abstract

    Although species interactions are often assumed to be strongest at small spatial scales, they can interact with regional environmental factors to modify food web dynamics across biogeographic scales. The eastern oyster (Crassostrea virginica) is a widespread foundational species of both ecological and economic importance. The oyster and its associated assemblage of fish and macroinvertebrates is an ideal system to investigate how regional differences in environmental variables influence trophic interactions and food web structure. We quantified multiple environmental factors, oyster reef properties, associated species, and trophic guilds on intertidal oyster reefs within 10 estuaries along 900 km of the southeastern United States. Geographical gradients in fall water temperature and mean water depth likely influenced regional (i.e., the northern, central and southern sections of the SAB) variation in oyster reef food web structure. Variation in the biomass of mud crabs, an intermediate predator, was mostly (84.1%) explained by reefs within each site, and did not differ substantially among regions; however, regional variation in the biomass of top predators and of juvenile oysters also contributed to biogeographic variation in food web structure. In particular, region explained almost half (40.2%) of the variation in biomass of predators of blue crab, a top predator that was prevalentmore »only in the central region where water depth was greater. Field experiments revealed that oyster mortality due to predation was greatest in the central region, suggesting spatial variation in the importance of trophic cascades. However, high oyster recruitment in the middle region probably compensates for this enhanced predation, potentially explaining why relatively less variation (17.9%) in oyster cluster biomass was explained by region. Region also explained over half of the variation in biomass of mud crab predators (55.2%), with the southern region containing almost an order of magnitude more biomass than the other two regions. In this region, higher water temperatures in the fall corresponded with higher biomass of fish that consume mud crabs and of fish that consume juvenile and forage fish, whereas biomas of their prey (mud crabs and juvenile and forage fish, respectively) was generally low in the southern region. Collectively, these results show how environmental gradients interact with trophic cascades to structure food webs associated with foundation species across biogeographic regions.

    « less
  3. Abstract

    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 changingmore »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.

    « less
  4. Abstract

    Predators affect community structure by influencing prey density and traits, but the importance of these effects often is difficult to predict. We measured the strength of blue crab predator effects on mud crab prey consumption of juvenile oysters across a flow gradient that inflicts both physical and sensory stress to determine how the relative importance of top predator density‐mediated indirect effects (DMIEs) and trait‐mediated indirect effects (TMIEs) change within systems. Overall, TMIEs dominated in relatively benign flow conditions where blue crab predator cues increased oyster survivorship by reducing mud crab–oyster consumption. Blue crab DMIEs became more important in high sensory stress conditions, which impaired mud crab perception of blue crab chemical cues. At high physical stress, the environment benefitted oyster survival by physically constraining mud crabs. Thus, factors that structure communities may be predicted based on an understanding of how physical and sensory performances change across environmental stress gradients.

  5. Abstract

    Mesopredator release following top predator loss may reduce biodiversity and harm foundation species. We investigated the potential for moderate environmental changes to trigger mesopredator release by disrupting the foraging ability of top predators without affecting their abundance by performing an in situ experiment designed to isolate the magnitude of mesopredator effects on oyster reefs (Crassostrea virginica). In estuaries, fishes occupy upper trophic levels. Most are visual foragers and become less effective predators in high turbidity. Communities were 10% more diverse, fish predation was 20% higher, and oyster recruitment four times higher in low turbidity. Crab mesopredators were 10% larger and 260% more abundant in high turbidity. Caging treatments to exclude mesopredators significantly affected communities in high but not low turbidity. Oysters had 150% stronger shells in turbid areas, a known response to crabs that was indicative of higher crab abundance. These findings indicated that increased turbidity attenuated fish foraging ability without disrupting the foraging ability of mesopredators (e.g., crabs) that forage by chemoreception. Larger and more numerous crab mesopredators significantly affected oyster reef community structure as well as the survival and growth of oysters in turbid environments. In environments where apex predators and mesopredators utilize different sensory mechanisms, sensory‐mediated mesopredatormore »release may occur when conditions affect the foraging ability of higher order predators but not their prey.

    « less