Environmental gradients influence biogeographic patterns of nonconsumptive predator effects on oysters

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, the 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

Nonconsumptive effects of a predator weaken then rebound over time

Predators can influence prey traits and behavior (nonconsumptive effects [NCEs]), often with cascading effects for basal resources and ecosystem function. But critiques of NCE experiments suggest that their duration and design produce results that describe the potential importance of NCEs rather than their actual importance. In light of these critiques, we re-evaluated a toadfish (predator), crab (prey), and oyster (resource) NCE-mediated trophic cascade. In a 4-month field experiment, we varied toadfish cue (NCE) and crab density ( approximating variation in predator consumptive effects, CE). Toadfish initially benefitted oyster survival by causing crabs to reduce consumption. But this NCE weakened over time (possibly due to prey hunger), so that after 2 months, crab density (CE) dictated oyster survivorship, regardless of cue. However, the NCE ultimately re-emerged on reefs with a toadfish cue, increasing oyster survivorship. At no point did the effect of toadfish cue on mud crab foraging behavior alter oyster population growth or sediment organic matter on the reef, which is a measure of benthic-pelagic coupling. Instead, both decreased with increasing crab density. Thus, within a system shown to exhibit strong NCEs in short-term experiments (days) our study supported predictions from theoretical models: (a) within the generation of individual prey, the relative influence of NCEs appears to cycle over longer time periods (months); and (b) predator CEs, not NCEs, drive longer-term resource dynamics and ecosystem function. Thus, our study implies that the impacts of removing top predators via activities such as hunting and overfishing will cascade to basal resources and ecosystem properties primarily through density-mediated interactions

Regional environmental variation and local species interactions influence biogeographic structure on oyster reefs

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 prevalent 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

Genetic diversity and phenotypic variation within hatchery-produced oyster cohorts predict size and success in the field

The rapid growth of the aquaculture industry to meet global seafood demand offers both risks and opportunities for resource management and conservation. In particular, hatcheries hold promise for stock enhancement and restoration, yet cultivation practices may lead to enhanced variation between populations at the expense of variation within populations, with uncertain implications for performance and resilience. To date, few studies have assessed how production techniques impact genetic diversity and population structure, as well as resultant trait variation in and performance of cultivated offspring. We collaborated with a commercial hatchery to produce multiple cohorts of the eastern oyster (Crassostrea virginica) from field-collected broodstock using standard practices. We recorded key characteristics of the broodstock (male : female ratio, effective population size), quantified the genetic diversity of the resulting cohorts, and tested their trait variation and performance across multiple field sites and experimental conditions. Oyster cohorts produced under the same conditions in a single hatchery varied almost twofold in genetic diversity. In addition, cohort genetic diversity was a significant positive predictor of oyster performance traits, including initial size and survival in the field. Oyster cohorts produced in the hatchery had lower within-cohort genetic variation and higher among-cohort genetic structure than adults surveyed from the same source sites. These findings are consistent with “sweepstakes reproduction” in oysters, even when manually spawned. A readily measured characteristic of broodstock, the ratio of males to females, was positively correlated with within-cohort genetic diversity of the resulting offspring. Thus, this metric may offer a tractable way both to meet short-term production goals for seafood demand and to ensure the capacity of hatchery-produced stock to achieve conservation objectives, such as the recovery of self-sustaining wild populations

Fish and invertebrate use of restored vs. natural oyster reefs in a shallow temperate latitude estuary

Coastal marine habitats continue to be degraded, thereby compelling large-scale restoration in many parts of the world. Whether restored habitats function similarly to natural habitats and fully recover lost ecosystem services is unclear. In estuaries, oyster reefs have been degraded by multiple anthropogenic activities including destructive fishing practices and reduced water quality, motivating restoration to maintain oyster fisheries and other ecosystem services, often at relatively high cost. We compared fish and invertebrate communities on recently restored (0–1 year post-restoration), older restored (3–4 years post-restoration), and natural oyster reefs to determine if and when restored reefs support functionally similar faunal communities. To test the influence of landscape setting on the faunal communities, the restored and natural reefs, as well as a control without reef present, were distributed among three landscapes (on the edge of salt marsh away from seagrass [salt marsh landscape], on mudflats [mudflat landscape], and near to seagrass and salt marsh [seagrass landscape]). Oyster density and biomass were greatest on restored reef habitat, as were those of non-oyster bivalve species. Total abundance of invertebrates was much greater on oyster reefs than in control plots, regardless of reef or landscape type, yet were frequently highest on older restored reefs. Meanwhile, juvenile fish densities were greatest on natural reefs, at intermediate densities on older restored reefs, and least abundant on controls. When comparing the effects of reef age and landscape setting, juvenile fish densities were greatest on younger reefs within the mudflat landscape. Collectively, these results indicate that oyster reefs harbor higher densities of resident invertebrate prey, which may explain why reef habitat is also important for juvenile fish. Laboratory and field experiments supported the notion that gag grouper (a predatory demersal fish) forage more effectively on oyster reefs than on unstructured mud bottom, whereas our experiments suggest that flounders that utilize oyster reefs likely forage on adjacent mud bottom. Because landscape setting influenced fish and invertebrate communities on restored reefs, the ecological consequences of landscape setting should be incorporated into restoration decision making and site selection to enhance the recovery of ecosystem goods and services

Regional environmental variation and local species interactions influence biogeographic structure on oyster reefs

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 prevalent 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