Effects of landscape setting on oyster reef structure and function largely persist more than a decade post-restoration

Long-term monitoring is vital to understanding the efficacy of restoration approaches and how restoration may enhance ecosystem functions. We revisited restored oyster reefs 13 years post-restoration and quantified the resident and transient fauna that utilize restored reefs in three differing landscape contexts: on mudflats isolated from vegetated habitat, along the edge of salt marsh, and in between seagrass and salt marsh habitat. Differences observed 1–2 years post-restoration in reef development and associated fauna within reefs restored on mudflats versus adjacent to seagrass/salt marsh and salt marsh-only habitats persisted more than 10 years post-restoration. Reefs constructed on open mudflat habitats had the highest densities of oysters and resident invertebrates compared to those in other landscape contexts, although all restored reefs continued to enhance local densities of invertebrate taxa (e.g. bivalves, gastropods, decapods, polychaetes, etc.). Catch rates of juvenile fishes were enhanced on restored reefs relative to controls, but to a lesser extent than directly post-restoration, potentially because the reefs have grown vertically within the intertidal and out of the preferred inundation regime of small juvenile fishes. Reef presence and landscape setting did not augment the catch rates of piscivorous fishes in passive gill nets, similar to initial findings; however, hook-and-line catch rates were greater on restored reefs than non-reef controls. We conclude that ecosystem functions and associated services provided by restored habitats can vary both spatially and temporally; therefore, a better understanding of how service delivery varies among landscape setting and over time should enhance efforts to model these processes and restoration decision-making

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

Threat of Predation Does Not Affect Crassostrea virginica Filtration

Biotic interactions can structure ecological communities and influence ecosystem functioning. As ecosystem engineers and filter feeders, bivalves often have disproportionately large effects on ecosystem functioning. They also utilize numerous morphological and behavioral responses to reduce predation, which can include changes in their filtration rates. To test the response of Crassostrea virginica filtration rates to the presence of predators, juvenile and adult oysters were separately exposed to varying types of predation risk from Callinectes sapidus and Panopeus herbstii in outdoor mesocosms. Water column chlorophyll a concentrations and crab behavior were measured over the duration of the experiment. Predation risk had no effect on oyster reef drawdown of chlorophyll a, which suggests that this important ecosystem function of oyster reefs is not mediated by behaviorally induced predator effects. Therefore, efforts to model how oyster predators influence filtration rates and associated ecosystem services should focus primarily on the factors that influence oyster mortality rather than predator effects on oyster behavior

Juvenile Eastern Oysters More Resilient to Extreme Ocean Acidification than Their Mud Crab Predators

Ocean acidification is predicted to impair marine calcifiers' abilities to produce shells and skeletons. We conducted laboratory experiments investigating the impacts of CO2-induced ocean acidification (pCO2 = 478–519, 734–835, 8,980–9,567; Ωcalcite = 7.3–5.7, 5.6–4.3, 0.6–0.7) on calcification rates of two estuarine calcifiers involved in a classic predator-prey model system: adult Panopeus herbstii (Atlantic mud crab) and juvenile Crassostrea virginica (eastern oyster). Both oyster and crab calcification rates significantly decreased at the highest pCO2 level. Notably, however, oysters maintained positive net calcification rates in the highest pCO2 treatment that was undersaturated with respect to calcite, while mud crabs exhibited net dissolution (i.e., net loss of shell mass) in calcite-undersaturated conditions. Secondary electron imaging of oyster shells revealed minor microstructural alterations in the moderate-pCO2 treatment, and major microstructural and macrostructural changes (including shell dissolution, delamination of periostracum) in the high-pCO2 treatment. These results underscore the threat that ocean acidification poses for marine organisms that produce calcium carbonate shells, illustrate the strong biological control that some marine calcifiers exert over their shell-building process, and shows that ocean acidification differentially impacts the crab and oyster species involved in this classical predator-prey model system

Consumption rates vary based on the presence and type of oyster structure: A seasonal and latitudinal comparison

As oyster reefs continue to decline worldwide, interest has turned to restoration and aquaculture as ways to sustain the services derived from these ecologically and economically valuable habitats. While biogenic oyster reefs support a variety of ecological functions, it remains unclear whether aquaculture and its associated infrastructure can provide equivalent levels of functioning. Here, we compare consumption rates by fish and invertebrate predators, a key indicator of energy transfer between trophic levels, between reef and aquaculture habitats for the Eastern oyster (Crassostrea virginica) in the Western Atlantic. We deployed a standardized dried squid prey item (‘Squidpops’) in three different structured settings: biogenic oyster reefs, on-bottom aquaculture, and off-bottom aquaculture. For each habitat treatment, we also implemented an adjacent control in nearby bare (unstructured) sediment. These assays were repeated across three seasons at twelve locations spanning 900 km of coastline. We found that consumption rates were contingent on the presence and type of structure: they were highest near off-bottom floating bags, and the difference between structured habitats and unstructured controls was also greatest for this treatment. Moreover, at large temporal and spatial scales, consumption rates increased with increasing temperature, and independently declined with increasing latitude. Our study revealed that certain types of aquaculture support comparable or greater consumption rates than natural reefs, suggesting an important role for this novel structured habitat in maintaining coastal food webs

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

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

Effects of habitat fragmentation on Zostera marina seed distribution

Habitat fragmentation is a process which can alter the spatial configuration and reduce the overall area of a habitat. This generally results in a degradation of habitat functioning. Fragmentation of seagrass (Zostera marina) beds has become increasingly common, and it may threaten the valuable ecosystem services they provide. Sexual reproduction through flowering and seed dispersal could contribute to the species' potential resiliency by reducing its vulnerability to fragmentation. We investigated whether the proportion and density of flowering Z. marina shoots, and subsequently the density and distribution of seeds, differed between fragmented and continuous beds. Our results revealed that while flowering effort did not differ between the two bed types, seed density was significantly reduced in fragmented versus continuous beds. Further, seed distributions were altered in fragmented beds when compared to continuous beds, both within and directly outside the bed's boundaries. Seagrass patch size positively influenced seed density, with lower seed densities in small patches. Fragmented beds consistently contained fewer seeds per-unit-area than continuous beds, regardless of bed seagrass area and flowering effort. Collectively, these results emphasize the vulnerability of Z. marina to habitat fragmentation by demonstrating a negative effect on seed density and an impact on seed distribution, which likely reduces the potential advantages of sexual reproduction for bed growth and resiliency to perturbations

Oyster reefs as carbon sources and sinks

Carbon burial is increasingly valued as a service provided by threatened vegetated coastal habitats. Similarly, shellfish reefs contain significant pools of carbon and are globally endangered, yet considerable uncertainty remains regarding shellfish reefs’ role as sources (+) or sinks (-) of atmospheric CO2. While CO2 release is a by-product of carbonate shell production (then burial), shellfish also facilitate atmospheric-CO2 drawdown via filtration and rapid biodeposition of carbon-fixing primary producers. We provide a framework to account for the dual burial of inorganic and organic carbon, and demonstrate that decade-old experimental reefs on intertidal sandflats were net sources of CO2 (7.1 ± 1.2 MgC ha-1 yr-1 (m ± s.e.)) resulting from predominantly carbonate deposition, whereas shallow subtidal reefs (-1.0 ± 0.4 MgC ha-1 yr-1) and saltmarsh-fringing reefs (-1.3 ± 0.4 MgC ha-1 yr-1) were dominated by organic-carbon-rich sediments and functioned as net carbon sinks (on par with vegetated coastal habitats). These landscape-level differences reflect gradients in shellfish growth, survivorship and shell bioerosion. Notably, down-core carbon concentrations in 100- to 4000-year-old reefs mirrored experimental-reef data, suggesting our results are relevant over centennial to millennial scales, although we note that these natural reefs appeared to function as slight carbon sources (0.5 ± 0.3 MgC ha-1 yr-1). Globally, the historical mining of the top metre of shellfish reefs may have reintroduced more than 400 000 000 Mg of organic carbon into estuaries. Importantly, reef formation and destruction do not have reciprocal, counterbalancing impacts on atmospheric CO2 since excavated organic material may be remineralized while shell may experience continued preservation through reburial. Thus, protection of existing reefs could be considered as one component of climate mitigation programmes focused on the coastal zone