Legacy of past exposure to hypoxia and warming regulates an ecosystem service provided by oysters.

Climate change is having substantial impacts on organism fitness and ability to deliver critical ecosystem services, but these effects are often examined only in response to current environments. Past exposure to stress can also affect individuals via carryover effects, and whether these effects scale from individuals to influence ecosystem function and services is unknown. We explored within-generation carryover effects of two coastal climate change stressors-hypoxia and warming-on oyster (Crassostrea virginica) growth and nitrogen bioassimilation, an important ecosystem service. Oysters were exposed to a factorial combination of two temperature and two diel-cycling dissolved oxygen treatments at 3-months-old and again 1 year later. Carryover effects of hypoxia and warming influenced oyster growth and nitrogen storage in complex and context-dependent ways. When operating, carryover effects of single stressors generally reduced oyster nitrogen bioassimilation and relative investment in tissue versus shell growth, particularly in warm environments, while early life exposure to multiple stressors generally allowed oysters to perform as well as control oysters. When extrapolated to the reef scale, carryover effects decreased nitrogen stored by modeled oyster reefs in most conditions, with reductions as large as 41%, a substantial decline in a critical ecosystem service. In some scenarios, however, carryover effects increased nitrogen storage by modeled oyster reefs, again highlighting the complexity of these effects. Hence, even brief exposure to climate change stressors early in life may have persistent effects on an ecosystem service 1 year later. Our results show for the first time that within-generation carryover effects on individual phenotypes can impact processes at the ecosystem scale and may therefore be an overlooked factor determining ecosystem service delivery in response to anthropogenic change.

Context-dependent carryover effects of hypoxia and warming in a coastal ecosystem engineer.

Organisms are increasingly likely to be exposed to multiple stressors repeatedly across ontogeny as climate change and other anthropogenic stressors intensify. Early life stages can be particularly sensitive to environmental stress, such that experiences early in life can "carry over" to have long-term effects on organism fitness. Despite the potential importance of these within-generation carryover effects, we have little understanding of how they vary across ecological contexts, particularly when organisms are re-exposed to the same stressors later in life. In coastal marine systems, anthropogenic nutrients and warming water temperatures are reducing average dissolved oxygen (DO) concentrations while also increasing the severity of naturally occurring daily fluctuations in DO. Combined effects of warming and diel-cycling DO can strongly affect the fitness and survival of coastal organisms, including the eastern oyster (Crassostrea virginica), a critical ecosystem engineer and fishery species. However, whether early life exposure to hypoxia and warming affects oysters' subsequent response to these stressors is unknown. Using a multiphase laboratory experiment, we explored how early life exposure to diel-cycling hypoxia and warming affected oyster growth when oysters were exposed to these same stressors 8 weeks later. We found strong, interactive effects of early life exposure to diel-cycling hypoxia and warming on oyster tissue : shell growth, and these effects were context-dependent, only manifesting when oysters were exposed to these stressors again two months later. This change in energy allocation based on early life stress exposure may have important impacts on oyster fitness. Exposure to hypoxia and warming also influenced oyster tissue and shell growth, but only later in life. Our results show that organisms' responses to current stress can be strongly shaped by their previous stress exposure, and that context-dependent carryover effects may influence the fitness, production, and restoration of species of management concern, particularly for sessile species such as oysters.

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.

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.

Aquatic deoxygenation as a planetary boundary and key regulator of Earth system stability.

Planetary boundaries represent thresholds in major Earth system processes that are sensitive to human activity and control global-scale habitability and stability. These processes are interconnected such that movement of one planetary boundary process can alter the likelihood of crossing other boundaries. Here we argue that the observed deoxygenation of the Earth's freshwater and marine ecosystems represents an additional planetary boundary process that is critical to the integrity of Earth's ecological and social systems, and both regulates and responds to ongoing changes in other planetary boundary processes. Research on the rapid and ongoing deoxygenation of Earth's aquatic habitats indicates that relevant, critical oxygen thresholds are being approached at rates comparable to other planetary boundary processes. Concerted global monitoring, research and policy efforts are needed to address the challenges brought on by rapid deoxygenation, and the expansion of the planetary boundaries framework to include deoxygenation as a boundary helps to focus those efforts.

Global marine biosecurity and ship lay-ups: intensifying effects of trade disruptions.

Recent global trade disruptions, due to blockage of the Suez Canal and cascading effects of COVID-19, have altered the movement patterns of commercial ships and may increase worldwide invasions of marine non-indigenous species. Organisms settle on the hulls and underwater surfaces of vessels and can accumulate rapidly, especially when vessels remain stationary during lay-ups and delays. Once present, organisms can persist on vessels for long-periods (months to years), with the potential to release propagules and seed invasions as ships visit ports across the global transportation network. Shipborne propagules also may be released in increasing numbers during extended vessel residence times at port or anchor. Thus, the large scale of shipping disruptions, impacting thousands of vessels and geographic locations and still on-going for over two years, may elevate invasion rates in coastal ecosystems in the absence of policy and management efforts to prevent this outcome. Concerted international and national biosecurity actions, mobilizing existing frameworks and tools with due diligence, are urgently needed to address a critical gap and abate the associated invasion risks.

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.

Transgenerational Plasticity in Human-Altered Environments.

Our ability to predict how species will respond to human-induced rapid environmental change (HIREC) may depend upon our understanding of transgenerational plasticity (TGP), which occurs when environments experienced by previous generations influence phenotypes of subsequent generations. TGP evolved to help organisms cope with environmental stressors when parental environments are highly predictive of offspring environments. HIREC can alter conditions that favored TGP in historical environments by reducing parents' ability to detect environmental conditions, disrupting previous correlations between parental and offspring environments, and interfering with the transmission of parental cues to offspring. Because of the propensity to produce errors in these processes, TGP will likely generate negative fitness outcomes in response to HIREC, though beneficial fitness outcomes may occur in some cases.