Project

Marine global change and animal behaviour

Goal: Ongoing research investigating the effects of global change on marine animal behaviour.

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Jeff C. Clements
added a research item
Ocean acidification-decreasing oceanic pH resulting from the uptake of excess atmospheric CO2 has the potential to affect marine life in the future. Among the possible consequences , a series of studies on coral reef fish suggested that the direct effects of acidification on fish behavior may be extreme and have broad ecological ramifications. Recent studies documenting a lack of effect of experimental ocean acidification on fish behavior, however, call this prediction into question. Indeed, the phenomenon of decreasing effect sizes over time is not uncommon and is typically referred to as the "decline effect." Here, we explore the consistency and robustness of scientific evidence over the past decade regarding direct effects of ocean acidification on fish behavior. Using a systematic review and meta-analysis of 91 studies empirically testing effects of ocean acidification on fish behavior, we provide quantitative evidence that the research to date on this topic is characterized by a decline effect, where large effects in initial studies have all but disappeared in subsequent studies over a decade. The decline effect in this field cannot be explained by 3 likely biological explanations, including increasing proportions of studies examining (1) cold-water species; (2) nonolfactory-associated behaviors; and (3) nonlarval life stages. Furthermore , the vast majority of studies with large effect sizes in this field tend to be characterized by low sample sizes, yet are published in high-impact journals and have a disproportionate influence on the field in terms of citations. We contend that ocean acidification has a negligible direct impact on fish behavior, and we advocate for improved approaches to minimize the potential for a decline effect in future avenues of research.
Jeff C. Clements
added a research item
Startle response behaviours are important in predator avoidance and escape for a wide array of animals. For many marine invertebrates, however, startle response behaviours are understudied, and the effects of global change stressors on these responses are unknown. We exposed two size classes of blue mussels (Mytilus edulis × trossulus) to different combinations of temperature (15 and 19 °C) and pH (8.2 and 7.5 pHT) for three months and subsequently measured individual time to open following a tactile predator cue (i.e., startle response time) over a series of four consecutive trials. Time to open was highly repeatable on the short-term and decreased linearly across the four trials. Individuals from the larger size class had a shorter time to open than their smaller-sized counterparts. High temperature increased time to open compared to low temperature, while pH had no effect. These results suggest that bivalve time to open is repeatable, related to relative vulnerability to predation, and affected by temperature. Given that increased closure times impact feeding and respiration, the effect of temperature on closure duration may play a role in the sensitivity to ocean warming in this species and contribute to ecosystem-level effects.
Jeff C. Clements
added a research item
Ocean acidification – decreasing oceanic pH resulting from the uptake of excess atmospheric CO2 – has the potential to affect marine life in the future. Among the possible consequences, a series of studies on coral reef fishes suggested that the direct effects of acidification on fish behaviour may be extreme and have broad ecological ramifications. Recent studies documenting a lack of effect of experimental ocean acidification on fish behaviour, however, call this prediction into question. Indeed, the phenomenon of decreasing effect sizes over time is not uncommon and is typically referred to as the “decline effect”. Here, we explore the consistency and robustness of scientific evidence over the past decade regarding direct effects of ocean acidification on fish behaviour. Using a systematic review and meta-analysis of 91 studies empirically testing effects of ocean acidification on fish behaviour, we provide quantitative evidence that the research to date on this topic is characterized by the decline effect, where large effects in initial studies have all but disappeared in subsequent studies over a decade. The decline effect in this field cannot be explained by three likely biological explanations, including increasing proportions of studies examining (1) cold-water species, (2) non-olfactory associated behaviours, and (3) non-larval life stages. Furthermore, the vast majority of studies with large effect sizes in this field tend to be characterized by low sample sizes, yet are published in high impact journals and have a disproportionate influence on the field in terms of citations. We contend that ocean acidification has a negligible direct impact on fish behaviour, and we advocate for improved approaches to minimize the potential for a decline effect in future avenues of research.
Jeff C. Clements
added a research item
Ocean acidification is expected to affect marine organisms in the near future. Furthermore, abrupt short-term fluctuations in seawater pCO2 characteristic of near-short coastal regions and high-density aquaculture sites currently have the potential to influence organismal and community functioning by altering animal behaviour. While anti-predator responses in fishes exposed to elevated pCO2 are well documented, such responses in benthic marine invertebrates are poorly studied. We used high frequency, non-invasive biosensors to test whether or not short term (3-week) exposure to elevated pCO2 could impact behavioural responses to the threat of predation in adult Mediterranean mussels from Galicia on the northwestern coast of Spain. Predator alarm cues (crushed conspecifics) resulted in a prolonged (1 h) reduction in the degree of valve opening (−20%) but had no clear effect on overall valve movement activity, while elevated pCO2 did not affect either response. Our results add to the increasing body of evidence suggesting that the effects of end-of-century pCO2 levels on marine animal behaviour are likely weak. Nonetheless, longer-term exposures spanning multiple generations are needed to better understand how ocean acidification might impact behavioural responses to predation in marine bivalves.
Jeff C. Clements
added a research item
Apart from ocean acidification, hypoxia is another stressor to marine organisms, especially those in coastal waters. Their interactive effects of elevated CO2 and hypoxia on the physiological energetics in mussel Mytilus edulis were evaluated. Mussels were exposed to three pH levels (8.1, 7.7, 7.3) at two dissolved oxygen levels (6 and 2 mg L−1) and clearance rate, absorption efficiency, respiration rate, excretion rate, scope for growth and O: N ratio were measured during a14-day exposure. After exposure, all parameters (except excretion rate) were significantly reduced under low pH and hypoxic conditions, whereas excretion rate was significantly increased. Additive effects of low pH and hypoxia were evident for all parameters and low pH appeared to elicit a stronger effect than hypoxia (2.0 mg L−1). Overall, hypoxia can aggravate the effects of acidification on the physiological energetics of mussels, and their populations may be diminished by these stressors.
Jeff C. Clements
added a research item
Biological interactions between predators and prey constitute a key component of the ecology and evolution of marine systems, and animal behavior can affect the outcome of predator–prey interactions. It has been recently demonstrated that CO2-induced ocean acidification can alter the behavior of marine organisms and potentially alter predator–prey dynamics. This study combines both quantitative (meta-analysis) and qualitative approaches to review the effects of ocean acidification on behavioral prey defenses in marine invertebrates. A systematic literature search identified 34 studies that experimentally assessed behavioral defenses under elevated pCO2 spanning three phyla: crustaceans, echinoderms, and molluscs. A meta-analysis suggested that exposure to elevated seawater pCO2 can negatively affect behavioral defenses in bivalve molluscs and malacostracan crustaceans. By contrast, defenses of cephalopod molluscs seem to be positively impacted by elevated pCO2, whereas gastropods and echinoids appear unaffected. A qualitative assessment of studies on combined effects of ocean acidification and warming revealed that combined effects typically differ from ocean acidification–only effects. Based on a qualitative assessment of three studies to date, neurological interference of GABAA receptors under elevated pCO2 may play a major role in ocean acidification effects on prey defense behaviors; however, more research is needed, and other mechanistic underpinnings are also important to consider. Ultimately, the results of this study suggest that behavioral prey defenses in some shellfish taxa may be vulnerable to ocean acidification, that the effects of ocean acidification are often different under warming scenarios than under present-day temperature scenarios, and that GABAA interference may be an important mechanism underpinning behavioral responses of shellfish prey under ocean acidification. Despite the importance of shellfish behavioral defenses in the ecology and evolution of marine biological communities, however, research to date has only scraped the surface in understanding ocean acidification effects. Increased research efforts on the effects of multiple stressors, acclimation and adaptation, environmental variability, and complex situational and ecological contexts are needed. Studies of fish behavioral defenses under ocean acidification can help streamline hypotheses and experimental approaches, particularly given the similar effects of elevated pCO2 on GABAA function.
Jeff C. Clements
added a research item
While ocean acidification (OA) studies relating to marine animal behaviour have increased in recent years, the behavioural effects of OA on shellfish are relatively understudied, even though marine shellfish exhibit a wealth of behaviours that can modify organismal interactions and biological community functioning. Furthermore, detecting acute behavioural changes may provide a biological indicator of ecosystem stress and/or an early-warning system for aquaculture operations. This paper highlights a new and emerging technology – high-frequency, non-invasive (HFNI) electromagnetic-based biosensors – that can be used to document acute and long-term effects of elevated CO2 on the valve gaping behaviour of marine bivalves. An overview of the technology is presented and the current and potential uses of these biosensors in OA-shellfish behaviour research are highlighted, along with current limitations and next steps. We find that while a handful of studies have used these biosensors to test for effects of OA on bivalve valve gaping behaviour, their potential for testing critical and novel hypotheses regarding OA effects in a broader range of shellfish taxa is currently under-utilized. Ultimately, this paper provides a basis for expanding OA-shellfish behaviour research through the use of HFNI electromagnetic biosensors.
Jeff C. Clements
added 8 research items
Sediment acidification is known to influence the burrowing behaviour of juvenile marine bivalves. Unlike the alteration of behaviour by ocean acidification (OA) observed in many marine organisms, this burrowing response to present-day variation in sediment pH is likely adaptive in that it allows these organisms to avoid shell dissolution. However, the consequences of global climate stressors on these burrowing responses have yet to be tested. Further, while neurotransmitter interference appears to be linked to alteration of behaviour by OA in marine vertebrates, the mechanism(s) controlling the burrowing responses of juvenile bivalves in response to present-day variation in sediment acidification remain unknown. We tested the interactive effects of elevated seawater temperature and sediment acidification on juvenile soft-shell clam burrowing behaviour, (measured as the proportion of clams burrowed into sediment) to test for effects of elevated temperature on bivalve burrowing responses to sediment acidification. We also examined whether GABAA-like receptor interference could act as a potential biological mechanism underpinning the burrowing responses of these clams to present-day variation in sediment acidification. Results showed that both elevated temperature and gabazine administration reduced the proportion of clams that avoided burrowing into low pH sediment. These results suggest that CO2 effects on neurophysiology (GABAA receptors) can act to mediate adaptive behaviours in juvenile marine bivalves, but that these behaviours may be adversely affected by elevated temperature.
Recently, the impacts of ocean acidification (OA) on marine animal behaviour have garnered considerable attention, as they can impact biological interactions and, in turn, ecosystem structure and functioning. We synthesize current understanding of how a high CO2 ocean may impact animal behaviour, elucidate critical unknowns, and provide suggestions for future research by reviewing current published literature surrounding OA and marine behaviour. Although studies have focused equally on vertebrates and invertebrates, vertebrate studies have primarily focused on coral reef fishes, in contrast to the broader diversity of invertebrate taxa studied. A meta-analysis of the direction and magnitude of change in behaviours from current conditions under OA scenarios suggests primarily negative impacts that vary depending on species, ecosystem, and behaviour. The interactive effects of co-occurring environmental parameters with CO2 elicit different effects than those observed under elevated CO2 alone, though only 12% of studies have incorporated multiple factors; only one study has examined the effects of carbonate system variability on the behaviour of a marine animal. Altered GABAA receptor functioning under elevated CO2 appears responsible for many behavioural responses; however, this mechanism is unlikely to be universal. We recommend a new focus on determining the behavioural effects of elevated CO2 in the context of multiple environmental drivers and future carbonate system variability, and gaining a better mechanistic understanding of the association between acid-base regulation and GABAA receptor functioning. This knowledge could explain observed species-specificity in behavioural responses to OA and lend to a unifying theory of OA effects on marine animal behaviour.
While many studies document effects of elevated pCO 2 on coastal organisms, the environmental variability characteristic of coastal regions is often not directly tested. We tested for effects of elevated pCO 2 on the valve gaping activity of adult eastern oysters (Crassostrea virginica) in response to acute heat shock that can occur in nearshore shallow coastal waters. In two consecutive experimental trials, oysters (n = 4) wired with Hall Effect biosensors (that measured valve gaping at one-second intervals) were exposed for 10 days at six different pCO 2 treatments spanning a range currently observed in nearshore coastal regions, and predicted under near-future ocean acidification. After the 10-day acclimation period, oysters from each pCO 2 treatment were exposed to a 3-hour heat shock assay (simulating a future heat wave; 11-1230°C) and valve gaping activity was monitored continuously. During the heat shock assays, valve gaping activity increased with increasing temperature and then ceased when temperature was reduced back to 10°C; however, these valve gaping rate increases during heat shock were not characteristic of overly-stressed oysters. Exposure to elevated pCO 2 had no effect on the valve gaping response of oysters to acute heat shock. Our results suggest that the valve gaping responses of adult eastern oysters to acute temperature increases are unaffected by short-term elevations in seawater pCO 2. Future studies incorporating the roles of local adaptation, food availability, and direct functional consequences of valve gaping (e.g. physiological rates, predator avoidance, response to environmental toxins) are warranted.
Jeff C. Clements
added a project goal
Ongoing research investigating the effects of global change on marine animal behaviour.