Escape response kinematics in two species of tropical shark: short escape latencies and high turning performance.

Accelerative manoeuvres, such as fast-starts, are crucial for fish to avoid predation. Escape responses are fast-starts that include fundamental survival traits for prey that experience high predation pressure. However, no previous study has assessed escape performance in neonate tropical sharks. We quantitatively evaluated vulnerability traits of neonate tropical sharks by testing predictions on their fast-start escape performance. We predicted (1) high manoeuvrability, given their high flexibility, but (2) low propulsive locomotion owing to the drag costs associated with pectoral fin extension during escape responses. Further, based on previous work on dogfish, Squalus suckleyi, we predicted (3) long reaction times (as latencies longer than teleosts, >20 ms). We used two-dimensional, high-speed videography analysis of mechano-acoustically stimulated neonate blacktip reef shark, Carcharhinus melanopterus (n=12), and sicklefin lemon shark, Negaprion acutidens (n=8). Both species performed a characteristic C-start double-bend response (i.e. two body bends), but single-bend responses were only observed in N. acutidens. As predicted, neonate sharks showed high manoeuvrability with high turning rates and tight turning radii (3-11% of body length) but low propulsive performance (i.e. speed, acceleration and velocity) when compared with similar-sized teleosts and S. suckleyi. Contrary to expectations, escape latencies were <20 ms in both species, suggesting that the neurophysiological system of sharks when reacting to a predatory attack may not be limited to long response times. These results provide a quantitative assessment of survival traits in neonate tropical sharks that will be crucial for future studies that consider the vulnerability of these sharks to predation.

Indirect predator effects influence behaviour but not morphology of juvenile coral reef Ambon damselfish Pomacentrus amboinensis.

A 6-week laboratory experiment exposed juvenile Ambon damselfish Pomacentrus amboinensis to visual and chemical cues of either a predator, a herbivore or a null control (sea water) and found no effect of predator cues on prey morphology (proportion of ocellus to eye diameter, body depth, standard length and fin area). Nonetheless, behaviour was significantly affected by predator presence, with prey less active and taking half as many feeding strikes when exposed to predators compared to fish from the null control. The presence of a herbivore also affected prey behaviour similar to that of the predator, suggesting that the presence of a non-predator may have important effects on development.

Microplastic exposure interacts with habitat degradation to affect behaviour and survival of juvenile fish in the field.

Coral reefs are degrading globally due to increased environmental stressors including warming and elevated levels of pollutants. These stressors affect not only habitat-forming organisms, such as corals, but they may also directly affect the organisms that inhabit these ecosystems. Here, we explore how the dual threat of habitat degradation and microplastic exposure may affect the behaviour and survival of coral reef fish in the field. Fish were caught prior to settlement and pulse-fed polystyrene microplastics six times over 4 days, then placed in the field on live or dead-degraded coral patches. Exposure to microplastics or dead coral led fish to be bolder, more active and stray further from shelter compared to control fish. Effect sizes indicated that plastic exposure had a greater effect on behaviour than degraded habitat, and we found no evidence of synergistic effects. This pattern was also displayed in their survival in the field. Our results highlight that attaining low concentrations of microplastic in the environment will be a useful management strategy, since minimizing microplastic intake by fishes may work concurrently with reef restoration strategies to enhance the resilience of coral reef populations.

Parasite infection directly impacts escape response and stress levels in fish.

Parasites can account for a substantial proportion of the biomass in marine communities. As such, parasites play a significant ecological role in ecosystem functioning via host interactions. Unlike macropredators, such as large piscivores, micropredators, such as parasites, rarely cause direct mortality. Rather, micropredators impose an energetic tax, thus significantly affecting host physiology and behaviour via sublethal effects. Recent research suggests that infection by gnathiid isopods (Crustacea) causes significant physiological stress and increased mortality rates. However, it is unclear whether infection causes changes in the behaviours that underpin escape responses or changes in routine activity levels. Moreover, it is poorly understood whether the cost of gnathiid infection manifests as an increase in cortisol. To investigate this, we examined the effect of experimental gnathiid infection on the swimming and escape performance of a newly settled coral reef fish and whether infection led to increased cortisol levels. We found that micropredation by a single gnathiid caused fast-start escape performance and swimming behaviour to significantly decrease and cortisol levels to double. Fast-start escape performance is an important predictor of recruit survival in the wild. As such, altered fitness-related traits and short-term stress, perhaps especially during early life stages, may result in large scale changes in the number of fish that successfully recruit to adult populations.

Effect of elevated CO2 and small boat noise on the kinematics of predator-prey interactions.

Oceans of the future are predicted to be more acidic and noisier, particularly along the productive coastal fringe. This study examined the independent and combined effects of short-term exposure to elevated CO2 and boat noise on the predator-prey interactions of a pair of common coral reef fishes (Pomacentrus wardi and its predator, Pseudochromis fuscus). Successful capture of prey by predators was the same regardless of whether the pairs had been exposed to ambient control conditions, the addition of either playback of boat noise, elevated CO2 (925 µatm) or both stressors simultaneously. The kinematics of the interaction were the same for all stressor combinations and differed from the controls. The effects of CO2 or boat noise were the same, suggesting that their effects were substitutive in this situation. Prey reduced their perception of threat under both stressors individually and when combined, and this coincided with reduced predator attack distances and attack speeds. The lack of an additive or multiplicative effect when both stressors co-occurred was notable given the different mechanisms involved in sensory disruptions and highlights the importance of determining the combined effects of key drivers to aid in predicting community dynamics under future environmental scenarios.

Ocean warming has a greater effect than acidification on the early life history development and swimming performance of a large circumglobal pelagic fish.

Ocean warming and acidification are serious threats to marine life; however, their individual and combined effects on large pelagic and predatory fishes are poorly understood. We determined the effects of projected future temperature and carbon dioxide (CO2 ) levels on survival, growth, morphological development and swimming performance on the early life stages of a large circumglobal pelagic fish, the yellowtail kingfish Seriola lalandi. Eggs, larvae and juveniles were reared in cross-factored treatments of temperature (21 and 25°C) and pCO2 (500 and 985 µatm) from fertilisation to 25 days post hatching (dph). Temperature had the greatest effect on survival, growth and development. Survivorship was lower, but growth and morphological development were faster at 25°C, with surviving fish larger and more developed at 1, 11 and 21 dph. Elevated pCO2 affected size at 1 dph, but not at 11 or 21 dph, and did not affect survival or morphological development. Elevated temperature and pCO2 had opposing effects on swimming performance at 21 dph. Critical swimming speed (Ucrit ) was increased by elevated temperature but reduced by elevated pCO2 . Additionally, elevated temperature increased the proportion of individuals that responded to a startle stimulus, reduced latency to respond and increased maximum escape speed, potentially due to the more advanced developmental stage of juveniles at 25°C. By contrast, elevated pCO2 reduced the distance moved and average speed in response to a startle stimulus. Our results show that higher temperature is likely to be the primary driver of global change impacts on kingfish early life history; however, elevated pCO2 could affect critical aspects of swimming performance in this pelagic species. Our findings will help parameterise and structure fisheries population dynamics models and improve projections of impacts to large pelagic fishes under climate change scenarios to better inform adaptation and mitigation responses.

Not equal in the face of habitat change: closely related fishes differ in their ability to use predation-related information in degraded coral.

Coral reefs are biodiversity hotpots that are under significant threat due to the degradation and death of hard corals. When obligate coral-dwelling species die, the remaining species must either move or adjust to the altered conditions. Our goal was to investigate the effect of coral degradation on the ability of coral reef fishes to assess their risk of predation using alarm cues from injured conspecifics. Here, we tested the ability of six closely related species of juvenile damselfish (Pomacentridae) to respond to risk cues in both live coral or dead-degraded coral environments. Of those six species, two are exclusively associated with live coral habitats, two are found mostly on dead-degraded coral rubble, while the last two are found in both habitat types. We found that the two live coral associates failed to respond appropriately to the cues in water from degraded habitats. In contrast, the cue response of the two rubble associates was unaffected in the same degraded habitat. Interestingly, we observed a mixed response from the species found in both habitat types, with one species displaying an appropriate cue response while the other did not. Our second experiment suggested that the lack of responses stemmed from deactivation of the alarm cues, rather than the inability of the species to smell. Habitat preference (live coral versus dead coral associates) and phylogeny are good candidates for future work aimed at predicting which species are affected by coral degradation. Our results point towards a surprising level of variation in the ability of congeneric species to fare in altered habitats and hence underscores the difficulty of predicting community change in degraded habitats.

Warming has a greater effect than elevated CO2 on predator-prey interactions in coral reef fish.

Ocean acidification and warming, driven by anthropogenic CO2 emissions, are considered to be among the greatest threats facing marine organisms. While each stressor in isolation has been studied extensively, there has been less focus on their combined effects, which could impact key ecological processes. We tested the independent and combined effects of short-term exposure to elevated CO2 and temperature on the predator-prey interactions of a common pair of coral reef fishes (Pomacentrus wardi and its predator, Pseudochromis fuscus). We found that predator success increased following independent exposure to high temperature and elevated CO2 Overall, high temperature had an overwhelming effect on the escape behaviour of the prey compared with the combined exposure to elevated CO2 and high temperature or the independent effect of elevated CO2 Exposure to high temperatures led to an increase in attack and predation rates. By contrast, we observed little influence of elevated CO2 on the behaviour of the predator, suggesting that the attack behaviour of P. fuscus was robust to this environmental change. This is the first study to address how the kinematics and swimming performance at the basis of predator-prey interactions may change in response to concurrent exposure to elevated CO2 and high temperatures and represents an important step to forecasting the responses of interacting species to climate change.

Habitat degradation disrupts neophobia in juvenile coral reef fish.

Habitat degradation not only disrupts habitat-forming species, but alters the sensory landscape within which most species must balance behavioural activities against predation risk. Rapidly developing a cautious behavioural phenotype, a condition known as neophobia, is advantageous when entering a novel risky habitat. Many aquatic organisms rely on damage-released conspecific cues (i.e. alarm cues) as an indicator of impending danger and use them to assess general risk and develop neophobia. This study tested whether settlement-stage damselfish associated with degraded coral reef habitats were able to use alarm cues as an indicator of risk and, in turn, develop a neophobic response at the end of their larval phase. Our results indicate that fish in live coral habitats that were exposed to alarm cues developed neophobia, and, in situ, were found to be more cautious, more closely associated with their coral shelters and survived four-times better than non-neophobic control fish. In contrast, fish that settled onto degraded coral habitats did not exhibit neophobia and consequently suffered much greater mortality on the reef, regardless of their history of exposure to alarm cues. Our results show that habitat degradation alters the efficacy of alarm cues with phenotypic and survival consequences for newly settled recruits.

At odds with the group: changes in lateralization and escape performance reveal conformity and conflict in fish schools.

Many vertebrates are known to show behavioural lateralization, whereby they differentially use one side of their body or either of their bilateral organs or limbs. Behavioural lateralization often manifests in a turning bias in fishes, with some individuals showing a left bias and others a right bias. Such biases could be the source of considerable conflict in fish schools given that there may be considerable social pressure to conform to the group to maintain effective group evasion. Here, we show that predation pressure is a major determinant of the degree of lateralization, both in a relative and absolute sense, in yellow-and-blueback fusiliers (Caesio teres), a schooling fish common on coral reefs. Wild-caught fish showed a bias for right turning. When predation pressure was experimentally elevated or relaxed, the strength of lateralization changed. Higher predation pressure resulted in an increase in the strength of lateralization. Individuals that exhibited the same turning bias as the majority of individuals in their group had improved escape performance compared with individuals that were at odds with the group. Moreover, individuals that were right-biased had improved escape performance, compared with left-biased ones. Plasticity in lateralization might be an important evolutionary consequence of the way gregarious species respond to predators owing to the probable costs associated with this behaviour.

Interactive effects of ocean acidification and rising sea temperatures alter predation rate and predator selectivity in reef fish communities.

Ocean warming and acidification are serious threats to marine life. While each stressor alone has been studied in detail, their combined effects on the outcome of ecological interactions are poorly understood. We measured predation rates and predator selectivity of two closely related species of damselfish exposed to a predatory dottyback. We found temperature and CO2 interacted synergistically on overall predation rate, but antagonistically on predator selectivity. Notably, elevated CO2 or temperature alone reversed predator selectivity, but the interaction between the two stressors cancelled selectivity. Routine metabolic rates of the two prey showed strong species differences in tolerance to CO2 and not temperature, but these differences did not correlate with recorded mortality. This highlights the difficulty of linking species-level physiological tolerance to resulting ecological outcomes. This study is the first to document both synergistic and antagonistic effects of elevated CO2 and temperature on a crucial ecological process like predator-prey dynamics.

Parental effects improve escape performance of juvenile reef fish in a high-CO2 world.

Rising CO2 levels in the oceans are predicted to have serious consequences for many marine taxa. Recent studies suggest that non-genetic parental effects may reduce the impact of high CO2 on the growth, survival and routine metabolic rate of marine fishes, but whether the parental environment mitigates behavioural and sensory impairment associated with high CO2 remains unknown. Here, we tested the acute effects of elevated CO2 on the escape responses of juvenile fish and whether such effects were altered by exposure of parents to increased CO2 (transgenerational acclimation). Elevated CO2 negatively affected the reactivity and locomotor performance of juvenile fish, but parental exposure to high CO2 reduced the effects in some traits, indicating the potential for acclimation of behavioural impairment across generations. However, acclimation was not complete in some traits, and absent in others, suggesting that transgenerational acclimation does not completely compensate the effects of high CO2 on escape responses.

Investigating the metabolic and oxidative stress induced by biofouled microplastics exposure in Seriola lalandi (yellowtail kingfish).

Microorganisms quickly colonise microplastics entering the ocean, forming a biofilm that, if ingested, is consumed with the microplastics. Past research often neglects to expose fish to biofouled microplastics, opting only for clean microplastics despite the low likelihood that fish will encounter clean microplastics. Here, we investigate the physiological impacts of biofouled polyethylene microplastic (300-335 µm) exposure in juvenile fish. Intermittent flow respirometry, antioxidant enzyme activity, and lipid peroxidation were investigated after fish were exposed to clean, biofouled, or no microplastic beads. Fish exposed to biofouled microplastics had a wider aerobic scope than those exposed to clean microplastics while antioxidant enzyme and lipid peroxidation levels were higher in clean microplastics. Clean microplastic exposure indicated higher fitness costs, potentially due to a nutritional advantage of the biofilm or varying bioavailability. These findings highlight the importance of replicating natural factors in exposure experiments when predicting the impacts of increasing pollutants in marine systems.

Habitat complexity and predator odours impact on the stress response and antipredation behaviour in coral reef fish.

Mass coral bleaching events coupled with local stressors have caused regional-scale loss of corals on reefs globally. Following the loss of corals, the structural complexity of these habitats is often reduced. By providing shelter, obscuring visual information, or physically impeding predators, habitat complexity can influence predation risk and the perception of risk by prey. Yet little is known on how habitat complexity and risk assessment interact to influence predator-prey interactions. To better understand how prey's perception of threats may shift in degraded ecosystems, we reared juvenile Pomacentrus chrysurus in environments of various habitat complexity levels and then exposed them to olfactory risk odours before simulating a predator strike. We found that the fast-start escape responses were enhanced when forewarned with olfactory cues of a predator and in environments of increasing complexity. However, no interaction between complexity and olfactory cues was observed in escape responses. To ascertain if the mechanisms used to modify these escape responses were facilitated through hormonal pathways, we conducted whole-body cortisol analysis. Cortisol concentrations interacted with habitat complexity and risk odours, such that P. chrysurus exhibited elevated cortisol levels when forewarned with predator odours, but only when complexity levels were low. Our study suggests that as complexity is lost, prey may more appropriately assess predation risk, likely as a result of receiving additional visual information. Prey's ability to modify their responses depending on the environmental context suggests that they may be able to partly alleviate the risk of increased predator-prey interactions as structural complexity is reduced.

Investigating the impacts of biofouled marine plastic debris on the olfactory behaviour of juvenile yellowtail kingfish (Seriola lalandi).

Marine microplastics are rapidly colonised by a microbial community which form a biofilm unique from the surrounding seawater that often contains infochemical-producing species associated with food sources. Here, we investigated whether juvenile kingfish (Seriola lalandi) were more attracted to biofouled plastics compared to clean plastics. Plastics were exposed to unfiltered seawater for one month to cultivate a microbial community. An olfactory behavioural experiment showed little difference in their response to the biofilm compared to clean plastic and control treatment. Further, ingestion experiments demonstrated that S. lalandi ingested fewer biofouled microplastics compared to clean microplastics. However, this was likely due to the bioavailability of the biofouled microplastics. This study highlights that while juvenile kingfish will ingest microplastics, they are not more attracted to those with a naturally acquired biofilm.

Increasing temperature and prey availability affect the growth and swimming kinematics of Atlantic herring (Clupea harengus) larvae.

Climate change will increase the magnitude and duration of warming events and the variability in the phenology and abundance of available prey to the early life stages of fish. These factors influence physiological, behavioral and ecological processes, impacting growth, development and survival. Using a fully factorial design with two prey-availability treatments (1200 prey items L-1 (high prey abundance) or 40 prey items L-1 (low prey abundance)) under three temperature regimes (8, 10 and 12°C), the swimming kinematics of 6-week old spring-spawning Atlantic herring larvae were examined using silhouette video photography. Higher temperatures combined with food limitation significantly decreased the growth and swimming kinematics of larval herring, with the most negative effect observed in larvae reared at 12°C and exposed to low food abundances. Specifically, larvae displayed reduced locomotory behaviors and reduced vertical movements. By contrast, larvae reared at high prey abundance and at 12°C displayed more active swimming and exploratory behavior, as evidenced by an increase in both locomotory behavior and vertical and horizontal turn angles, suggesting increased motivation to search for food. This research highlights the importance of determining to what degree fish larvae are sensitive to changes in temperature and how these changes might be further influenced by food availability.

Quantification and characterization of microplastics in commercial fish from southern New Zealand.

Plastics are ubiquitous throughout global marine ecosystems. To date, there has been limited research on the prevalence of microplastic ingestion by commercially important marine fish in the southern hemisphere, particularly in the South Pacific. Therefore, this research aimed to quantify ingested microplastics from ten commercially important fish species from southern New Zealand using microscopy and Raman spectroscopy. Overall, we found evidence of microplastic ingestion in 75 % of fish, with an average of 2.5 individual particles per fish. Microplastic fibers were the most commonly ingested. The most common colored microplastics ingested were blue, black and red, and 99.68 % of plastics identified were smaller than 5 mm. Raman spectroscopy of plastics recovered from nine fish species found polyethylene and polypropylene to be the most common plastic polymers ingested. Further research is necessary to ascertain the human ecological and health risks involved when exposed to microplastics through eating plastic contaminated fish.

Conceptualisation of multiple impacts interacting in the marine environment using marine infrastructure as an example.

The human population is increasingly reliant on the marine environment for food, trade, tourism, transport, communication and other vital ecosystem services. These services require extensive marine infrastructure, all of which have direct or indirect ecological impacts on marine environments. The rise in global marine infrastructure has led to light, noise and chemical pollution, as well as facilitation of biological invasions. As a result, marine systems and associated species are under increased pressure from habitat loss and degradation, formation of ecological traps and increased mortality, all of which can lead to reduced resilience and consequently increased invasive species establishment. Whereas the cumulative bearings of collective human impacts on marine populations have previously been demonstrated, the multiple impacts associated with marine infrastructure have not been well explored. Here, building on ecological literature, we explore the impacts that are associated with marine infrastructure, conceptualising the notion of correlative, interactive and cumulative effects of anthropogenic activities on the marine environment. By reviewing the range of mitigation approaches that are currently available, we consider the role that eco-engineering, marine spatial planning and agent-based modelling plays in complementing the design and placement of marine structures to incorporate the existing connectivity pathways, ecological principles and complexity of the environment. Because the effect of human-induced, rapid environmental change is predicted to increase in response to the growth of the human population, this study demonstrates that the development and implementation of legislative framework, innovative technologies and nature-informed solutions are vital, preventative measures to mitigate the multiple impacts associated with marine infrastructure.

Microplastic ingestion induces asymmetry and oxidative stress in larvae of the sea urchin Pseudechinus huttoni.

Determining the effects of microplastic (MP) ingestion by marine organisms, especially during the sensitive larval stages, is an important step in understanding wider ecosystem responses. We investigated the ingestion, retention (1-5 µm), and short-term exposure effects (1-4 µm) of spherical MPs by larvae of the sea urchin Pseudechinus huttoni. Larvae ingested MPs in a dose-dependent manner and successfully egested particles after a short retention period. Survival was not significantly affected by exposure to MPs over the 10-day experimental period, however, a teratogenic response in terms of delayed development resulted in an increase of larval arm asymmetry. Additionally, MP exposure resulted in oxidative damage to lipids and proteins in larval body tissue despite a significant upregulation of antioxidant defences. The findings indicate MP exposure may impair cellular function, leading to negative consequences for an organism's fitness and survival.

Species-specific molecular responses of wild coral reef fishes during a marine heatwave.

The marine heatwave of 2016 was one of the longest and hottest thermal anomalies recorded on the Great Barrier Reef, influencing multiple species of marine ectotherms, including coral reef fishes. There is a gap in our understanding of what the physiological consequences of heatwaves in wild fish populations are. Thus, in this study, we used liver transcriptomes to understand the molecular response of five species to the 2016 heatwave conditions. Gene expression was species specific, yet we detected overlap in functional responses associated with thermal stress previously reported in experimental setups. The molecular response was also influenced by the duration of exposure to elevated temperatures. This study highlights the importance of considering the effects of extreme warming events when evaluating the consequences of climate change on fish communities.