Friend or foe? Development of odour detection, differentiation and antipredator response in an embryonic elasmobranch

Young animals, especially those developing within eggs, are extremely vulnerable to predation risk given their immobility, small size and limited functionality of developing sensory systems. Embryos from a range of taxa can detect predator cues and use antipredator responses to reduce risk; however, little is known about this capacity in elasmobranchs, especially regarding olfactory detection. Embryonic Port Jackson sharks (Heterodontus portusjacksoni) were exposed to elasmobranch and teleost odours across key developmental stages to investigate their capacity to detect and discern between cues. Oxygen uptake rates were measured as a proxy for antipredator response and to estimate their energetic costs. Earlier developmental stages exhibited limited responses, regardless of the odour, likely associated with an undeveloped sensory system. However, older shark embryos depressed oxygen uptake rates (i.e. crypsis responses) when exposed to teleost cues, but showed little response to elasmobranch cues. In contrast, hatchlings exhibited minimal responses to teleost cues but a significant increase in oxygen uptake rates when exposed to elasmobranch odours, indicative of a general stress response in preparation for escape. Collectively, our data suggest that embryonic sharks can differentiate between odour cues and elicit various responses, but this ability is limited by their developing sensory capacity

Population variation in the thermal response to climate change reveals differing sensitivity in a benthic shark

Many species with broad distributions are exposed to different thermal regimes which often select for varied phenotypes. This intraspecific variation is often overlooked but may be critical in dictating the vulnerability of different populations to environmental change. We reared Port Jackson shark (Heterodontus portusjacksoni) eggs from two thermally discrete populations (i.e. Jervis Bay and Adelaide) under each location's present-day mean temperatures, predicted end-of-century temperatures and under reciprocal-cross conditions to establish intraspecific thermal sensitivity. Rearing temperatures strongly influenced ṀO2Max and critical thermal limits, regardless of population, indicative of acclimation processes. However, there were significant population-level effects, such that Jervis Bay sharks, regardless of rearing temperature, did not exhibit differences in ṀO2Rest, but under elevated temperatures exhibited reduced maximum swimming activity with step-wise increases in temperature. In contrast, Adelaide sharks reared under elevated temperatures doubled their ṀO2Rest, relative to their present-day temperature counterparts; however, maximum swimming activity was not influenced. With respect to reciprocal-cross comparisons, few differences were detected between Jervis Bay and Adelaide sharks reared under ambient Jervis Bay temperatures. Similarly, juveniles (from both populations) reared under Adelaide conditions had similar thermal limits and swimming activity (maximum volitional velocity and distance) to each other, indicative of conserved acclimation capacity. However, under Adelaide temperatures, the ṀO2Rest of Jervis Bay sharks was greater than that of Adelaide sharks. This indicates that the energetics of cooler water population (Adelaide) is likely more thermally sensitive than that of the warmer population (Jervis Bay). While unique to elasmobranchs, these data provide further support that by treating species as static, homogeneous populations, we ignore the impacts of thermal history and intraspecific variation on thermal sensitivity. With climate change, intraspecific variation will manifest as populations move, demographics change or extirpations occur, starting with the most sensitive populations

Aquatic Walking and Swimming Kinematics of Neonate and Juvenile Epaulette Sharks

The epaulette shark, Hemiscyllium ocellatum, is a small, reef-dwelling, benthic shark that-using its paired fins-can walk, both in and out of water. Within the reef flats, this species experiences short periods of elevated CO2 and hypoxia as well as fluctuating temperatures as reef flats become isolated with the outgoing tide. Past studies have shown that this species is robust (i.e., respiratory and metabolic performance, behavior) to climate change-relevant elevated CO2 levels as well as hypoxia and anoxia tolerant. However, epaulette shark embryos reared under ocean warming conditions hatch earlier and smaller, with altered patterns and coloration, and with higher metabolic costs than their current-day counterparts. Findings to date suggest that this species has adaptations to tolerate some, but perhaps not all, of the challenging conditions predicted for the 21st century. As such, the epaulette shark is emerging as a model system to understand vertebrate physiology in changing oceans. Yet, few studies have investigated the kinematics of walking and swimming, which may be vital to their biological fitness, considering their habitat and propensity for challenging environmental conditions. Given that neonates retain embryonic nutrition via an internalized yolk sac, resulting in a bulbous abdomen, while juveniles actively forage for worms, crustaceans, and small fishes, we hypothesized that difference in body shape over early ontogeny would affect locomotor performance. To test this, we examined neonate and juvenile locomotor kinematics during the three aquatic gaits they utilize-slow-to-medium walking, fast walking, and swimming-using 13 anatomical landmarks along the fins, girdles, and body midline. We found that differences in body shape did not alter kinematics between neonates and juveniles. Overall velocity, fin rotation, axial bending, and tail beat frequency and amplitude were consistent between early life stages. Data suggest that the locomotor kinematics are maintained between neonate and juvenile epaulette sharks, even as their feeding strategy changes. Studying epaulette shark locomotion allows us to understand this-and perhaps related-species' ability to move within and away from challenging conditions in their habitats. Such locomotor traits may not only be key to survival, in general, as a small, benthic mesopredator (i.e., movements required to maneuver into small reef crevices to avoid aerial and aquatic predators), but also be related to their sustained physiological performance under challenging environmental conditions, including those associated with climate change-a topic worthy of future investigation

Anthropogenic stressors influence reproduction and development in elasmobranch fishes

The consequences of human influence can arise in vertebrates as primary, secondary, or even tertiary stressors and may be especially detrimental for slow growing species with long generation times (i.e., K-selected species). Here, we review the impacts of both direct and indirect human interactions on the reproductive biology of elasmobranchs. Within direct human influence, capture-induced stress from fisheries bycatch and poor coastal management practices leading to habitat destruction and pollution are among the most impactful on elasmobranch reproduction. Capture-induced stress has been shown to negatively influence offspring and reproductive capacity via capture-induced parturition as well as by disrupting the reproductive physiology of adults. Habitat degradation impacts essential ecosystems that are necessary for the development of young elasmobranchs. Pollutants such as heavy metals, legacy pesticides, and flame retardants have been traced through elasmobranch reproduction; however, the long-term effects of these exogenous chemicals are yet to be determined. Furthermore, within indirect human impacts, climate change-mediated influences (e.g., ocean warming and acidification) can impact development, physiological processes, and behavioral patterns necessary for essential tasks such as foraging, growth, reproduction, and ultimately survival. Here, we also present a case study, where data regarding temperature and incubation time from 28 egg-laying elasmobranch species were examined to show relevance of such data in predicting how suitable (e.g., via maximum threshold temperatures) habitats will be for skate and shark development in the coming century. Concomitantly, this information highlights areas for future research that will help inform better management as well as climate change forecasting for this threatened group of aquatic vertebrates

Too hot to handle? Using movement to alleviate effects of elevated temperatures in a benthic elasmobranch, <i>Hemiscyllium ocellatum</i>

Tropical coral reef flats can be 3–4 °C warmer than surrounding deeper reef slopes, and some experience daily temperature fluctuations of up to 12 °C, which will be exacerbated as global temperatures continue to rise. Epaulette sharks (Hemiscyllium ocellatum), predominantly found on reef flats, may have evolved behavioural and/or physiological strategies to mitigate the effects of these dramatic temperature fluctuations. Here, juvenile sharks were acclimated, for at least 6 weeks, to average summer temperatures (28 °C) or predicted end-of-century summer temperatures (32 °C) to investigate the effects of elevated temperatures on growth, survival, and the use of movement to thermoregulate. In addition, sharks experience seasonal temperature changes; therefore, the upper critical thermal limits were determined for adult, wild sharks during both summer and winter months. We found that regardless of acclimation temperature, juveniles maintained the same food consumption rates (~ 5% body mass every other day), but for those living at 32 °C, this resulted in significantly decreased growth rates (body mass and total length). During winter months, maximum habitat temperatures (~ 24 °C) are far below adult sharks’ critical thermal limits (35.92 ± 0.21 °C). During summer months, maximum habitat temperatures (~ 35 °C) are closer to adult critical thermal limits (38.85 ± 0.31 °C). When estimating thermoregulatory behaviour of juvenile sharks maintained at 28 °C, those sharks examined in winter exhibited no thermoregulatory behaviour, while those examined in summer actively sought to control their thermal exposure, preferring 30.7 ± 1.04 °C (day) and 28.54 ± 0.75 °C (night). Furthermore, after acclimation to predicted end-of-century conditions, these same sharks behaviourally sought out 32.94 ± 0.46 °C (day) and 30.74 ± 0.68 °C (night); despite the cost of decreased growth and/or survival. Sharks maintained in control conditions had a mortality rate of 33% during the initial 90-day period of exposure, while mortality was 100% in those sharks exposed to elevated conditions. Ultimately, as ocean temperatures continue to rise, the distribution and abundance patterns for epaulette sharks and many other coral reef species are likely to change if trade-offs associated with acclimation outweigh the benefits of moving to more favourable habitats

The emergence emergency:a mudskipper's response to temperatures

Temperature has a profound effect on all life and a particularly influential effect on ectotherms, such as fishes. Amphibious fishes have a variety of strategies, both physiological and/or behavioural, to cope with a broad range of thermal conditions. This study examined the relationship between prolonged (5 weeks) exposure to a range of temperatures (22, 25, 28, or 32 degrees C) on oxygen uptake rate and movement behaviours (i.e., thermoregulation and emergence) in a common amphibious fish, the barred mudskipper (Periophthalmus argentilneatuis). At the highest temperature examined (32 degrees C, approximately 5 degrees C above their summer average temperatures), barred mudskippers exhibited 33.7-97.7% greater oxygen uptake rates at rest ((M) over dotO(2Rest)), emerged at a higher temperature (CTe; i.e., a modified critical thermal maxima (CTMax) methodology) of 41.3 +/- 0.3 degrees C relative to those maintained at 28, 25, or 22 degrees C. The 32 degrees C-maintained fish also ceased movement activity at the highest holding temperature suggesting that prolonged submergence at elevated temperatures is physiologically and energetically stressful to the individual. Using exhaustive exercise protocols with and without air exposure to simulate a predatory chase, the time to recovery was examined for all individuals. When submerged, mudskippers required 2.5x longer recovery time to return to resting oxygen uptake from exhaustive exercise than those fully emerged in air. Oxygen uptake data revealed that air exposure did not accrue oxygen debt, thereby allowing faster return to resting oxygen consumption rates. If the option to emerge was not available, mudskippers preferentially sought more benign water temperatures (26.7 +/- 2.1 degrees C), resembling those experienced by these fish during the Austral autumn, regardless of prolonged exposure higher or lower temperatures. These results add to our understanding of the strategies that amphibious fishes may use to mitigate extra costs associated with living in warm waters, and could be the key to understanding how such species will cope with increasing temperatures in the future

Regulate or tolerate: thermal strategy of a coral reef flat resident, the epaulette shark, Hemiscyllium ocellatum

Highly variable thermal environments, such as coral reef flats, are challenging for marine ectotherms and are thought to invoke the use of behavioural strategies to avoid extreme temperatures and seek out thermal environments close to their preferred temperatures. Common to coral reef flats, the epaulette shark (Hemiscyllium ocellatum) possesses physiological adaptations to hypoxic and hypercapnic conditions, such as those experienced on reef flats, but little is known regarding the thermal strategies used by these sharks. We investigated whether H. ocellatum uses behavioural thermoregulation (i.e., movement to occupy thermally favourable microhabitats) or tolerates the broad range of temperatures experienced on the reef flat. Using an automated shuttlebox system, we determined the preferred temperature of H. ocellatum under controlled laboratory conditions and then compared this preferred temperature to 6 months of in situ environmental and body temperatures of individual H. ocellatum across the Heron Island reef flat. The preferred temperature of H. ocellatum under controlled conditions was 20.7 +/- 1.5 degrees C, but the body temperatures of individual H. ocellatum on the Heron Island reef flat mirrored environmental temperatures regardless of season or month. Despite substantial temporal variation in temperature on the Heron Island reef flat (15-34 degrees C during 2017), there was a lack of spatial variation in temperature across the reef flat between sites or microhabitats. This limited spatial variation in temperature creates a low-quality thermal habitat limiting the ability of H. ocellatum to behaviourally thermoregulate. Behavioural thermoregulation is assumed in many shark species, but it appears that H. ocellatum may utilize other physiological strategies to cope with extreme temperature fluctuations on coral reef flats. While H. ocellatum appears to be able to tolerate acute exposure to temperatures well outside of their preferred temperature, it is unclear how this, and other, species will cope as temperatures continue to rise and approach their critical thermal limits. Understanding how species will respond to continued warming and the strategies they may use will be key to predicting future populations and assemblages