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Latitude and body size are generally considered key drivers of swimming performance for larval marine fishes, but evidence suggests that evolutionary relationships and habitat may also be important. We used a comparative phylogenetic framework, data synthesis and case study approach to investigate how swimming performance differs among larvae of fish species across latitude. First, we investigated how swimming performance changed with body length, and we found that temperate reef fishes have the greatest increases in swimming performance with length. Secondly, we compared differences in three swimming performance metrics (critical swimming speed, in situ swimming, and endurance) among post-flexion larvae, whilst considering phylogenetic relationships and morphology, and we found that reef fishes have higher swimming capacity than non-reef (pelagic and non-reef demersal) fishes, which is likely due to larger, more robust body sizes. Thirdly, we compared swimming performance of late-stage larvae of tropical fishes with oceanographic data to better understand the ecological relevance of their high-capacity swimming. We found that reef fishes have high swimming performance and grow larger than non-reef fish larvae, which we suggest is due to the pressures to find a specific, patchily distributed habitat upon which to settle. Given the current bias towards studies on percomorph fishes at low latitudes, we highlight that there is a need for more research on temperate reef fish larvae and other percomorph lineages from high latitudes. Overall, our findings provide valuable context to understand how swimming and morphological traits that are important for dispersal and recruitment processes are selected for among teleost fish larvae.

Coral reef ecosystems are currently under unprecedented stress due to anthropogenic induced climate change. Such stress causes coral habitats to degrade, which has been found to negatively impact the behaviour of some reef fishes. However, it is unknown whether the same chemical stresses from degraded habitats that impacts fish behaviour also impacts energy supporting swimming performance traits of fishes during the pelagic-to-reef life-history bottleneck. Here, we exposed newly settled juvenile Ambon damselfishes (Pomacentrus amboinensis) to either water that had passed over healthy or degraded coral for 24 h. Fishes were then swum at an ecologically relevant swimming speed for 200 min, and oxygen uptake rates were measured periodically. In general, fish swimming in water from degraded coral depressed oxygen uptake rates by 21%, which suggests that degraded habitats can have strong effects on fish physiology during this ecologically-critical time window.

Increasing ocean temperatures and the resulting poleward range shifts of species has highlighted the importance of a species preferred temperature and thermal range in shaping ecological communities. Understanding the temperatures preferred and avoided by individual species, and how these are influenced by species interactions is critical in predicting the future trajectories of populations, assemblages, and ecosystems. Using an automated shuttlebox system, we established the preferred temperature and upper and lower threshold temperatures (i.e., avoided temperatures) of a common coral reef fish, the black-axil chromis, Chromis atripectoralis. We then investigated how the presence of conspecifics, heterospecifics (Neopomacentrus bankieri), or a predator (Cephalopholis spiloparaea) influenced the selection of these temperatures. Control C. atripectoralis preferred 27.5 ± 1.0 °C, with individuals avoiding temperatures below 23.5 ± 0.9 °C and above 29.7 ± 0.7 °C. When associating with either conspecifics or heterospecifics, C. atripectoralis selected significantly lower temperatures (conspecifics: preferred = 21.2 ± 1.4 °C, lower threshold = 18.1 ± 0.8 °C; heterospecifics: preferred = 21.1 ± 1.1 °C, lower threshold = 19.2 ± 0.9 °C), but not higher temperatures (conspecifics: preferred = 28.9 ± 1.2 °C, upper threshold = 30.8 ± 0.9 °C; heterospecifics: preferred = 29.7 ± 1.1 °C, upper threshold = 31.4 ± 0.8 °C). The presence of the predator, however, had a significant effect on both lower and upper thresholds. Individual C. atripectoralis exposed themselves to temperatures ~ 5.5 °C cooler or warmer (lower threshold: 18.6 ± 0.5 °C, upper threshold: 35.2 ± 0.5 °C) than control fish before moving into the chamber containing the predator. These findings demonstrate how behavioural responses due to species interactions influence the thermal ecology of a tropical reef fish; however, there appears to be limited scope for individuals to tolerate higher temperatures unless faced with the risk of predation.

Tourism-related feeding of wildlife can result in detrimental, human-induced changes to the spatial distribution, social behaviour and health of target species. The feeding of sharks as part of shark-viewing activities has become increasingly popular in recent years to ensure reliable and consistent encounters. A common limitation in determining how feeding affects individuals or populations is the lack of baseline data prior to the establishment of a feeding site. Here, we documented the residency, spatial distribution, activity patterns and daily metabolic rates of juvenile lemon sharks, Negaprion brevirostris, prior to initiating daily feeding for 27 days to assess the effect of short-term feeding. We implanted acoustic transmitters equipped with accelerometers to record movement and activity in six lemon sharks. Sharks progressively anticipated the feeding events during the 27 days of daily feeding, as shown by a change in activity and increased time spent near the feeding site 1 h prior to feeding events. Shark behaviour did not fully return to baseline levels within the documented 90 days of postfeeding recovery. However, neither spatial distribution outside the refuge nor mean daily activity was affected by feeding. Sharks decreased their metabolic rates over the course of the study, but this was probably due to falling water temperature rather than the effect of feeding. Overall, our study shows that anticipatory behaviour in juvenile lemon sharks can occur within 11 days of daily feeding events, but behavioural changes seem confined to fine-scale movement patterns and may not affect these sharks’ daily energy needs. The ability to assess the effects of daily feeding at a site where tourism has not been occurring previously provides new information for operators and managers of wildlife tourism to account for and minimize potentially detrimental effects on the target species.

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.

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 ṀO2 Max 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 ṀO2 Rest , 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 ṀO2 Rest , 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 ṀO2 Rest 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.

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.

Aquatic anthropogenic noise is on the rise, with growing concern about its impact on species that are sensitive to low-frequency sounds (e.g. most fish and invertebrates). We investigated whether the reef fish Halichoeres bivittatus living in both noisy and quiet areas had differing levels of baseline stress (measured as whole-body cortisol) and whether they would exhibit a physiological stress response when exposed to boat noise playbacks. While the playback experiments significantly increased cortisol levels in fish from our experiment compared to baseline levels, there were minimal pairwise differences across treatments and no difference in baseline stress for fish living in noisy vs. quiet areas. These results may be explained by low overall auditory sensitivity, habituation to a fairly noisy environment (due to biological sounds), or that boat noise simply may not represent an immediate threat to survival in this species. These findings contrast recent studies that have shown elevated stress responses in fishes when exposed to boat noise and highlights that inter-specific differences must be considered when evaluating potential impacts of anthropogenic noise on marine life.

The larval phase of marine teleost fishes is characterized by important morphological and physiological modifications. Many of these modifications improve the larvae’s ability to swim, which satisfies a suite of crucial biological and ecological functions. Indeed, larval fish swimming performance has been considered a good proxy for overall condition, a predictor for growth and survival, and particularly helpful in assessing effects of natural and anthropogenic stress. Several methodologies have been developed to test larval fish swimming performance; however, measured swimming capabilities can strongly depend on the methodology utilised and developmental stage investigated. The aims of this review were, therefore, to link the ontogenetic development of swimming performance in early life stages of marine fishes, particularly the anatomical and physiological processes around the fins, muscles, and gills, with both the experimental methodologies used and the environmental stressors tested. We conducted a literature search and found 156 research papers relevant to swimming performance of marine teleost fish larvae. We found swimming performance to be highly variable among species and driven by temperature. In a meta-analysis focusing on the impacts of environmental stress on larval swimming performance, we found that prey reduction had the greatest impact on swimming. Methods used to evaluate swimming should keep the ontogenetic stage a focus, as forced swimming experiments are unfit for larvae prior to flexion of the notochord. Overall, while the data are deficient in some areas, we are able to highlight where the field of larval fish swimming could be directed and provide insight into which methods are best used under certain ecological scenarios, environmental stressors, and developmental stages.

The gill is one of the most important organs for growth and survival of fishes. Early life stages in coral reef fishes often exhibit extreme physiological and demographic characteristics that are linked to well-established respiratory and ionoregulatory processes. However, gill development and function in coral reef fishes is not well understood. Therefore, we investigated gill morphology, oxygen uptake and ionoregulatory systems throughout embryogenesis in two coral reef damselfishes, Acanthochromis polyacanthus and Amphiprion melanopus (Pomacentridae). In both species, we found key gill structures to develop rapidly early in the embryonic phase. Ionoregulatory cells appear on gill filaments 3–4 days post-fertilization and increase in density, whilst disappearing or shrinking in cutaneous locations. Primary respiratory tissue (lamellae) appears 5–7 days post-fertilization, coinciding with a peak in oxygen uptake rates of the developing embryos. Oxygen uptake was unaffected by phenylhydrazine across all ages (pre-hatching), indicating that haemoglobin is not yet required for oxygen uptake. This suggests that gills have limited contribution to respiratory functions during embryonic development, at least until hatching. Rapid gill development in damselfishes, when compared with that in most previously investigated fishes, may reflect preparations for a high-performance, challenging lifestyle on tropical reefs, but may also make reef fishes more vulnerable to anthropogenic stressors.

Despite the long evolutionary history of this group, the challenges brought by the Anthropocene have been inflicting an extensive pressure over sharks and their relatives. Overexploitation has been driving a worldwide decline in elasmobranch populations, and rapid environmental change, triggered by anthropogenic activities, may further test this group's resilience. In this context, we searched the literature for peer-reviewed studies featuring a sustained (>24 h) and controlled exposure of elasmobranch species to warming, acidification, and/or deoxygenation: three of the most pressing symptoms of change in the ocean. In a standardized comparative framework, we conducted an array of mixed-model meta-analyses (based on 368 control-treatment contrasts from 53 studies) to evaluate the effects of these factors and their combination as experimental treatments. We further compared these effects across different attributes (lineages, climates, lifestyles, reproductive modes, and life stages) and assessed the direction of impact over a comprehensive set of biological responses (survival, development, growth, aerobic metabolism, anaerobic metabolism, oxygen transport, feeding, behavior, acid-base status, thermal tolerance, hypoxia tolerance, and cell stress). Based on the present findings, warming appears as the most influential factor, with clear directional effects, namely decreasing development time and increasing aerobic metabolism, feeding, and thermal tolerance. While warming influence was pervasive across attributes, acidification effects appear to be more context-specific, with no perceivable directional trends across biological responses apart from the necessary to achieve acid-base balance. Meanwhile, despite its potential for steep impacts, deoxygenation has been the most neglected factor, with data paucity ultimately precluding sound conclusions. Likewise, the implementation of multi-factor treatments has been mostly restricted to the combination of warming and acidification, with effects approximately matching those of warming. Despite considerable progress over recent years, research regarding the impact of these drivers on elasmobranchs lags behind other taxa, with more research required to disentangle many of the observed effects. Given the current levels of extinction risk and the quick pace of global change, it is further crucial that we integrate the knowledge accumulated through different scientific approaches into a holistic perspective to better understand how this group may fare in a changing ocean.

Teleost fishes are diverse and successful, comprising almost half of all extant vertebrate species. It has been suggested that their success as a group is related, in part, to their unique O2 transport system, which includes pH-sensitive hemoglobin, a red blood cell β-adrenergic Na+/H+ exchanger (RBC β-NHE) that protects red blood cell pH, and plasma accessible carbonic anhydrase which is absent at the gills but present in some tissues, that short-circuits the β-NHE to enhance O2 unloading during periods of stress. However, direct support for this has only been examined in a few species of salmonids. Here, we expand the knowledge of this system to two warm-water, highly active marine percomorph fish, cobia (Rachycentron canadum) and mahi-mahi (Coryphaena hippurus). We show evidence for RBC β-NHE activity in both species, and characterize the Hb-O2 transport system in one of those species, cobia. We found significant RBC swelling following β-adrenergic stimulation in both species, providing evidence for the presence of a rapid, active RBC β-NHE in both cobia and mahi-mahi, with a time-course similar to that of salmonids. We generated oxygen equilibrium curves (OECs) for cobia blood and determined the P50, Hill, and Bohr coefficients, and used these data to model the potential for enhanced O2 unloading. We determined that there was potential for up to a 61% increase in O2 unloading associated with RBC β-NHE short-circuiting, assuming a - 0.2 ∆pHa-v in the blood. Thus, despite phylogenetic and life history differences between cobia and the salmonids, we found few differences between their Hb-O2 transport systems, suggesting conservation of this physiological trait across diverse teleost taxa.

In teleost fishes, catecholamine-induced increases in the activity of cation exchangers compensate for decreases in hemoglobin oxygen affinity and maximum blood oxygen carrying capacity caused by decreases in plasma pH (i.e., metabolic acidosis). The resultant red blood cell (RBC) swelling has been documented in sandbar (Carcharhinus plumbeus) and epaulette (Hemiscyllium ocellatum) sharks following capture by rod-and-reel or after a 1.5 h exposure to anoxia (respectively), although the underlying mechanisms remain unknown. To determine if RBC swelling could be documented in other elasmobranch fishes, we collected blood samples from clearnose skate (Rostroraja eglanteria), blacktip reef shark (Carcharhinus melanopterus), and sicklefin lemon shark (Negaprion acutidens) subjected to exhaustive exercise or air exposure (or both) and measured hematocrit, hemoglobin concentration, RBC count, RBC volume, and mean corpuscular hemoglobin content. We did likewise with sandbar and epaulette sharks to further explore the mechanisms driving swelling when present. We could not document RBC swelling in any species; although hematocrit increased in all species (presumably due to RBC ejection from the spleen or fluid shifts out of the vascular compartment) except epaulette shark. Our results indicate RBC swelling and associated ion shifts in elasmobranch fishes is not inducible by exercise or hypoxia, thus implying this response maybe of lesser importance for maintaining oxygen delivery during acute acidosis than in teleost fishes.

Temporal environmental variability causes behavioural and physiological responses in organisms that can affect their spatial location in time, and ultimately drive changes in population and community dynamics. Linking ecological changes with underlying environmental drivers is a complex task that can however be facilitated through the integration of physiology. Our overarching aim was to investigate the association between physiological performance and habitat utilisation patterns modulated by short temporal fluctuations in environmental factors. We used in situ monitoring data from a system experiencing extreme environmental fluctuations over a few hours and we selected four fish species with different habitat utilisation patterns across dissolved oxygen (DO) fluctuations: two commonly observed species (Siganus lineatus and Acanthopagrus pacificus), including at low DO (40 and 50% saturation, respectively), and two reef species (Heniochus acuminatus and Chaetodon vagabundus) never recorded below 70% saturation. We hypothesised that these patterns were associated to species' physiological performance in hypoxia. Therefore, we measured different metabolic variables (O2crit, incipient lethal oxygen (ILO), time to ILO, index of cumulative ambient oxygen deficit (O2deficit), maximum oxygen supply capacity (α)) using respirometry. Physiological performance differed among species and was intrinsically associated to habitat use patterns. S. lineatus had a lower O2crit than H. acuminatus, A. pacificus and C. vagabundus (13, 18.7, 20 and 20.2% saturation respectively). Additionally, S. lineatus and A. pacificus displayed better capacity for survival below O2crit than C. vagabundus and H. acuminatus (lower ILO, higher O2deficit and longer time to ILO) and higher α. Field monitoring data revealed that DO temporarily falls below species’ O2crit and even ILO on most days, suggesting that short temporal variability in DO likely forces species to temporarily avoid harmful conditions, driving important changes in ecosystem structure over a few hours. Our results support the hypothesis that organismal physiology can provide insights into ecological changes occurring over a few hours as a result of environmental variability. Consequently, integrating physiology with ecological data at relevant temporal scales may help predict temporal shifts in ecosystems structure and functions to account for ecological patterns often overlooked and difficult to identify.

Elasmobranch populations face worldwide declines owing to anthropogenic stressors, with lethal and sub-lethal consequences. Oxygen uptake rates ( $$ \dot{M} $$ O2, typically measured in mg O2 kg−1 h−1) can be quantified as proxies of whole-organism aerobic metabolic rates and are relevant to fisheries management and conservation through aerobic performance’s relationship with fitness and spatial ecology. The purpose of this review was to better understand how $$ \dot{M} $$ O2 has been and can be applied to predict how elasmobranch populations will respond to current and future anthropogenic stressors. We identified 10 studies spanning 9 elasmobranch species that quantified $$ \dot{M} $$ O2 to understand elasmobranch populations’ responses to exposure to anthropogenic stressors. Studies measuring responses to climate change stressors (ocean warming and acidification, declining oxygen content, increasing storm frequency) were most common. Studies with relevance to fisheries stressors used $$ \dot{M} $$ O2 to approximate energetic costs of capture and estimate recovery times in bycatch scenarios. Ecotourism encounters were investigated in the context of increases in energetic requirements owing to anthropogenic disruption of diel activity cycles. Furthermore, we discuss how an understanding of $$ \dot{M} $$ O2 in elasmobranchs has been and can be applied to predict populations’ responses to anthropogenic stressors with deliverables for improving species management and conservation. Specifically, $$ \dot{M} $$ O2 can be applied to predict population-level responses to stressors by quantifying associations between $$ \dot{M} $$ O2 and fitness-related processes, spatial ecology, and impact on ecosystem function (via bioenergetics modelling). This review is meant to serve as a call-to-action to further bridge the gap between experimental biology and elasmobranch conservation in the “good Anthropocene”.

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.

Climate change is affecting thermal regimes globally, and organisms relying on their environment to regulate biological processes face unknown consequences. In ectotherms, temperature affects development rates, body condition, and performance. Embryonic stages may be the most vulnerable life history stages, especially for oviparous species already living at the warm edge of their distribution, as embryos cannot relocate during this developmental window. We reared 27 epaulette shark (Hemiscyllium ocellatum) embryos under average summer conditions (27 °C) or temperatures predicted for the middle and end of the twenty-first century with climate change (i.e., 29 and 31 °C) and tracked growth, development, and metabolic costs both in ovo and upon hatch. Rearing sharks at 31 °C impacted embryonic growth, yolk consumption, and metabolic rates. Upon hatch, 31 °C-reared sharks weighed significantly less than their 27 °C-reared counterparts and exhibited reduced metabolic performance. Many important growth and development traits in this species may peak after 27 °C and start to become negatively impacted nearing 31 °C. We hypothesize that 31 °C approximates the pejus temperature (i.e., temperatures at which performance of a trait begin to decline) for this species, which is alarming, given that this temperature range is well within ocean warming scenarios predicted for this species’ distribution over the next century.

The COVID-19 pandemic and associated public health measures have had unanticipated effects on ecosystems and biodiversity. Conservation physiology and its mechanistic underpinnings are well positioned to generate robust data to inform the extent to which the Anthropause has benefited biodiversity through alterations in disturbance-, pollution- and climate change-related emissions. The conservation physiology toolbox includes sensitive biomarkers and tools that can be used both retroactively (e.g. to reconstruct stress in wildlife before, during and after lockdown measures) and proactively (e.g. future viral waves) to understand the physiological consequences of the pandemic. The pandemic has also created new risks to ecosystems and biodiversity through extensive use of various antimicrobial products (e.g. hand cleansers, sprays) and plastic medical waste. Conservation physiology can be used to identify regulatory thresholds for those products. Moreover, given that COVID-19 is zoonotic, there is also opportunity for conservation physiologists to work closely with experts in conservation medicine and human health on strategies that will reduce the likelihood of future pandemics (e.g. what conditions enable disease development and pathogen transfer) while embracing the One Health concept. The conservation physiology community has also been impacted directly by COVID-19 with interruptions in research, training and networking (e.g. conferences). Because this is a nascent discipline, it will be particularly important to support early career researchers and ensure that there are recruitment pathways for the next generation of conservation physiologists while creating a diverse and inclusive community. We remain hopeful for the future and in particular the ability of the conservation physiology community to deliver relevant, solutions-oriented science to guide decision makers particularly during the important post-COVID transition and economic recovery.

In 1992, the Union of Concerned Scientists shared their 'World Scientists'Warning to Humanity' with governmental leaders worldwide, calling for immediate action to halt the environmental degradation that threatens the systems that support life on Earth. A follow-up 'Second Warning' was released in 2017, with over 15 000 scientists as signatories, describing the lack of progress in adopting the sustainable practices necessary to safeguard the biosphere. In their 'SecondWarning', Ripple and colleagues provided 13 'diverse and effective steps humanity can take to transition to sustainability.' Here, we discuss how the field of conservation physiology can contribute to six of these goals: (i) prioritizing connected, well-managed reserves; (ii) halting the conversion of native habitats to maintain ecosystemservices; (iii) restoring native plant communities; (iv) rewilding regions with native species; (v) developing policy instruments; and (vi) increasing outdoor education, societal engagement and reverence for nature. Throughout, we focus our recommendations on specific aspects of physiological function while acknowledging that the exact traits that will be useful in each context are oftenstill being determined and refined. However, for each goal, we include a short case study to illustrate a specific physiological trait or group of traits that is already being utilized in that context. We conclude with suggestions for how conservation physiologists can broaden the impact of their science aimed at accomplishing the goals of the 'Second Warning'. Overall, we provide an overview of how conservation physiology can contribute to addressing the grand socio-environmental challenges of our time. National Science Foundation MacroSystems Biology program [DEB-DEB-1340856]; National Science FoundationNational Science Foundation (NSF) [IOS-1755055, 1951244, 2017949]; FutureMARES (Climate Change and Future Marine Ecosystem Services and Biodiversity, EU H2020) [869300] Published version K.R.H. was supported by the National Science Foundation MacroSystems Biology program (DEB-DEB-1340856). W.A.H. was supported by the National Science Foundation (grant #IOS-1755055). M.A.P. received partial support from FutureMARES (Climate Change and Future Marine Ecosystem Services and Biodiversity, EU H2020, award no. 869300). L.S. is funded by the National Science Foundation (grants 1951244 and 2017949).

As climate-driven heat waves become more frequent and intense, there is increasing urgency to understand how thermally sensitive species are responding. Acute heating events lasting days to months may elicit acclimation responses to improve performance and survival. However, the coordination of acclimation responses remains largely unknown for most stenothermal species. We documented the chronology of 18 metabolic and cardiorespiratory changes that occur in the gills, blood, spleen, and muscles when tropical coral reef fishes are thermally stressed (+3.0°C above ambient). Using representative coral reef fishes (Caesio cuning and Cheilodipterus quinquelineatus) separated by >100 million years of evolution and with stark differences in major life-history characteristics (i.e. lifespan, habitat use, mobility, etc.), we show that exposure duration illicited coordinated responses in 13 tissue and organ systems over 5 weeks. The onset and duration of biomarker responses differed between species, with C. cuning – an active, mobile species – initiating acclimation responses to unavoidable thermal stress within the first week of heat exposure; conversely, C. quinquelineatus – a sessile, territorial species – exhibited comparatively reduced acclimation responses that were delayed through time. Seven biomarkers, including red muscle citrate synthase and lactate dehydrogenase activities, blood glucose and hemoglobin concentrations, spleen somatic index, and gill lamellar perimeter and width, proved critical in evaluating acclimation progression and completion, as these provided consistent evaluation of thermal responses across species.

Lay Summary In tropical nearshore habitats, thermal stressors may exacerbate existing stressors in sharks. Here, we investigated the mobilization of plasma corticosteroids and metabolites in response to a heatwave stress and air exposure in the blacktip reef shark, Carcharhinus melanopterus. Thermal stress alters corticosteroid and metabolite mobilization; although, these measurements are not correlated., The increasing frequency and duration of marine heatwaves attributed to climate change threatens coastal elasmobranchs and may exacerbate existing anthropogenic stressors. While the elasmobranch stress response has been well studied, the role of the unique corticosteroid—1α-hydroxycorticosterone (1α-OHB)—in energy balance is not understood. Therefore, 1α-OHB’s utility as a stress biomarker in elasmobranch conservation physiology is equivocal. Here, we analyse the roles of corticosteroids, 1α-OHB and corticosterone, and metabolites, glucose and 3-hydroxybutyrate (3-HB), in response to stress in a protected tropical shark species, the blacktip reef shark (Carcharhinus melanopterus). Wild-caught neonates were exposed to ambient (27°C) or heatwave conditions (29°C) and subsequently a simulated fishing stressor (1 min air exposure). Blood samples were taken prior to temperature exposure, prior to air exposure, and 30 min, 1 h, 24 h, and 48 h post-air exposure at treatment temperatures. Plasma 1α-OHB was elevated for 48 h in 27°C-exposed sharks but declined over time in 29°C-exposed sharks. Plasma 1α-OHB was not correlated with either metabolite. Plasma glucose was higher and plasma 3-HB was lower in 29°C-exposed sharks. In a separate experiment, blood samples were collected from both neonate and adult sharks immediately following capture and again 5 min later, and analysed for corticosteroids and metabolites. Plasma 1α-OHB increased in neonates within 5 min, but neonates displayed lower plasma 1α-OHB and higher glucose concentrations than adults. We conclude that 1α-OHB does not serve as a classic glucocorticoid role in C. melanopterus under these stressors. Furthermore, we show for the first time, ontogenetic differences in plasma 1α-OHB. Ultimately, our findings provide insights into hormonal control of energy mobilization during stress in C. melanopterus, particularly during simulated heatwave conditions, which seem to alter both endocrine and energy mobilization. Further work is needed to determine the utility of 1α-OHB as a biomarker for the mobilization of energy during a stress event in elasmobranchs.

Temperature and oxygen limit the distribution of marine ectotherms. Haematological traits underlying blood-oxygen carrying capacity are thought to be correlated with thermal tolerance in certain fishes, and this relationship is hypothesised to be explained by oxygen supply capacity. We tested this hypothesis using reef shark neonates as experimental models because they live near their upper thermal limits and are physiologically sensitive to low oxygen conditions. We first described in situ associations between temperature and oxygen at the study site (Moorea, French Polynesia) and found that the habitats for reef shark neonates (Carcharhinus melanopterus and Negaprion acutidens) were hyperoxic at the maximum recorded temperatures. Next, we tested for in situ associations between thermal habitat characteristics and haematological traits of neonates. Contrary to predictions, we only demonstrated a negative association between haemoglobin concentration and maximum habitat temperatures in C. melanopterus. Next, we tested for ex situ associations between critical thermal maximum (CTMax) and haematological traits, but only demonstrated a negative association between haematocrit and CTMax in C. melanopterus. Finally, we measured critical oxygen tension (pcrit) ex situ and estimated its temperature sensitivity to predict oxygen-dependent values of CTMax. Estimated temperature sensitivity of pcrit was similar to reported values for sharks and skates, and predicted values for CTMax equalled maximum habitat temperatures. These data demonstrate unique associations between haematological traits and thermal tolerance in a reef shark that are likely not explained by oxygen supply capacity. However, a relationship between oxygen supply capacity and thermal tolerance remains to be demonstrated empirically.

Ocean warming and acidification act concurrently on marine ectotherms with the potential for detrimental, synergistic effects; yet, effects of these stressors remain understudied in large predatory fishes, including sharks. We tested for behavioural and physiological responses of blacktip reef shark (Carcharhinus melanopterus) neonates to climate change relevant changes in temperature (28 and 31 °C) and carbon dioxide partial pressures (pCO2; 650 and 1050 µatm) using a fully factorial design. Behavioural assays (lateralisation, activity level) were conducted upon 7–13 days of acclimation, and physiological assays (hypoxia tolerance, oxygen uptake rates, acid–base and haematological status) were conducted upon 14–17 days of acclimation. Haematocrit was higher in sharks acclimated to 31 °C than to 28 °C. Significant treatment effects were also detected for blood lactate and minimum oxygen uptake rate; although, these observations were not supported by adequate statistical power. Inter-individual variability was considerable for all measured traits, except for haematocrit. Moving forward, studies on similarly ‘hard-to-study’ species may account for large inter-individual variability by increasing replication, testing larger, yet ecologically relevant, differences in temperature and pCO2, and reducing measurement error. Robust experimental studies on elasmobranchs are critical to meaningfully assess the threat of global change stressors in these data-deficient species.

Sharks play important functional roles in coral reef ecosystems. Studying reef shark populations' spatial ecology also contributes important data for effective conservation planning. The purpose of this study was to define the home range of neonatal blacktip reef sharks (Carcharhinus melanopterus) around Moorea, French Polynesia, and compare estimates using both mark-recapture surveys and active acoustic telemetry. Mark-recapture surveys produced a minimum convex polygon (MCP) of 0.07 km(2) that was significantly larger than the MCP derived from acoustic telemetry (0.02 km(2)). Acoustic telemetry produced 50 and 95% kernel utilization densities that were smaller (0.02 km(2)) and larger (0.14 km(2)) than home range estimates from mark-recapture surveys, respectively. Home range estimates from this study are the smallest that have been documented for neonatal blacktip reef sharks, possibly owing to the study sites' proximity to deep channels. Mark-recapture and active acoustic telemetry are complementary approaches worthy of consideration where passive telemetry is impractical.

Chromis atripectoralis tolerated lower, but not higher, temperatures when associated with complex habitat structure compared to those under control conditions, which had no access to habitat structure. Understanding how habitat complexity influences thermal selection is critical given the rate of ocean warming and poleward expansions of tropical fishes., Coral reef species, like most tropical species, are sensitive to increasing environmental temperatures, with many species already living close to their thermal maxima. Ocean warming and the increasing frequency and intensity of marine heatwaves are challenging the persistence of reef-associated species through both direct physiological effects of elevated water temperatures and the degradation and loss of habitat structure following disturbance. Understanding the relative importance of habitat degradation and ocean warming in shaping species distributions is critical in predicting the likely biological effects of global warming. Using an automated shuttle box system, we investigated how habitat complexity influences the selection of thermal environments for a common coral reef damselfish, Chromis atripectoralis. In the absence of any habitat (i.e. control), C. atripectoralis avoided temperatures below 22.9 ± 0.8°C and above 31.9 ± 0.6°C, with a preferred temperature (Tpref) of 28.1 ± 0.9°C. When complex habitat was available, individual C. atripectoralis occupied temperatures down to 4.3°C lower (mean ± SE; threshold: 18.6 ± 0.7°C; Tpref: 18.9 ± 1.0°C) than control fish. Conversely, C. atripectoralis in complex habitats occupied similar upper temperatures as control fish (threshold: 31.7 ± 0.4°C; preference: 28.3 ± 0.7°C). Our results show that the availability of complex habitat can influence the selection of thermal environment by a coral reef fish, but only at temperatures below their thermal preference. The limited scope of C. atripectoralis to occupy warmer environments, even when associated with complex habitat, suggests that habitat restoration efforts in areas that continue to warm may not be effective in retaining populations of C. atripectoralis and similar species. This species may have to move to cooler (e.g. deeper or higher latitude) habitats under predicted future warming. The integration of habitat quality and thermal environment into conservation efforts will be essential to conserve of coral reef fish populations under future ocean warming scenarios.

Thermal dependence of growth and metabolism can influence thermal preference and tolerance in marine ectotherms, including threatened and data-deficient species. Here, we quantified the thermal dependence of physiological performance in neonates of a tropical shark species (blacktip reef shark, Carcharhinus melanopterus) from shallow, nearshore habitats. We measured minimum and maximum oxygen uptake rates (ṀO2), calculated aerobic scope, excess post-exercise oxygen consumption and recovery from exercise, and measured critical thermal maxima (CTmax), thermal safety margins, hypoxia tolerance, specific growth rates, body condition and food conversion efficiencies at two ecologically relevant acclimation temperatures (28 and 31°C). Owing to high post-exercise mortality, a third acclimation temperature (33°C) was not investigated further. Acclimation temperature did not affect ṀO2 or growth, but CTmax and hypoxia tolerance were greatest at 31°C and positively associated. We also quantified in vitro temperature (25, 30 and 35°C) and pH effects on haemoglobin–oxygen (Hb–O2) affinity of wild-caught, non-acclimated sharks. As expected, Hb–O2 affinity decreased with increasing temperatures, but pH effects observed at 30°C were absent at 25 and 35°C. Finally, we logged body temperatures of free-ranging sharks and determined that C. melanopterus neonates avoided 31°C in situ. We conclude that C. melanopterus neonates demonstrate minimal thermal dependence of whole-organism physiological performance across a seasonal temperature range and may use behaviour to avoid unfavourable environmental temperatures. The association between thermal tolerance and hypoxia tolerance suggests a common mechanism warranting further investigation. Future research should explore the consequences of ocean warming, especially in nearshore, tropical species.

Molecular responses of fishes to a heatwave are species specific and do not concur with measures of oxygen uptake in captivity., 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.

Marine ectotherms are often sensitive to thermal stress, and certain life stages can be particularly vulnerable (e.g., larvae or spawners). In this study, we investigated the critical thermal maxima (CTmax) of larval and early juvenile life stages of three tropical marine fishes (Acanthochromis polyacanthus, Amphiprion melanopus, and Lates calcarifer). We tested for potential effects of developmental acclimation, life stage, and experimental heating rates, and we measured metabolic enzyme activities from aerobic (citrate synthase, CS) and anaerobic pathways (lactate dehydrogenase, LDH). A slightly elevated rearing temperature neither influenced CTmax nor CS activity, which otherwise could have indicated thermal acclimation. However, we found CTmax to either remain stable (Acanthrochromis polyacanthus) or increase with body mass during early ontogeny (Amphiprion melanopus and Lates calcarifer). In all three species, faster heating rates lead to higher CTmax. Acute temperature stress did not change CS or LDH activities, suggesting that overall aerobic and anaerobic metabolism remained stable. Lates calcarifer, a catadromous species that migrates from oceanic to riverine habitats upon metamorphosis, had higher CTmax than the two coral reef fish species. We highlight that, for obtaining conservative estimates of a fish species’ upper thermal limits, several developmental stages and body mass ranges should be examined. Moreover, upper thermal limits should be assessed using standardized heating rates. This will not only benefit comparative approaches but also aid in assessing geographic (re-) distributions and climate change sensitivity of marine fishes.

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 rarely cause direct mortality. Rather, micropredators impose an energetic tax, thus significantly affecting host physiology and behaviour via such 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 would lead 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.

Anthropogenic ocean acidification (OA) is a threat to coral reef fishes, but few studies have investigated responses of high-trophic-level predators, including sharks. We tested the effects of 72-hr exposure to OA-relevant elevated partial pressures of carbon dioxide (pCO(2)) on oxygen uptake rates, acid-base status, and haematology of newborn tropical blacktip reef sharks (Carcharhinus melanopterus). Acute exposure to end-of-centurypCO(2)levels resulted in elevated haematocrit (i.e. stress or compensation of oxygen uptake rates) and blood lactate concentrations (i.e. prolonged recovery) in the newborns. Conversely, whole blood and mean corpuscular haemoglobin concentrations, blood pH, estimates of standard and maximum metabolic rates, and aerobic scope remained unaffected. Taken together, newborn blacktip reef sharks appear physiologically robust to end-of-centurypCO(2)levels, but less so than other, previously investigated, tropical carpet sharks. Our results suggest peak fluctuatingpCO(2)levels in coral reef lagoons could still physiologically affect newborn reef sharks, but studies assessing the effects of long-term exposure and in combination with other anthropogenic stressors are needed.

Lay summary Elasmobranch blood haematological parameters remained stable over 3 hours of storage duration, indicating that they do not need to be measured immediately. The HemoCue haemoglobin analyser can be used to measure haemoglobin concentrations from elasmobranch blood samples with the use of a correction equation., Blood samples collected from wild-caught fishes can provide important information regarding the effects of capture (and thus post-release survival) as well as other stressors. Unfortunately, blood samples often cannot be analysed immediately upon sampling, and blood parameters (e.g. blood oxygen levels and acid–base parameters) are known to change with storage duration due to the metabolic activity of the red blood cells. We obtained blood samples from both untreated and stressed individuals of both blacktip reef shark (Carcharhinus melanopterus) and sicklefin lemon shark (Negaprion acutidens) to determine the effects of storage duration on blood pH, haematocrit and haemoglobin concentration ([Hb]). We found no significant effects after storage on ice for up to 180 minutes. Moreover, to validate the usability of a HemoCue haemoglobin analyser (a point-of-care device), we compared data from this device to [Hb] determined using the cyanomethaemoglobin method with blood samples from 10 individuals from each of the aforementioned species as well as epaulette shark (Hemiscyllium ocellatum). Values from the HemoCue consistently overestimated [Hb], and we therefore developed the necessary correction equations. The correction equations were not statistically different among the three elasmobranch species within the biologically relevant range but did differ from published corrections developed using blood from temperate teleost fishes. Although the HemoCue is useful in field situations, development of species-specific calibration equations may be necessary to ensure the reliability of inter-species comparisons of blood [Hb]. Together, these data should increase confidence in haematological stress indicators in elasmobranch fishes, measurements of which are critical for understanding the impact of anthropogenic stressors on these ecologically important species.

The impacts of ocean acidification will depend on the ability of marine organisms to tolerate, acclimate and eventually adapt to changes in ocean chemistry. Here, we use a unique transgenerational experiment to determine the molecular response of a coral reef fish to short-term, developmental and transgenerational exposure to elevated CO2, and to test how these responses are influenced by variations in tolerance to elevated CO2 exhibited by the parents. Within-generation responses in gene expression to end-of-century predicted CO2 levels indicate that a self-amplifying cycle in GABAergic neurotransmission is triggered, explaining previously reported neurological and behavioural impairments. Furthermore, epigenetic regulator genes exhibited a within-generation specific response, but with some divergence due to parental phenotype. Importantly, we find that altered gene expression for the majority of within-generation responses returns to baseline levels following parental exposure to elevated CO2 conditions. Our results show that both parental variation in tolerance and cross-generation exposure to elevated CO2 are crucial factors in determining the response of reef fish to changing ocean chemistry.

Acquiring and storing energy is vital to sharks of all age-classes. Viviparous shark embryos receive endogenous maternal energy reserves to sustain the first weeks after birth. Then, in order to maintain body condition, sharks must start foraging. Our goal was to understand whether maternal energy investments vary between blacktip reef sharks (Carcharhinus melanopterus) from two populations and to what extent body condition and the initiation of foraging might be affected by presumably variable maternal investments. A total of 546 young sharks were captured at St. Joseph atoll (Seychelles) and Moorea (French Polynesia) between 2014 and 2018, and indices of body condition and percentage of stomachs containing prey were measured. Maternal investment was found to be site-specific, with significantly larger, heavier, and better conditioned individuals in Moorea. Despite these advantages, as time progressed, Moorea sharks exhibited significant decreases in body condition and were slower to initiate foraging. We suggest that the young sharks’ foraging success is independent of the quality of maternal energy resources, and that other factors, such as prey availability, prey quality, and/or anthropogenic stressors are likely responsible for the observed differences across sites. Insights into intraspecific variations in early life-stages may further support site-specific management strategies for young sharks from nearshore habitats.

Many studies have examined the average effects of ocean acidification and warming on phenotypic traits of reef fishes, finding variable, but often negative effects on behavioural and physiological performance. Yet the presence and nature of a relationship between these traits is unknown. A negative relationship between phenotypic traits could limit individual performance and even the capacity of populations to adapt to climate change. Here, we examined the relationship between behavioural and physiological performance of a juvenile reef fish under elevated CO2 and temperature in a full factorial design. Behaviourally, the response to an alarm odour was negatively affected by elevated CO2, but not elevated temperature. Physiologically, aerobic scope was significantly diminished under elevated temperature, but not under elevated CO2. At the individual level, there was no relationship between behavioural and physiological traits in the control and single-stressor treatments. However, a statistically significant negative relationship was detected between the traits in the combined elevated CO2 and temperature treatment. Our results demonstrate that trade-offs in performance between behavioural and physiological traits may only be evident when multiple climate change stressors are considered, and suggest that this negative relationship could limit adaptive potential to climate change.

Ocean acidification (OA) is predicted to affect the physiology of some fishes. To date, most studies have investigated this issue using stable pCO2 levels based on open ocean projections. Yet, most shallow, nearshore systems experience temporal and spatial pCO2 fluctuations. For example, pCO2 on coral reefs is highest at night and lowest during the day, but as OA progresses, both the average pCO2 and magnitude of fluctuations are expected to increase. We exposed four coral reef fishes - Lutjanus fulviflamma, Caesio cuning, Abudefduf whitleyi, and Cheilodipterus quinquelineatus - to ambient, stable elevated, or fluctuating elevated pCO2 conditions for 9-11 days. Then, we measured swimming performance, oxygen uptake rates, and haematological parameters during the day and at night. When compared to ambient pCO2 conditions, L. fulviflamma, C. cuning, and A. whitleyi exposed to fluctuating elevated pCO2 increased swimming performance, maximum oxygen uptake rates, and aerobic scope, regardless of time of day; whereas, the only nocturnal species studied, C. quinquelineatus, decreased maximum oxygen uptake rates and aerobic scope. Our findings suggest that exposure to fluctuating or stable elevated pCO2 can physiologically benefit some coral reef fishes; however, other species, such as the cardinalfish examined here, may be more sensitive to future OA conditions.

Ocean acidification, resulting from increasing atmospheric carbon dioxide (CO2) emissions, can affect the physiological performance of some fishes. Most studies investigating ocean acidification have used stable pCO(2) treatments based on open ocean predictions. However, nearshore systems can experience substantial spatial and temporal variations in pCO(2). Notably, coral reefs are known to experience diel fluctuations in pCO(2), which are expected to increase on average and in magnitude in the future. Though we know these variations exist, relatively few studies have included fluctuating treatments when examining the effects of ocean acidification conditions on coral reef species. To address this, we exposed two species of damselfishes, Amblyglyphidodon curacao and Acanthochromis polyacanthus, to ambient pCO(2), a stable elevated pCO(2) treatment, and two fluctuating pCO(2) treatments (increasing and decreasing) over an 8 h period. Oxygen uptake rates were measured both while fish were swimming and resting at low-speed. These 8 h periods were followed by an exhaustive swimming test (Ucrit) and blood draw examining swimming metrics and haematological parameters contributing to oxygen transport. When A. polyacanthus were exposed to stable pCO(2) conditions (ambient or elevated), they required more energy during the 8 h trial regardless of swimming type than fish exposed to either of the fluctuating pCO(2) treatments (increasing or decreasing). These results were reflected in the oxygen uptake rates during the Ucrit tests, where fish exposed to fluctuating pCO(2) treatments had a higher factorial aerobic scope than fish exposed to stable pCO(2) treatments. By contrast, A. curacao showed no effect of pCO(2) treatment on swimming or oxygen uptake metrics. Our results show that responses to stable versus fluctuating pCO(2) differ between species what is stressful for one species many not be stressful for another. Such asymmetries may have populationand community level impacts under higher more variable pCO(2) conditions in the future.

Predicting the impacts of ocean warming and acidification on marine ecosystems requires an evolutionary perspective because, for most marine species, these environmental changes will occur over a number of generations. Acclimation through phenotypic plasticity and adaptation through genetic selection could help populations of some species cope with future warmer and more acidic oceans. Coral reef species are predicted to be some of the most vulnerable to climate change because they live close to their thermal limits. Yet, their evolutionary history may indicate that they possess adaptations that enable them to cope with a high CO2 environment. Here, we first explore the evolutionary history of reef fishes and how their history has shaped their physiological adaptations to environmental temperatures and pCO2. We examine current-day thermal and CO2 environments experienced by coral reef fishes and summarize experimental studies that have tested how they respond to elevated temperatures and pCO2 levels. We then examine evidence for acclimation and adaptation to projected ocean warming and acidification. Indeed, new studies have demonstrated the potential for transgenerational plasticity and heritable genetic variation that would allow some fishes to maintain performance as the oceans warm and become more acidic. We conclude by outlining management approaches – specifically those that can help preserve genetic variation by maintaining population size – to enhance the potential for genetic adaptation to climate change.

{Extract} The transition from swimming to walking was an important event in the evolution of tetrapods. To understand this transition, researchers have studied movement in many extinct and extant aquatic and semi-aquatic species. The epaulette shark Hemiscillum ocellatum uses slow-to-medium walking, fast walking, and swimming forms of aquatic locomotion. We described kinematic differences between the three gaits in neonate (n=6) and juvenile (n=6) sharks hatched and reared in the laboratory. Neonates retain nutrition from an internal yolk until they develop a consistent feeding schedule (~35d post-hatch). They are then classified as juveniles, foraging for worms, crustaceans, and small fish. We hypothesized that changes in diet and feeding habits would affect gait performance between neonates and juveniles. Using video tracking software and 13 anatomical landmarks along the fins, girdles, and body mid-line, whole body velocity, duty factor, fin frequency, girdle rotation, and body curvature were calculated to identify characteristic movements of the gaits for each shark. Velocity was greater in neonates when compared to juveniles across all gaits; however, both groups increased velocity from walking to swimming. Regardless of gait, pelvic girdles had a greater range of motion than pectoral girdles for both neonates and juveniles. In juveniles, regardless of gait, the contralateral sides of the pectoral and pelvic girdles were synchronized during lateral excursions. Neonates, however, exhibited overlapping of ipsilateral sides of the girdles. Understanding the transition from neonate to juvenile locomotory forms in this species could provide insight on the water to land transition of tetrapods.

Elevated CO2 levels have been shown to affect metabolic performance in some coral reef fishes. However, all studies to date have employed stable elevated CO2 levels, whereas reef habitats can experience substantial diel fluctuations in pCO2 ranging from ±50 to 600 μatm around the mean, fluctuations that are predicted to increase in magnitude by the end of the century. Additionally, past studies have often investigated the effect of elevated CO2 in isolation, despite the fact that ocean temperatures will increase in tandem with CO2 levels. Here, we tested the effects of stable (1000 μatm) versus diel-cycling (1000 ± 500 μatm) elevated CO2 conditions and elevated temperature (+2 °C) on metabolic traits of juvenile spiny damselfish, Acanthochromis polyacanthus. Resting oxygen uptake rates (ṀO2) were higher in fish exposed to stable elevated CO2 conditions when compared to fish from stable control conditions, but were restored to control levels under diel CO2 fluctuations. However, the benefits of diel CO2 fluctuations were diminished at elevated temperature. Factorial aerobic scope showed a similar pattern, but neither maximal ṀO2 nor absolute aerobic scope was affected by CO2 or temperature. Our results suggest that diel CO2 cycles can ameliorate the increased metabolic cost associated with elevated CO2, but elevated temperature diminishes the benefits of diel CO2 cycles. Thus, previous studies may have misestimated the effect of ocean acidification on the metabolic performance of reef fishes by not accounting for environmental CO2 fluctuations. Our findings provide novel insights into the interacting effects of diel CO2 fluctuations and temperature on the metabolic performance of reef fishes.

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.

Increasing temperatures are expected to significantly affect the physiological performance of ectotherms, particularly in tropical locations. The shape of an organism's thermal reaction norm can provide important information on its capacity to persist under climate change scenarios; however, difficulty lies in choosing a measurable trait that best depicts physiological performance. This study investigated the effects of elevated temperatures on processes related to oxygen uptake and delivery, including oxygen consumption, haematology, and tissue health for a low-latitude population of coral reef damselfish. Acanthochromis polyacanthus were collected from the Torres Strait (10°31–46′S, 142°20–35′E) and maintained at current average ocean temperatures (+0 °C; seasonally cycling), + 1.5 °C and + 3 °C higher than present day temperatures for 10 months. Aerobic performance indicated a limit to metabolic function at + 3 °C (33 °C), following an increase in aerobic capacity at + 1.5 °C (31.5 °C). Neither haematological parameters nor gill morphology showed the same improvement in performance at + 1.5 °C. Gill histopathology provided the first indicator of a decline in organism health, which corresponded with mortality observations from previous research. Findings from this study suggest thermal specialisation in this low-latitude population as well as variation in thermal sensitivity, depending on the physiological trait.

Long-term exposure to projected future CO2 levels has no effect on the aerobic performance of two tropical cephalopod species. The resting oxygen uptake rates, maximal oxygen uptake rates, aerobic scope, and recovery time of both bigfin reef squid and two-toned pygmy squid were unaltered by elevated CO2., Squid and many other cephalopods live continuously on the threshold of their environmental oxygen limitations. If the abilities of squid to effectively take up oxygen are negatively affected by projected future carbon dioxide (CO2) levels in ways similar to those demonstrated in some fish and invertebrates, it could affect the success of squid in future oceans. While there is evidence that acute exposure to elevated CO2 has adverse effects on cephalopod respiratory performance, no studies have investigated this in an adult cephalopod after relatively prolonged exposure to elevated CO2 or determined any effects on aerobic scope. Here, we tested the effects of prolonged exposure (≥20% of lifespan) to elevated CO2 levels (~1000 μatm) on the routine and maximal oxygen uptake rates, aerobic scope and recovery time of two tropical cephalopod species, the two-toned pygmy squid, Idiosepius pygmaeus and the bigfin reef squid, Sepioteuthis lessoniana. Neither species exhibited evidence of altered aerobic performance after exposure to elevated CO2 when compared to individuals held at control conditions. The recovery time of I. pygmaeus under both control and elevated CO2 conditions was less than 1 hour, whereas S. lessoniana required approximately 8 hours to recover fully following maximal aerobic performance. This difference in recovery time may be due to the more sedentary behaviours of I. pygmaeus. The ability of these two cephalopod species to cope with prolonged exposure to elevated CO2 without detriment to their aerobic performance suggests some resilience to an increasingly high CO2 world.

Marine protected areas (MPAs) can protect shark populations from targeted fisheries, but resident shark populations may remain exposed to stressors like capture as bycatch and environmental change. Populations of young sharks that rely on shallow coastal habitats, e.g. as nursery areas, may be at risk of experiencing these stressors. The purpose of this study was to characterize various components of the physiological stress response of neonatal reef sharks following exposure to an exhaustive challenge under relevant environmental conditions. To accomplish this, we monitored markers of the secondary stress response and measured oxygen uptake rates (⁠MO2⁠) to compare to laboratory-derived baseline values in neonatal blacktip reef (Carcharhinus melanopterus) and sicklefin lemon sharks (Negaprion acutidens). Measurements occurred over three hours following exposure to an exhaustive challenge (gill-net capture with air exposure). Blood lactate concentrations and pH deviated from baseline values at the 3-h sample, indicating that both species were still stressed 3 h after capture. Evidence of a temperature effect on physiological status of either species was equivocal over 28–31°C. However, aspects of the physiological response were species-specific; N. acutidens exhibited a larger difference in blood pH relative to baseline values than C. melanopterus, possibly owing to higher minimum MO2⁠. Neither species experienced immediate mortality during the exhaustive challenge; although, single instances of delayed mortality were documented for each species. Energetic costs and recovery times could be extrapolated for C. melanopterus via respirometry; sharks were estimated to expend 9.9 kJ kg−1 (15% of energy expended on daily swimming) for a single challenge and could require 8.4 h to recover. These data suggest that neonatal C. melanopterus and N. acutidens are resilient to brief gill-net capture durations, but this was under a narrow temperature range. Defining species' vulnerability to stressors is important for understanding the efficacy of shark conservation tools, including MPAs.

Sharks have maintained a key role in marine food webs for 400 million years and across varying physicochemical contexts, suggesting plasticity to environmental change. In this study, we investigated the biochemical effects of ocean acidification (OA) levels predicted for 2100 (pCO(2) ~ 900 μatm) on newly hatched tropical whitespotted bamboo sharks (Chiloscyllium plagiosum). Specifically, we measured lipid, protein, and DNA damage levels, as well as changes in the activity of antioxidant enzymes and non-enzymatic ROS scavengers in juvenile sharks exposed to elevated CO(2) for 50 days following hatching. Moreover, we also assessed the secondary oxidative stress response, i.e., heat shock response and ubiquitin levels. Newly hatched sharks appear to cope with OA-related stress through a range of tissue-specific biochemical strategies, specifically through the action of antioxidant enzymatic compounds. Our findings suggest that ROS-scavenging molecules, rather than complex enzymatic proteins, provide an effective defense mechanism in dealing with OA-elicited ROS formation. We argue that sharks’ ancient antioxidant system, strongly based on non-enzymatic antioxidants (e.g., urea), may provide them with resilience towards OA, potentially beyond the tolerance of more recently evolved species, i.e., teleosts. Nevertheless, previous research has provided evidence of detrimental effects of OA (interacting with other climate-related stressors) on some aspects of shark biology. Moreover, given that long-term acclimation and adaptive potential to rapid environmental changes are yet experimentally unaccounted for, future research is warranted to accurately predict shark physiological performance under future ocean conditions. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1007/s12192-018-0892-3) contains supplementary material, which is available to authorized users.

Boat noise is becoming increasingly common and is now recognized as an environmental pollutant (Slabbekoorn et al., 2010). We show, for the first time that boat noise elicits a stress response in fish embryos, and that their stress response is greater upon exposure to 2-stroke engines than 4-stroke engines., Human generated noise is changing the natural underwater soundscapes worldwide. The most pervasive sources of underwater anthropogenic noise are motorboats, which have been found to negatively affect several aspects of fish biology. However, few studies have examined the effects of noise on early life stages, especially the embryonic stage, despite embryo health being critical to larval survival and recruitment. Here, we used a novel setup to monitor heart rates of embryos from the staghorn damselfish (Amblyglyphidodon curacao) in shallow reef conditions, allowing us to examine the effects of in situ boat noise in context with real-world exposure. We found that the heart rate of embryos increased in the presence of boat noise, which can be associated with the stress response. Additionally, we found 2-stroke outboard-powered boats had more than twice the effect on embryo heart rates than did 4-stroke powered boats, showing an increase in mean individual heart rate of 1.9% and 4.6%, respectively. To our knowledge this is the first evidence suggesting boat noise elicits a stress response in fish embryo and highlights the need to explore the ecological ramifications of boat noise stress during the embryo stage. Also, knowing the response of marine organisms caused by the sound emissions of particular engine types provides an important tool for reef managers to mitigate noise pollution.

As global temperatures increase, fish populations at low latitudes are thought to be at risk as they are adapted to narrow temperature ranges and live at temperatures close to their thermal tolerance limits. Behavioural movements, based on a preference for a specific temperature (T pref), may provide a strategy to cope with changing conditions. A temperature-sensitive coral reef cardinalfish (Cheilodipterus quinquelineatus) was exposed to 28 °C (average at collection site) or 32 °C (predicted end-of-century) for 6 weeks. T pref was determined using a shuttlebox system, which allowed fish to behaviourally manipulate their thermal environment. Regardless of treatment temperature, fish preferred 29.5 ± 0.25 °C, approximating summer average temperatures in the wild. However, 32 °C fish moved more frequently to correct their thermal environment than 28 °C fish, and daytime movements were more frequent than night-time movements. Understanding temperature-mediated movements is imperative for predicting how ocean warming will influence coral reef species and distribution patterns.

Increased oceanic uptake of atmospheric carbon dioxide (CO2) is a threat to marine organisms and ecosystems. Among the most dramatic consequences predicted to date are behavioural impairments in marine fish which appear to be caused by the interference of elevated CO2 with a key neurotransmitter receptor in the brain. In this study, we tested the effects of elevated CO2 on the foraging and shelter-seeking behaviours of the reef-dwelling epaulette shark, Hemiscyllium ocellatum. Juvenile sharks were exposed for 30 d to control CO2 (400 µatm) and two elevated CO2 treatments (615 and 910 µatm), consistent with medium- and high-end projections for ocean pCO2 by 2100. Contrary to the effects observed in teleosts and in some other sharks, behaviour of the epaulette shark was unaffected by elevated CO2. A potential explanation is the remarkable adaptation of H. ocellatum to low environmental oxygen conditions (hypoxia) and diel fluctuations in CO2 encountered in their shallow reef habitat. This ability translates into behavioural tolerance of near-future ocean acidification, suggesting that behavioural tolerance and subsequent adaptation to projected future CO2 levels might be possible in some other fish, if adaptation can keep pace with the rate of rising CO2 levels.

Reduced water quality, in particular increases in suspended sediments, has been linked to declines in fish abundance on coral reefs. Changes in gill structure induced by suspended sediments have been hypothesized to impair gill function and may provide a mechanistic basis for the observed declines; yet, evidence for this is lacking. We exposed juveniles of three reef fish species ( Amphiprion melanopus , Amphiprion percula and Acanthochromis polyacanthus ) to suspended sediments (0–180 mg l −1 ) for 7 days and examined changes in gill structure and metabolic performance (i.e. oxygen consumption). Exposure to suspended sediments led to shorter gill lamellae in A. melanopus and A. polyacanthus and reduced oxygen diffusion distances in all three species. While A. melanopus exhibited impaired oxygen uptake after suspended sediment exposure, i.e. decreased maximum and increased resting oxygen consumption rates resulting in decreased aerobic scope, the oxygen consumption rates of the other two species remained unaffected. These findings imply that species sensitive to changes in gill structure such as A. melanopus may decline in abundance as reefs become more turbid, whereas species that are able to maintain metabolic performance despite suspended sediment exposure, such as A. polyacanthus or A. percula , may be able to persist or gain a competitive advantage.

The term ‘Anthropocene’ describes Earth's current geological period, which is characterized by human-induced changes to our atmosphere, geology and biodiversity. Although the narrative surrounding the fate of the world's species and ecosystems is often negative, many researchers are calling for strategies that can contribute to a ‘good Anthropocene’. We outline how the field of conservation physiology can infuse optimistic perspectives, pragmatic approaches and heightened public engagement into this pursuit., It has been proposed that we are now living in a new geological epoch known as the Anthropocene, which is specifically defined by the impacts that humans are having on the Earth's biological diversity and geology. Although the proposal of this term was borne out of an acknowledgement of the negative changes we are imparting on the globe (e.g. climate change, pollution, coastal erosion, species extinctions), there has recently been action amongst a variety of disciplines aimed at achieving a ‘good Anthropocene’ that strives to balance societal needs and the preservation of the natural world. Here, we outline ways that the discipline of conservation physiology can help to delineate a hopeful, progressive and productive path for conservation in the Anthropocene and, specifically, achieve that vision. We focus on four primary ways that conservation physiology can contribute, as follows: (i) building a proactive approach to conservation; (ii) encouraging a pragmatic perspective; (iii) establishing an appreciation for environmental resilience; and (iv) informing and engaging the public and political arenas. As a collection of passionate individuals combining theory, technological advances, public engagement and a dedication to achieving conservation success, conservation physiologists are poised to make meaningful contributions to the productive, motivational and positive way forward that is necessary to curb and reverse negative human impact on the environment.