What if you can't sense your enemy... and your enemy is an invasive predator?

It turns out that the lionfish—an invasive fish species that is especially plaguing western Atlantic waters these days—is even more of a threat than we originally thought. Some of its prey species, like small coral reef fishes, cannot identify the lionfish as a threat

Physiology can contribute to better understanding, management, and conservation of coral reef fishes

Coral reef fishes, like many other marine organisms, are affected by anthropogenic stressors such as fishing and pollution and, owing to climate change, are experiencing increasing water temperatures and ocean acidification. Against the backdrop of these various stressors, a mechanistic understanding of processes governing individual organismal performance is the first step for identifying drivers of coral reef fish population dynamics. In fact, physiological measurements can help to reveal potential cause-and-effect relationships and enable physiologists to advise conservation management by upscaling results from cellular and individual organismal levels to population levels. Here, we highlight studies that include physiological measurements of coral reef fishes and those that give advice for their conservation. A literature search using combined physiological, conservation and coral reef fish key words resulted in similar to 1900 studies, of which only 99 matched predefined requirements. We observed that, over the last 20 years, the combination of physiological and conservation aspects in studies on coral reef fishes has received increased attention. Most of the selected studies made their physiological observations at the whole organism level and used their findings to give conservation advice on population dynamics, habitat use or the potential effects of climate change. The precision of the recommendations differed greatly and, not surprisingly, was least concrete when studies examined the effects of projected climate change scenarios. Although more and more physiological studies on coral reef fishes include conservation aspects, there is still a lack of concrete advice for conservation managers, with only very few published examples of physiological findings leading to improved management practices. We conclude with a call to action to foster better knowledge exchange between natural scientists and conservation managers to translate physiological findings more effectively in order to obtain evidence-based and adaptive management strategies for the conservation of coral reef fishes

Root effect haemoglobins in fish may greatly enhance general oxygen delivery relative to other vertebrates

The teleost fishes represent over half of all extant vertebrates; they occupy nearly every body of water and in doing so, occupy a diverse array of environmental conditions. We propose that their success is related to a unique oxygen (O2) transport system involving their extremely pH-sensitive haemoglobin (Hb). A reduction in pH reduces both Hb-O2 affinity (Bohr effect) and carrying capacity (Root effect). This, combined with a large arterial-venous pH change (ΔpHa-v) relative to other vertebrates, may greatly enhance tissue oxygen delivery in teleosts (e.g., rainbow trout) during stress, beyond that in mammals (e.g., human). We generated oxygen equilibrium curves (OECs) at five different CO2 tensions for rainbow trout and determined that, when Hb-O2 saturation is 50% or greater, the change in oxygen partial pressure (ΔPO2) associated with ΔpHa-v can exceed that of the mammalian Bohr effect by at least 3-fold, but as much as 21-fold. Using known ΔpHa-v and assuming a constant arterial-venous PO2 difference (Pa-vO2), Root effect Hbs can enhance O2 release to the tissues by 73.5% in trout; whereas, the Bohr effect alone is responsible for enhancing O2 release by only 1.3% in humans. Disequilibrium states are likely operational in teleosts in vivo, and therefore the ΔpHa-v, and thus enhancement of O2 delivery, could be even larger. Modeling with known Pa-vO2 in fish during exercise and hypoxia indicates that O2 release from the Hb and therefore potentially tissue O2 delivery may double during exercise and triple during some levels of hypoxia. These characteristics may be central to performance of athletic fish species such as salmonids, but may indicate that general tissue oxygen delivery may have been the incipient function of Root effect Hbs in fish, a trait strongly associated with the adaptive radiation of teleosts

A negative correlation between behavioural and physiological performance under ocean acidification and warming

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 sing le-stressor treatments. However, a statistically significant negative relationship was detected between the traits in the combined elevated CO(2 )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

Nonlethally assessing elasmobranch ontogenetic shifts in energetics

Body condition is an important proxy for the overall health and energetic status of fishes. The classically used Fulton's condition factor requires length and mass measurements, but mass can be difficult to obtain in large species. Girth measurements can replace mass for wild pelagic sharks. However, girth-calculated condition has not been validated against Fulton's condition factor intraspecifically, across ontogeny or reproduction, or in a controlled setting. We used the epaulette shark (Hemiscyllium ocellatum), because they are amenable to captive reproduction, to track fine-scale body condition changes across life stages, oviparous reproduction and between condition indices. We measured four girths, total length and mass of 16 captive epaulette sharks across 1 year and tracked female reproduction daily. We also collected length and mass data from an additional 72 wild-caught sharks and 155 sharks from five previous studies and two public aquaria to examine the relationship between length and mass for this species. Even though data were derived from a variety of sources, a predictable length–mass relationship (R2 = 0.990) was achievable, indicating that combining data from a variety of sources could help overcome knowledge gaps regarding basic life history characteristics. We also found that condition factor decreased during early life stages, then increased again into adulthood, with predictable changes across the female reproductive cycle. Finally, we determined that both Fulton's and girth condition analyses were comparable. Outcomes from this study uniquely provide body condition changes across the complete life history, including fine-scale female reproductive stages, and validate the use of girths as a nonlethal whole-organism energetic assessment for fishes

The upper thermal limit of epaulette sharks (Hemiscyllium ocellatum) is conserved across three life history stages, sex and body size

Owing to climate change, most notably the increasing frequency of marine heatwaves and long-term ocean warming, better elucidating the upper thermal limits of marine fishes is important for predicting the future of species and populations. The critical thermal maximum (CTmax), or the highest temperature a species can tolerate, is a physiological metric that is used to establish upper thermal limits. Among marine organisms, this metric is commonly assessed in bony fishes but less so in other taxonomic groups, such as elasmobranchs (subclass of sharks, rays and skates), where only thermal acclimation effects on CTmax have been assessed. Herein, we tested whether three life history stages, sex and body size affected CTmax in a tropical elasmobranch, the epaulette shark (Hemiscyllium ocellatum), collected from the reef flats surrounding Heron Island, Australia. Overall, we found no difference in CTmax between life history stages, sexes or across a range of body sizes. Findings from this research suggest that the energetically costly processes (i.e. growth, maturation and reproduction) associated with the life history stages occupying these tropical reef flats do not change overall acute thermal tolerance. However, it is important to note that neither embryos developing in ovo, neonates, nor females actively encapsulating egg cases were observed in or collected from the reef flats. Overall, our findings provide the first evidence in an elasmobranch that upper thermal tolerance is not impacted by life history stage or size. This information will help to improve our understanding of how anthropogenic climate change may (or may not) disproportionally affect particular life stages and, as such, where additional conservation and management actions may be required

Adapt, move, or die: how will tropical coral reef fishes cope with ocean warming?

Previous studies hailed thermal tolerance and the capacity for organisms to acclimate and adapt as the primary pathways for species survival under climate change. Here we challenge this theory. Over the past decade more than 365 tropical stenothermal fish species have been documented moving pole-ward, away from ocean warming hotspots where temperatures 2-3 °C above long-term annual means can compromise critical physiological processes. We examined the capacity of a model species - a thermally-sensitive coral reef fish, Chromis viridis (Pomacentridae) – to use preference behaviour to regulate its body temperature. Movement could potentially circumvent the physiological stress response associated with elevated temperatures and may be a strategy relied upon before genetic adaptation can be effectuated. Individuals were maintained at one of six temperatures (23, 25, 27, 29, 31 and 33 °C) for at least six weeks. We compared the relative importance of acclimation temperature to changes in upper critical thermal limits, aerobic metabolic scope, and thermal preference. While acclimation temperature positively affected the upper critical thermal limit, neither aerobic metabolic scope nor thermal preference exhibited such plasticity. Importantly, when given the choice to stay in a habitat reflecting their acclimation temperatures or relocate, fish acclimated to end-of-century predicted temperatures (i.e., 31 or 33 °C) preferentially sought out cooler temperatures, those equivalent to long-term summer averages in their natural habitats (~29 °C). This was also the temperature providing the greatest aerobic metabolic scope and body condition across all treatments. Consequently, acclimation can confer plasticity in some performance traits, but may be an unreliable indicator of the ultimate survival and distribution of mobile stenothermal species under global warming. Conversely, thermal preference can arise long before, and remain long after, the harmful effects of elevated ocean temperatures take hold and may be the primary driver of the escalating pole-ward migration of species

Will ocean acidification affect the early ontogeny of a tropical oviparous elasmobranch (Hemiscyllium ocellatum)?

Atmospheric CO2 is increasing due to anthropogenic causes. Approximately 30% of this CO2 is being absorbed by the oceans and is causing ocean acidification (OA). The effects of OA on calcifying organisms are starting to be understood, but less is known about the effects on non-calcifying organisms, notably elasmobranchs. One of the few elasmobranch species that has been studied with respect to OA is the epaulette shark, Hemiscyllium ocellatum. Mature epaulette sharks can physiologically and behaviourally tolerate prolonged exposure to elevated CO2, and this is thought to be because they are routinely exposed to diurnal decreases in O2 and probably concomitant increases in CO2 in their coral reef habitats. It follows that H. ocellatum embryos, while developing in ovo on the reefs, would have to be equally if not more tolerant than adults because they would not be able to escape such conditions. Epaulette shark eggs were exposed to either present-day control conditions (420 µatm) or elevated CO2 (945 µatm) and observed every 3 days from 10 days post-fertilization until 30 days post-hatching. Growth (in square centimetres per day), yolk usage (as a percentage), tail oscillations (per minute), gill movements (per minute) and survival were not significantly different in embryos reared in control conditions when compared with those reared in elevated CO2 conditions. Overall, these findings emphasize the importance of investigating early life-history stages, as the consequences are expected to transfer not only to the success of an individual but also to populations and their distribution patterns

Aerobic performance of two tropical cephalopod species unaltered by prolonged exposure to projected future carbon dioxide levels

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 the routine and maximal oxygen uptake rates, aerobic scope and recovery time of two tropical cephalopod species, the two- aerobic scope. Here, we tested the effects of prolonged exposure (≥20% of lifespan) to elevated CO2 levels (∼1000 μatm) on tonedpygmy 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. Ke

Thermal acclimation of tropical coral reef fishes to global heat waves

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 \u3e100 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