Species interactions alter the selection of thermal environment in a coral reef fish.

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.

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

Highly variable thermal environments, such as coral reef flats, are challenging for marine ectotherms and are thought to invoke the use of behavioural strategies to avoid extreme temperatures and seek out thermal environments close to their preferred temperatures. Common to coral reef flats, the epaulette shark (Hemiscyllium ocellatum) possesses physiological adaptations to hypoxic and hypercapnic conditions, such as those experienced on reef flats, but little is known regarding the thermal strategies used by these sharks. We investigated whether H. ocellatum uses behavioural thermoregulation (i.e., movement to occupy thermally favourable microhabitats) or tolerates the broad range of temperatures experienced on the reef flat. Using an automated shuttlebox system, we determined the preferred temperature of H. ocellatum under controlled laboratory conditions and then compared this preferred temperature to 6 months of in situ environmental and body temperatures of individual H. ocellatum across the Heron Island reef flat. The preferred temperature of H. ocellatum under controlled conditions was 20.7 ± 1.5°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°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.

Habitat complexity influences selection of thermal environment in a common coral reef fish.

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 (T pref) 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; T pref: 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.

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 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.

The emergence emergency: A mudskipper's response to temperatures.

Temperature has a profound effect on all life and a particularly influential effect on ectotherms, such as fishes. Amphibious fishes have a variety of strategies, both physiological and/or behavioural, to cope with a broad range of thermal conditions. This study examined the relationship between prolonged (5 weeks) exposure to a range of temperatures (22, 25, 28, or 32 °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 °C, approximately 5 °C above their summer average temperatures), barred mudskippers exhibited 33.7-97.7% greater oxygen uptake rates at rest (MO2Rest), emerged at a higher temperature (CTe; i.e., a modified critical thermal maxima (CTMax) methodology) of 41.3 ±â€¯0.3 °C relative to those maintained at 28, 25, or 22 °C. The 32 °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 ±â€¯2.1 °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.

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 poleward, 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 6 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 poleward migration of species.