Energy use, growth and survival of coral reef snapper larvae reared at elevated temperatures

The success of individuals during the pelagic larval phase is critical to maintaining healthy and viable populations of coral reef fishes; however, it is also the most environmentally sensitive and energetically demanding life stage. Climate change is increasing the frequency and intensity of marine heatwaves, which could have significant effects on the development and survival of larval coral reef fishes. However, little is known about how the larvae of pelagic-spawning coral reef fishes will be affected due to the difficulty of spawning and rearing these species in captivity. In this study, we tested how elevated temperatures, similar to those occurring during a marine heatwave, affected the yolk utilization, growth, and survival of larval, Lutjanus carponotatus, a common mesopredatory fish on Indo-west Pacific coral reefs. Eggs and larvae were reared at a current-day average summer temperature (28.5 °C) and two elevated temperatures (30 °C and 31.5 °C) until 14 d post-hatch (dph). Larvae in the elevated temperatures depleted their yolk reserves 39% faster than at the control temperature. The standard length of larvae was 55% (30 °C) and 92% (31.5 °C) longer in the elevated temperature treatments than the control temperature at 14 dph. Conversely, survival of larvae was 54% (30 °C) and 68% (31.5 °C) lower at elevated temperatures compared with the control temperature. This study provides new insights as to how the early life stages of coral reef fishes could be affected by ocean warming and marine heatwaves, with implications for their population dynamics

Impact of ocean warming on a coral reef fish learning and memory

Tropical ectotherms are highly sensitive to environmental warming, especially coral reef fishes, which are negatively impacted by an increase of a few degrees in ocean temperature. However, much of our understanding on the thermal sensitivity of reef fish is focused on a few traits (e.g., metabolism, reproduction) and we currently lack knowledge on warming effects on cognition, which may endanger decision-making and survival. Here, we investigated the effects of warming on learning and memory in a damselfish species, Acanthochromis polyacanthus. Fish were held at 28–28.5◦C (control group), 30–30.5◦C (moderate warming group) or 31.5–32◦C (high warming group) for 2 weeks, and then trained to associate a blue tag (cue) to the presence of a conspecific (reward). Following 20 training trials (5 days), fish were tested for associative learning (on the following day) and memory storage (after a 5-days interval). The control group A. polyacanthus showed learning of the task and memory retention after five days, but increasing water temperature impaired learning and memory. A thorough understanding of the effects of heat stress, cognition, and fitness is urgently required because cognition may be a key factor determining animals’ performance in the predicted scenario of climate changes. Knowing how different species respond to warming can lead to better predictions of future community dynamics, and because it is species specific, it could pinpoint vulnerable/resilience species

Molecular Response of the Brain to Cross-Generational Warming in a Coral Reef Fish

Ocean warming is a threat to marine biodiversity, as it can push marine species beyond their physiological limits. Detrimental effects can occur when marine poikilotherms are exposed to conditions beyond their thermal optima. However, acclamatory mechanisms, such as plasticity, may enable compensation of detrimental effects if warming is experienced during development or across generations. Studies evaluating the molecular responses of fishes to warming have mostly focused on liver, muscle, and gonads, and little is known about the effects on other vital organs, including the brain. This study evaluated the transcriptional program of the brain in the coral reef fish Acanthochromis polyacanthus, exposed to two different warming scenarios: +1.5°C and +3.0°C, across successive generations. Fish were exposed to these conditions in both developmental (F1 and F2) and transgenerational settings (F2 only), as well as a treatment with step-wise warming between generations. The largest differences in gene expression were between individuals of the first and second generation, a pattern that was corroborated by pairwise comparisons between Control F1 and Control F2 (7,500 DEGs) fish. This large difference could be associated with parental effects, as parents of the F1 generation were collected from the wild, whereas parents of the F2 generation were reared in captivity. A general response to warming was observed at both temperatures and in developmental and transgenerational treatments included protein folding, oxygen transport (i.e., myoglobin), apoptosis and cell death, modification of cellular structure, mitochondrial activity, immunity and changes in circadian regulation. Treatments at the highest temperature showed a reduction in synaptic activity and neurotransmission, which matches previous behavioral observations in coral reef fishes. The Transgenerational +3.0°C treatment showed significant activation of the gene pls3, which is known for the development of neuro-muscular junctions under heat-stress. F2 samples exposed to step-wise warming showed an intermediate response, with few differentially expressed genes compared to developmental and transgenerational groups (except for Transgenerational +1.5°C). In combination with previous studies on liver gene expression, this study indicates that warming produces a molecular signature of stress response in A. polyacanthus that is influenced both by the intensity of warming as well as the duration of exposure

The effects of water temperature on the juvenile performance of two tropical damselfishes expatriating to temperate reefs

Ocean warming associated with global climate change is already inducing geographic range shifts of marine species. Juvenile coral reef fishes transported into temperate latitudes (termed 'vagrant' fishes) can experience winter water temperatures below their normal thermal minimum. Such environmental extremes may increase energetic costs for such fishes, resulting in reduced performance, which may be the governing factor that limits the potential for poleward range expansion of such fishes. This study compared the juvenile physiological performance and behaviour of two congeneric tropical damselfishes which settle during austral summer months within temperate eastern Australia: Abudefduf vaigiensis have an extended southern range, and lower threshold survival temperature than the congeneric A. whitleyi. Physiological and behavioural performance parameters that may be affected by cooler temperature regimes at higher latitudes were measured in aquaria. Lower water temperature resulted in reduced growth rates, feeding rates, burst escape speed and metabolic rates of both species, with significantly reduced performance (up to six-fold reductions) for fishes reared at 18°C relative to 22°C and 26°C. However, A. whitleyi exhibited lower growth rates than A. vaigiensis across all temperatures, and lower aerobic capacity at the lowest temperature (18°C). This difference between species in growth and metabolic capacity suggests that the extended southern distribution and greater overwintering success of A. vaigiensis, in comparison to A. whitleyi is related to thermal performance parameters which are critical in maintaining individual health and survival. Our results support previous findings in the region that water temperature below 22°C represents a critical physiological threshold for tropical Abudefduf species expatriating into temperate south-eastern Australia

Parents exposed to warming produce offspring lower in weight and condition

The parental environment can alter offspring phenotypes via the transfer of non-genetic information. Parental effects may be viewed as an extension of (within-generation) phenotypic plasticity. Smaller size, poorer physical condition, and skewed sex ratios are common responses of organisms to global warming, yet whether parental effects alleviate, exacerbate, or have no impact on these responses has not been widely tested. Further, the relative non-genetic influence of mothers and fathers and ontogenetic timing of parental exposure to warming on offspring phenotypes is poorly understood. Here, we tested how maternal, paternal, and biparental exposure of a coral reef fish (Acanthochromis polyacanthus) to elevated temperature (+1.5°C) at different ontogenetic stages (development vs reproduction) influences offspring length, weight, condition, and sex. Fish were reared across two generations in present-day and projected ocean warming in a full factorial design. As expected, offspring of parents exposed to present-day control temperature that were reared in warmer water were shorter than their siblings reared in control temperature; however, within-generation plasticity allowed maintenance of weight, resulting in a higher body condition. Parental exposure to warming, irrespective of ontogenetic timing and sex, resulted in decreased weight and condition in all offspring rearing temperatures. By contrast, offspring sex ratios were not strongly influenced by their rearing temperature or that of their parents. Together, our results reveal that phenotypic plasticity may help coral reef fishes maintain performance in a warm ocean within a generation, but could exacerbate the negative effects of warming between generations, regardless of when mothers and fathers are exposed to warming. Alternatively, the multigenerational impact on offspring weight and condition may be a necessary cost to adapt metabolism to increasing temperatures. This research highlights the importance of examining phenotypic plasticity within and between generations across a range of traits to accurately predict how organisms will respond to climate change

Sharks and their relatives: can their past help predict their future?

Elasmobranchs (i.e., sharks, skates, and rays) have survived five mass extinction events and changed relatively little throughout their ~450-million-year evolutionary history. Therefore, elasmobranchs may provide critical evolutionary perspectives on how species and populations can elicit phenotypic plasticity and adaptation responses to climate change. Unfortunately, despite their roles as critical apex- and meso-predators, most elasmobranch species are considered to be highly vulnerable to the impacts of fisheries exploitation and climate change, which is compounded by their K-selected life history strategies. Furthermore, the future of elasmobranchs is uncertain at best in the face of anthropogenic climate change because there have only been a handful of studies that have directly investigated the effects of climate change related stressors. Phenotypic plasticity in response to climate change, specifically ocean warming, may be a species’ best chance of resilience given the expedited rate of environmental change. However, despite extensive research on plasticity within and across generations in teleost fishes, there remains a knowledge gap for elasmobranch species, owing to their extended life spans and delayed sexual maturity. Here, we present four case studies on different elasmobranch species to lend perspectives on the capacity for phenotypic plasticity within the context of ocean warming. Furthermore, we discuss potential research avenues and modern technologies that may enable future investigations to empirically explore the capacity for phenotypic plasticity in elasmobranchs

Impacts of ocean warming on the settlement success and post‐settlement survival of Pacific crown‐of‐thorns starfish (Acanthaster cf. solaris)

Ocean warming and population irruptions of crown-of-thorns starfish (CoTS; Acanthaster cf. solaris) are two of the greatest threats to coral reefs. As such, there is significant interest in understanding how CoTS may be directly impacted by rising ocean temperatures. Settlement of planktonic larvae and subsequent metamorphosis is purported to be a major population bottleneck in marine invertebrates, yet it is unknown how ocean warming will impact these processes in CoTS. Herein, the effect of temperature (28 °C ambient, 30 °C, 32 °C, 34 °C) on the settlement success, metamorphic success, and post-settlement survival of this corallivore was explored. While larval settlement was robust to elevated temperature, with at least 94% of larvae settling after 48 h across all temperatures, it was observed that settlement success was lower on substrate that had been pre-treated ≥ 32 °C. Metamorphic success was also significantly constrained at temperatures ≥ 32 °C. At 32 °C and 34 °C metamorphic success was 16% and 63% lower than at ambient temperature, respectively. Significant adverse effects of warming on post-settlement survival were observed at even cooler temperatures, with 10% lower survival at 30 °C compared to at ambient temperature, and at 34 °C, survival was 34% lower. Substantial reductions in metamorphic success and early post-settlement survival at elevated temperatures, as well as negative impacts of warming on the settlement substrate and its capacity to induce settlement, may present a bottleneck for recruitment in a warmer ocean

Effects of elevated temperature on the performance and survival of pacific crown-of-thorns starfish (Acanthaster cf. solaris)

Population irruptions of Pacific crown-of-thorns starfish (Acanthaster cf. solaris) have caused substantial damage to coral reefs, but it is largely unknown how this asteroid will fare in a warmer ocean. We exposed these starfish to one of four thermal treatments, with final temperatures of 26 °C (control, annual average), 28 °C (summer average), 30 °C (summer maximum) and 32 °C (predicted summer maximum by 2100). We measured the righting time, movement rate, standard metabolic rate and probability of survival of the crown-of-thorns starfish at various timepoints over ~ 60 days. We found that while tempera- ture did not affect righting time, it did significantly affect movement rate. The movement rate of starfish increased across the 26 to 30 °C range, with those at 28 °C and 30 °C moving 18 and 27% faster than those at the control temperature. Similarly, the standard metabolic rate of starfish increased from 26 to 30 °C, with metabolism 100% and 260% faster at 28 °C and 30 °C compared to those at the 26 °C control. At 32 °C, individual starfish exhibited a 14% slower movement rate, a 33% slower metabolic rate, and also exhibited a fourfold lower probability of survival than those at 30 °C. These results indicate that 32 °C is above the thermal optimum of crown-of-thorns starfish, suggesting that prolonged exposure to temperatures that are expected to be regularly exceeded under near-future climate change may be detrimental to this species

Surviving the Anthropocene: the resilience of marine animals to climate change

If marine organisms are to persist through the Anthropocene, they will need to be resilient, but what is resilience, and can resilience of marine organisms build within a single lifetime or over generations? The aim of this review is to evaluate the resilience capacity of marine animals in a time of unprecedented global climate change. Resilience is the capacity of an ecosystem, society, or organism to recover from stress. Marine organisms can build resilience to climate change through phenotypic plasticity or adaptation. Phenotypic plasticity involves phenotypic changes in physiology, morphology, or behaviour which improve the response of an organism in a new environment without altering their genotype. Adaptation is an evolutionary longer process, occurring over many generations and involves the selection of tolerant genotypes which shift the average phenotype within a population towards the fitness peak. Research on resilience of marine organisms has concentrated on responses to specific species and single climate change stressors. It is unknown whether phenotypic plasticity and adaptation of marine organisms including molluscs, echinoderms, polychaetes, crustaceans, corals, and fish will be rapid enough for the pace of climate change

Impacts of ocean warming on echinoderms: A meta‐analysis

Rising ocean temperatures are threatening marine species and populations worldwide, and ectothermic taxa are particularly vulnerable. Echinoderms are an ecologically important phylum of marine ectotherms and shifts in their population dynamics can have profound impacts on the marine environment. The effects of warming on echinoderms are highly variable across controlled laboratory-based studies. Accordingly, synthesis of these studies will facilitate the better understanding of broad patterns in responses of echinoderms to ocean warming. Herein, a meta-analysis incorporating the results of 85 studies (710 individual responses) is presented, exploring the effects of warming on various performance predictors. The mean responses of echinoderms to all magnitudes of warming were compared across multiple biological responses, ontogenetic life stages, taxonomic classes, and regions, facilitated by multivariate linear mixed effects models. Further models were conducted, which only incorporated responses to warming greater than the projected end-of-century mean annual temperatures at the collection sites. This meta-analysis provides evidence that ocean warming will generally accelerate metabolic rate (+32%) and reduce survival (−35%) in echinoderms, and echinoderms from subtropical (−9%) and tropical (−8%) regions will be the most vulnerable. The relatively high vulnerability of echinoderm larvae to warming (−20%) indicates that this life stage may be a significant developmental bottleneck in the near-future, likely reducing successful recruitment into populations. Furthermore, asteroids appear to be the class of echinoderms that are most negatively affected by elevated temperature (−30%). When considering only responses to magnitudes of warming representative of end-of-century climate change projections, the negative impacts on asteroids, tropical species and juveniles were exacerbated (−51%, −34% and −40% respectively). The results of these analyses enable better predictions of how keystone and invasive echinoderm species may perform in a warmer ocean, and the possible consequences for populations, communities and ecosystems