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Physical body condition, the relationship between log10(mass + 1) and log10(SL + 1) of aHalichoeres melanurus (control: n = 10; +2 °C: n = 12), bHalichoeres miniatus (control: n = 8; +2 °C: n = 8) and cThalassoma amblycephalum (control: n = 15; +2 °C: n = 14) reared at control and +2 °C developmental treatments
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For effective conservation and management of marine systems, it is essential that we understand the biological impacts of and capacity for acclimation to increased ocean temperatures. This study investigated for the first time the effects of developing in projected warmer ocean conditions in the tropical wrasse species: Halichoeres melanurus, Halic...
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... This was despite the equatorial populations residing in a very narrow range (e.g., approximately 2°C) and the southern Great Barrier Reef populations residing in a much wider range (e.g., approximately 10°C) of annual, seasonal temperatures , suggesting a wide thermal buffer zone for high latitude populations and high temperature sensitivity in the near-equatorial populations. This is not unprecedented either with loss of hypoxia tolerance , increased metabolic costs (Gardiner et al., 2010;Rodgers et al., 2018Rodgers et al., , 2019, reductions in swimming performance ( Johansen and Jones, 2011), and worsened predator escape responses (i.e., slower reaction times, slower escape speeds, and shorter escape distances; Allan et al., 2015;Motson and Donelson, 2017;Warren et al., 2017) when compared to their control temperature counterparts. Although these trends in coral reef fishes have only been revealed since the early 21st century, this topic has been historically wellresearched in terrestrial species Tewksbury et al., 2008). ...
Coral reef fishes and the ecosystems they support represent some of the most biodiverse and productive ecosystems on the planet yet are under threat as they face dramatic increases in multiple, interacting stressors that are largely intensified by anthropogenic influences, such as climate change. Coral reef fishes have been the topic of 875 studies between 1979 and 2020 examining physiological responses to various abiotic and biotic stressors. Here, we highlight the current state of knowledge regarding coral reef fishes' responses to eight key abiotic stressors (i.e., pollutants, temperature, hypoxia and ocean deoxygenation, pH/CO2, noise, salinity, pressure/depth, and turbidity) and four key biotic stressors (i.e., prey abundance, predator threats, parasites, and disease) and discuss stressors that have been examined in combination. We conclude with a horizon scan to discuss acclimation and adaptation, technological advances, knowledge gaps, and the future of physiological research on coral reef fishes. As we proceed through this new epoch, the Anthropocene, it is critical that the scientific and general communities work to recognize the issues that various habitats and ecosystems, such as coral reefs and the fishes that depend on and support them, are facing so that mitigation strategies can be implemented to protect biodiversity and ecosystem health.
... larval growth and length at settlement decrease in some reef fishes (McLeod et al., 2014). However, maintenance of condition may not be a consistent pattern across reef fishes, as wrasses reared in warmer water had reduced length, weight, and body condition (Motson & Donelson, 2017). It may be that for some reef fishes, high condition is beneficial in elevated temperatures as it can increase predator evasion, competitive ability, and enhance thermal tolerance (Booth & Beretta, 2004;Booth & Hixon, 1999;Grorud-Colvert & Sponaugle, 2006;Robinson et al., 2008); thus, this within-generation plasticity could be adaptive. ...
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. Our study teases apart the timing of maternal and paternal non‐genetic contributions to offspring phenotype in response to warming in a coral reef fish. We found offspring were lower in body weight and physical condition when parents were exposed to elevated water temperature, regardless of when or which parent was exposed. Yet the parental thermal experience did not impact offspring sex ratios. We discuss the ecological consequences of these results in comparison to other ectotherms.
... Here we investigated the thermal sensitivity of two closely-related, but habitat-distinct species of mobile fishes belonging to the family Siganidae, following a period of a 14 week exposure to ambient and elevated temperatures during juvenile development. In comparison to results previously reported for site-attached species, which displayed high thermal sensitivity and negative physical effects at 1.5 to 3°C warming above summer averages (Munday et al. 2008b;Zarco-Perelló et al. 2012;Motson and Donelson 2017), we found evidence of robustness of juvenile rabbitfish to elevated thermal conditions. Although juvenile S. lineatus exhibited behavioral changes (feeding rates and propensity to feed) in response to higher water temperatures, they were able to maintain growth, physical condition and immune function across the 28.0 to 31.5°C developmental temperature range. ...
... Overall, our results suggest that juvenile rabbitfish may be less sensitive to small increases in water temperature than previously studied site-attached species such as damselfish, cardinalfish and wrasses (Sponaugle et al. 2006;Munday et al. 2008a, b;Gardiner et al. 2010;Nilsson et al. 2010;Nowicki et al. 2012;Zarco-Perelló et al. 2012; Fig. 3 Behavioral traits of juvenile S. doliatus and S. lineatus at three experimental temperature treatments: a time until first feeding (i.e., latency to feed) of S. doliatus (n = 10, 10, 9) and S. lineatus (n = 11, 16, 16); b number of bites taken within 5 min by S. doliatus (n = 12, 13, 10) and S. lineatus (n = 11, 16, 16); (c) time spent out of shelter by S. doliatus (n = 12, 13, 11) and S. lineatus (n = 13, 16, 16). In all cases, data are means ± SE Motson and Donelson 2017). Juvenile rabbitfish in the current study also exhibited lower thermal sensitivity than larval and adult coral trout (Plectropomus spp.) in terms of development and growth, although they did demonstrate similar increases in feeding rate at elevated temperatures (Pratchett et al. 2013;Johansen et al. 2015). ...
... While we observed trends of decreased latency and increased feeding rate with warming, S. doliatus showed no significant differences in behavior between temperature treatments. We also observed no differences in the overall length and mass of fish exposed to higher temperatures, although fish had greater body depth as water temperature increased (counter to the expected pattern of reduced growth at elevated temperatures (Munday et al. 2008b;Zarco-Perelló et al. 2012;Motson and Donelson 2017)). This result could have been due to the experimental temperatures being within the thermal tolerance of the species, meaning that higher temperature treatments could have simply provided a thermal advantage in terms of growth rate. ...
The majority of our understanding of the effects of climate change on coral reef fishes are currently based on studies of small-bodied species such as damselfishes. By contrast, we know little about the potential impacts of ocean warming on larger species of herbivorous and detritivorous reef fish, despite them being a critical functional group and an essential source of food protein for millions of people. In addition, we know little of the role of habitat in determining species’ thermal sensitivity and the legitimacy of extrapolating thermal performance across closely-related species from different habitat types. Here we test the effect of exposure to increased water temperature during juvenile development on key physiological and behavioral traits of two species of rabbitfish typically associated with different habitats: Siganus doliatus (reef-associated) and S. lineatus (estuarine). Wild-caught juveniles were reared for 14 weeks at temperatures representing present-day ambient conditions (28.0 °C), late-summer ambient conditions (30.0 °C), or those projected on reefs under future global warming scenarios (31.5 °C). We then measured the somatic (growth, condition, immune response) and behavioral (feeding rate, latency to feed and activity level) traits of individuals within each treatment to determine the sensitivity of each species to elevated water temperatures. Overall, both species showed comparatively robust levels of thermal tolerance, based on previously-documented responses of small-bodied reef fishes. However, two very different patterns emerged. The reef-associated S. doliatus showed a greater physiological response to temperature, with negative effects on hepatosomatic condition and immune function observed in individuals exposed to the 31.5 °C treatment. By contrast, there were no negative physiological effects of temperature observed in S. lineatus and instead we recorded behavioral changes, with individuals at 30 °C and 31.5 °C displaying altered feeding behavior (increased feeding rate and decreased latency to feed). These distinct responses observed between congeners are likely due to their evolutionary history and flag the potential inaccuracies that could arise from extrapolating effects of ocean warming across even closely-related species adapted to different habitats.
... Some of the most heattolerant freshwater species, in terms of AS, are the barramundi Lates calcarifer that maintain AS from 23 to 38°C (Norin et al., 2014Gomez Isaza et al., 2019), the hot-springs population of lake Magadi tilapia Alcolapia grahami with highest AS at 39°C (Wood et al., 2016), and central stoneroller Campostoma anomalum and Southern redbelly dace Chrosomus erythrogaster that maintain AS from 10 to 30°C (Frenette et al., 2019). Most of the marine species that decrease AS are tropical coral reef cardinalfishes (Apogonidae) and damselfishes (Pomacentridae) (Nilsson et al., 2009;Gardiner et al., 2010;Rummer et al., 2014;Motson and Donelson, 2017;Laubenstein et al., 2019). Other marine species seem more resilient (Duthie, 1982;Mallekh and Lagardere, 2002;Marras et al., 2015;Mazloumi et al., 2017;Laubenstein et al., 2018;Crear et al., 2019Crear et al., , 2020Bouyoucos et al., 2020; Table S1). ...
... In other words, longer acclimation periods make it less likely to find a decline in AS at upper temperatures (Lefevre, 2016). The number of studies using an acclimation period of several weeks and even months has now increased (Habary et al., 2017;Motson and Donelson, 2017;Slesinger et al., 2019;Vagner et al., 2019;Zhou et al., 2019), although studies using transgenerational and developmental acclimation remain quite rare. In three coral reef wrasses (Labridae), AS at elevated temperature did not improve with developmental exposure, and the same was the case for spiny chromis damselfish Acanthochromis polyacanthus (Laubenstein et al., 2019), although in this case AS at elevated temperature was restored with transgenerational acclimation (Munday et al., 2017). ...
Warming of aquatic environments as a result of climate change is already having measurable impacts on fishes, manifested as changes in phenology, range shifts and reductions in body size. Understanding the physiological mechanisms underlying these seemingly universal patterns is crucial if we are to reliably predict the fate of fish populations with future warming. This includes an understanding of mechanisms for acute thermal tolerance, as extreme heatwaves may be a major driver of observed effects. The hypothesis of gill oxygen limitation (GOL) is claimed to explain asymptotic fish growth, and why some fish species are decreasing in size with warming; but its underlying assumptions conflict with established knowledge and direct mechanistic evidence is lacking. The hypothesis of oxygen- and capacity-limited thermal tolerance (OCLTT) has stimulated a wave of research into the role of oxygen supply capacity and thermal performance curves for aerobic scope, but results vary greatly between species, indicating that it is unlikely to be a universal mechanism. As thermal performance curves remain important for incorporating physiological tolerance into models, we discuss potentially fruitful alternatives to aerobic scope, notably specific dynamic action and growth rate. We consider the limitations of estimating acute thermal tolerance by a single rapid measure whose mechanism of action is not known. We emphasise the continued importance of experimental physiology, particularly in advancing our understanding of underlying mechanisms, but also the challenge of making this knowledge relevant to the more complex reality.
... For example, exposure to 1.5-3°C above summer averages during early life can partially restore or even enhance aerobic scope of damselfish (Donelson et al., 2011;Donelson, 2015;Grenchik et al., 2013). In contrast, predominately negative developmental effects on body size, aerobic scope, escape performance and swimming ability were observed in juvenile wrasses exposed to 2°C above summer average (Motson and Donelson, 2017). These results suggest that exposure to higher temperature from early life may induce developmental changes to morphology or behaviour that, in turn, influence individual performance; however, all the relevant studies conducted to date have employed designs focused on testing the effect of long-term increases in average water temperature associated with global warming. ...
... The thermal sensitivity of escape performance has been found to vary between species of reef fish tested in various studies. The locomotor aspects of the escape response were not affected by short-term changes in water temperature from 29 to 31°C in three wrasse species (Motson and Donelson, 2017) or in the damselfishes Pomacentrus moluccensis and P. amboinensis (Warren et al., 2017). In contrast, the damselfish P. wardi exhibited reduced escape distance and speed with acute temperature change from 26.7 to 29.6°C (Allan et al., 2015). ...
Marine heatwaves, which are increasing in frequency, duration and intensity owing to climate change, are an imminent threat to marine ecosystems. On coral reefs, heatwave conditions often coincide with periods of peak recruitment of juvenile fishes and exposure to elevated temperature may affect their development. However, whether differences in the duration of high temperature exposure have effects on individual performance is unknown. We exposed juvenile spiny damselfish, Acanthochromis polyacanthus, to increasing lengths of time (3, 7, 30 and 108 days post-hatching) of elevated temperature (+2°C). After 108 days, we measured escape performance at present-day control and elevated temperatures, standard length, mass and critical thermal maximum. Using a Bayesian approach, we show that 30 days or more exposure to +2°C leads to improved escape performance, irrespective of performance temperature, possibly owing to developmental effects of high temperature on muscle development and/or anaerobic metabolism. Continued exposure to elevated temperature for 108 days caused a reduction in body size compared with the control, but not in fish exposed to high temperature for 30 days or less. By contrast, exposure to elevated temperatures for any length of time had no effect on critical thermal maximum, which, combined with previous work, suggests a short-term physiological constraint of ∼37°C in this species. Our study shows that extended exposure to increased temperature can affect the development of juvenile fishes, with potential immediate and future consequences for individual performance.