Jennifer M. Donelson

Ocean acidification impairs olfactory discrimination and homing ability of a marine fish

The persistence of most coastal marine species depends on larvae finding suitable adult habitat at the end of an offshore dispersive stage that can last weeks or months. We tested the effects that ocean acidification from elevated levels of atmospheric carbon dioxide (CO2) could have on the ability of larvae to detect olfactory cues from adult habitats. Larval clownfish reared in control seawater (pH 8.15) discriminated between a range of cues that could help them locate reef habitat and suitable settlement sites. This discriminatory ability was disrupted when larvae were reared in conditions simulating CO2-induced ocean acidification. Larvae became strongly attracted to olfactory stimuli they normally avoided when reared at levels of ocean pH that could occur ca. 2100 (pH 7.8) and they no longer responded to any olfactory cues when reared at pH levels (pH 7.6) that might be attained later next century on a business-as-usual carbon-dioxide emissions trajectory. If acidification continues unabated, the impairment of sensory ability will reduce population sustainability of many marine species, with potentially profound consequences for marine diversity.

Effects of ocean acidification on the early life history of a tropical marine fish.

Little is known about how fishes and other non-calcifying marine organisms will respond to the increased levels of dissolved CO2 and reduced sea water pH that are predicted to occur over the coming century. We reared eggs and larvae of the orange clownfish, Amphiprion percula, in sea water simulating a range of ocean acidification scenarios for the next 50–100 years (current day, 550, 750 and 1030 ppm atmospheric CO2). CO2 acidification had no detectable effect on embryonic duration, egg survival and size at hatching. In contrast, CO2 acidification tended to increase the growth rate of larvae. By the time of settlement (11 days post-hatching), larvae from some parental pairs were 15 to 18 per cent longer and 47 to 52 per cent heavier in acidified water compared with controls. Larvae from other parents were unaffected by CO2 acidification. Elevated CO2 and reduced pH had no effect on the maximum swimming speed of settlement-stage larvae. There was, however, a weak positive relationship between length and swimming speed. Large size is usually considered to be advantageous for larvae and newly settled juveniles. Consequently, these results suggest that levels of ocean acidification likely to be experienced in the near future might not, in isolation, significantly disadvantage the growth and performance of larvae from benthic-spawning marine fishes.

Parental effects on offspring life histories: when are they important?

Both the parental legacy and current environmental conditions can affect offspring life histories; however, their relative importance and the potential relationship between these two influences have rarely been investigated. We tested for the interacting effects of parental and juvenile environments on the early life history of the marine fish Acanthochromis polyacanthus. Juveniles from parents in good condition were longer and heavier at hatching than juveniles from parents in poor condition. Parental effects on juvenile size were evident up to 29 days post-hatching, but disappeared by 50 days. Offspring from good condition parents had higher early survival than offspring from poor-condition parents when reared in a low-food environment. By contrast, parental condition did not affect juvenile survival in the high-food environment. These results suggest that parental effects on offspring performance are most important when poor environmental conditions are encountered by juveniles. Furthermore, parental effects observed at hatching may often be moderated by compensatory mechanisms when environmental conditions are good.

Thermal sensitivity does not determine acclimation capacity for a tropical reef fish

1. Short-term measures of metabolic responses to warmer environments are expected to indicate the sensitivity of species to regional warming. However, given time, species may be able to acclimate to increasing temperature. Thus, it is useful to determine if short-term responses provide a good predictor for long-term acclimation ability. 2. The tropical reef fish Acanthochromis polyacanthus was used to test whether the ability for developmental thermal acclimation of two populations was indicated by their short-term metabolic response to temperature. 3. While both populations exhibited similar short-term responses of resting metabolic rate (RMR) to temperature, fish from the higher-latitude population were able to fully acclimate RMR, while the lower-latitude population could only partially compensate RMR at the warmest temperature. These differences in acclimation ability are most likely due to genetic differences between the populations rather than differences in thermal regimes. 4. This research indicates that acclimation ability may vary greatly between populations and that understanding such variation will be critical for predicting the impacts of warming environmental temperatures. Moreover, the thermal metabolic reaction norm does not appear to be a good predictor of long-term acclimation ability.

Reproductive Acclimation to Increased Water Temperature in a Tropical Reef Fish

Understanding the capacity of organisms to cope with projected global warming through acclimation and adaptation is critical to predicting their likely future persistence. While recent research has shown that developmental acclimation of metabolic attributes to ocean warming is possible, our understanding of the plasticity of key fitness-associated traits, such as reproductive performance, is lacking. We show that while the reproductive ability of a tropical reef fish is highly sensitive to increases in water temperature, reproductive capacity at +1.5°C above present-day was improved to match fish maintained at present-day temperatures when fish complete their development at the higher temperature. However, reproductive acclimation was not observed in fish reared at +3.0°C warmer than present-day, suggesting limitations to the acclimation possible within one generation. Surprisingly, the improvements seen in reproduction were not predicted by the oxygen- and capacity-limited thermal tolerance hypothesis. Specifically, pairs reared at +1.5°C, which showed the greatest capacity for reproductive acclimation, exhibited no acclimation of metabolic attributes. Conversely, pairs reared at +3.0°C, which exhibited acclimation in resting metabolic rate, demonstrated little capacity for reproductive acclimation. Our study suggests that understanding the acclimation capacity of reproductive performance will be critically important to predicting the impacts of climate change on biological systems.

Rapid adaptive responses to climate change in corals

Pivotal to projecting the fate of coral reefs is the capacity of reef-building corals to acclimatize and adapt to climate change. Transgenerational plasticity may enable some marine organisms to acclimatize over several generations and it has been hypothesized that epigenetic processes and microbial associations might facilitate adaptive responses. However, current evidence is equivocal and understanding of the underlying processes is limited. Here, we discuss prospects for observing transgenerational plasticity in corals and the mechanisms that could enable adaptive plasticity in the coral holobiont, including the potential role of epigenetics and coral-associated microbes. Well-designed and strictly controlled experiments are needed to distinguish transgenerational plasticity from other forms of plasticity, and to elucidate the underlying mechanisms and their relative importance compared with genetic adaptation.

Transgenerational plasticity mitigates the impact of global warming to offspring sex ratios

Global warming poses a threat to organisms with temperature-dependent sex determination because it can affect operational sex ratios. Using a multigenerational experiment with a marine fish, we provide the first evidence that parents developing from early life at elevated temperatures can adjust their offspring gender through nongenetic and nonbehavioural means. However, this adjustment was not possible when parents reproduced, but did not develop, at elevated temperatures. Complete restoration of the offspring sex ratio occurred when parents developed at 1.5 °C above the present-day average temperature for one generation. However, only partial improvement in the sex ratio occurred at 3.0 °C above average conditions, even after two generations, suggesting a limitation to transgenerational plasticity when developmental temperature is substantially increased. This study highlights the potential for transgenerational plasticity to ameliorate some impacts of climate change and that development from early life may be essential for expression of transgenerational plasticity in some traits.

Transgenerational plasticity of reproduction depends on rate of warming across generations

Predicting the impacts of climate change to biological systems requires an understanding of the ability for species to acclimate to the projected environmental change through phenotypic plasticity. Determining the effects of higher temperatures on individual performance is made more complex by the potential for environmental conditions experienced in previous and current generations to independently affect phenotypic responses to high temperatures. We used a model coral reef fish (Acanthochromis polyacanthus) to investigate the influence of thermal conditions experienced by two generations on reproductive output and the quality of offspring produced by adults. We found that more gradual warming over two generations, +1.5°C in the first generation and then +3.0°C in the second generation, resulted in greater plasticity of reproductive attributes, compared to fish that experienced the same increase in one generation. Reproduction ceased at the projected future summer temperature (31.5°C) when fish experienced +3.0°C for two generations. Additionally, we found that transgenerational plasticity to +1.5°C induced full restoration of thermally affected reproductive and offspring attributes, which was not possible with developmental plasticity alone. Our results suggest that transgenerational effects differ depending on the absolute thermal change and in which life stage the thermal change is experienced.

Transgenerational plasticity and climate change experiments: Where do we go from here?

Phenotypic plasticity, both within and across generations, is an important mechanism that organisms use to cope with rapid climate change. While an increasing number of studies show that plasticity across generations (transgenerational plasticity or TGP) may occur, we have limited understanding of key aspects of TGP, such as the environmental conditions that may promote it, its relationship to within-generation plasticity (WGP) and its role in evolutionary potential. In this review, we consider how the detection of TGP in climate change experiments is affected by the predictability of environmental variation, as well as the timing and magnitude of environmental change cues applied. We also discuss the need to design experiments that are able to distinguish TGP from selection and TGP from WGP in multigenerational experiments. We conclude by suggesting future research directions that build on the knowledge to date and admit the limitations that exist, which will depend on the way environmental change is simulated and the type of experimental design used. Such an approach will open up this burgeoning area of research to a wider variety of organisms and allow better predictive capacity of the role of TGP in the response of organisms to future climate change.

Managing consequences of climate-driven species redistribution requires integration of ecology, conservation and social science

Climate change is driving a pervasive global redistribution of the planets species. Species redistribution poses new questions for the study of ecosystems, conservation science and human societies that require a coordinated and integrated approach. Here we review recent progress, key gaps and strategic directions in this nascent research area, emphasising emerging themes in species redistribution biology, the importance of understanding underlying drivers and the need to anticipate novel outcomes of changes in species ranges. We highlight that species redistribution has manifest implications across multiple temporal and spatial scales and from genes to ecosystems. Understanding range shifts from ecological, physiological, genetic and biogeographical perspectives is essential for informing changing paradigms in conservation science and for designing conservation strategies that incorporate changing population connectivity and advance adaptation to climate change. Species redistributions present challenges for human well‐being, environmental management and sustainable development. By synthesising recent approaches, theories and tools, our review establishes an interdisciplinary foundation for the development of future research on species redistribution. Specifically, we demonstrate how ecological, conservation and social research on species redistribution can best be achieved by working across disciplinary boundaries to develop and implement solutions to climate change challenges. Future studies should therefore integrate existing and complementary scientific frameworks while incorporating social science and human‐centred approaches. Finally, we emphasise that the best science will not be useful unless more scientists engage with managers, policy makers and the public to develop responsible and socially acceptable options for the global challenges arising from species redistributions.