Ecological generalism and physiology mediate fish biogeographic ranges under ocean warming.

Climate-driven species redistributions are facilitated by niche modifications that increase a species's chances of establishment in novel communities. It is well understood how range-extending species adjust individual niche traits when entering novel environments, yet whether modification of ecological niche traits collectively alters the pace of range extensions or contractions remains unknown. We quantified habitat niche, abundance, physiological performance and cellular defence/damage of range-extending coral reef fishes and coexisting local temperate fishes along a 2000 km latitudinal gradient. We also assessed their dietary and behavioural niches, and establishment potential, to understand whether ecological generalism facilitates successful range extension of coral reef fishes. The coral reef fish that increased all ecological niches, showed stronger establishment, increased physiological performance and cellular damage, but decreased cellular defence at their cold-range edge, whereas tropical species that showed unmodified ecological niches showed lower establishment. One temperate species showed decreased abundance, habitat niche width and body condition, but increased cellular defence, cellular damage and energy reserves at their warm-trailing range, while other temperate species showed contrasting responses. Therefore, ecological generalists might be more successful than ecological specialists during the initial stages of climate change, with increasing future warming strengthening this pattern by physiologically benefitting tropical generalists but disadvantaging temperate specialists.

Novel ecological interactions alter physiological responses of range-extending tropical and local temperate fishes under ocean warming.

Global warming facilitates species range-expansions, leading to novel biological interactions between local and range-expanding species. Little is still known of how such novel interactions modify the performance of interacting species or how these interactions might be altered under climate change. Here, we used an aquarium experiment to investigate the novel ecological interactions between a poleward range-extending coral reef damselfish ("tropical-vagrant") and a local temperate species ("temperate-local") collected from a climate warming hotspot in SE Australia. We measured the effect of novel interactions (isolated vs. paired fish species) on energy expenditure (activity levels, oxidative stress, and antioxidant responses), energy gain (feeding rates), and growth rates of both fish species under present-day (23 °C) and future ocean temperatures (26 °C). Short-term growth rates were faster in both species under novel interactions (paired species), regardless of elevated temperature. Compared to isolated species, activity level, feeding rate and oxidative stress level were also higher in the paired temperate fish but not in the paired tropical fish. The tropical fish showed an increased feeding rate and long-term growth under elevated temperature, irrespective of novel interactions. We conclude that novel ecological interactions under climate change can be an important driver of physiological traits in sympatric tropical and temperate fishes and can mediate critical physiological performance of fishes under ocean warming.

Future shock: Ocean acidification and seasonal water temperatures alter the physiology of competing temperate and coral reef fishes.

Climate change can directly (physiology) and indirectly (novel species interactions) modify species responses to novel environmental conditions during the initial stages of range shifts. Whilst the effects of climate warming on tropical species at their cold-water leading ranges are well-established, it remains unclear how future seasonal temperature changes, ocean acidification, and novel species interactions will alter the physiology of range-shifting tropical and competing temperate fish in recipient ecosystems. Here we used a laboratory experiment to examine how ocean acidification, future summer vs winter temperatures, and novel species interactions could affect the physiology of competing temperate and range-extending coral reef fish to determine potential range extension outcomes. In future winters (20 °C + elevated pCO2) coral reef fish at their cold-water leading edges showed reduced physiological performance (lower body condition and cellular defence, and higher oxidative damage) compared to present-day summer (23 °C + control pCO2) and future summer conditions (26 °C + elevated pCO2). However, they showed a compensatory effect in future winters through increased long-term energy storage. Contrastingly, co-shoaling temperate fish showed higher oxidative damage, and reduced short-term energy storage and cellular defence in future summer than in future winter conditions at their warm-trailing edges. However, temperate fish benefitted from novel shoaling interactions and showed higher body condition and short-term energy storage when shoaling with coral reef fish compared to same-species shoaling. We conclude that whilst during future summers, ocean warming will likely benefit coral reef fishes extending their ranges, future winter conditions may still reduce coral reef fish physiological functioning, and may therefore slow their establishment at higher latitudes. In contrast, temperate fish species benefit from co-shoaling with smaller-sized tropical fishes, but this benefit may dissipate due to their reduced physiological functioning under future summer temperatures and increasing body sizes of co-shoaling tropical species.

Ocean warming and acidification degrade shoaling performance and lateralization of novel tropical-temperate fish shoals.

Gregarious behaviours are common in animals and provide various benefits such as food acquisition and protection against predators. Many gregarious tropical species are shifting poleward under current ocean warming, creating novel species and social interactions with local temperate taxa. However, how the dynamics of these novel shoals might be altered by future ocean warming and acidification remains untested. Here we evaluate how novel species interactions, ocean acidification and warming affect shoaling dynamics, motor lateralization and boldness of range-extending tropical and co-shoaling temperate fishes under controlled laboratory conditions. Fishes were exposed to 1 of 12 treatments (combinations of three temperature levels, two pCO2  levels and two shoal type levels: mixed species or temperate only) for 38 days. Lateralization (a measure of asymmetric expression of cognitive function in group coordination and predator escape) of tropical and temperate species was right-side biased under present-day conditions, but side bias significantly diminished in tropical and temperate fishes under ocean acidification. Ocean acidification also decreased shoal cohesion irrespective of shoaling type, with mixed-species shoals showing significantly lower cohesion than temperate-only shoals irrespective of climate stressors. Tropical fish became bolder under ocean acidification (after 4 weeks), and temperate fish became bolder with increasing temperature, while ocean acidification dampened temperate fish boldness. Our findings highlight the direct effect of climate stressors on fish behaviour and the interplay with the indirect effects of novel species interactions. Because strong shoal cohesion and lateralization are key determinants of species fitness, their degradation under ocean warming and acidification could adversely affect species performance in novel assemblages in a future ocean, and might slow down tropical species range extensions.