Foraging behaviour of the epaulette shark Hemiscyllium ocellatum is not affected by elevated CO2

Abstract

Increased oceanic uptake of atmospheric carbon dioxide (CO2) is a threat to marine organisms and ecosystems. Among the most dramatic consequences predicted to date are behavioural impairments in marine fish which appear to be caused by the interference of elevated CO2 with a key neurotransmitter receptor in the brain. In this study, we tested the effects of elevated CO2 on the foraging and shelter-seeking behaviours of the reef-dwelling epaulette shark, Hemiscyllium ocellatum. Juvenile sharks were exposed for 30 d to control CO2 (400 µatm) and two elevated CO2 treatments (615 and 910 µatm), consistent with medium- and high-end projections for ocean pCO2 by 2100. Contrary to the effects observed in teleosts and in some other sharks, behaviour of the epaulette shark was unaffected by elevated CO2. A potential explanation is the remarkable adaptation of H. ocellatum to low environmental oxygen conditions (hypoxia) and diel fluctuations in CO2 encountered in their shallow reef habitat. This ability translates into behavioural tolerance of near-future ocean acidification, suggesting that behavioural tolerance and subsequent adaptation to projected future CO2 levels might be possible in some other fish, if adaptation can keep pace with the rate of rising CO2 levels.

Biological responses of sharks to ocean acidification

“…The physiological effects of simulated end-of-century elevated CO 2 conditions have only been evaluated in four relatively sedentary, benthic species: the temperate lesserspotted (Scyliorhinus canicula) catshark [38] and Port Jackson (H. portusjacksoni) sharks [39,40] and the tropical bamboo (C. punctatum) [32][33][34] and epaulette (H. ocellatum) sharks [35,36] (table 1). Previous studies investigating physiological processes under elevated CO 2 in sharks have been conducted at very high CO 2 levels (.8-10 mm Hg, approximately 10 000-13 000 matm) (e.g.…”

Antagonistic effects of ocean acidification and warming on hunting sharks

“…However, antagonistic responses in interaction studies are very uncommon with only 17% of the studies reviewed showing such a response (Przeslawski et al ). Therefore, studies that have for example argued the potential existence of naturally‐adapted populations based on lack of a negative CO 2 effects in single‐stressor experiments (Munday et al , Heinrich et al ) may offer necessary, but insufficiently tested insights on the existence of resilient populations that might replenish more sensitive populations in a future warmer as well as acidified ocean.…”

“…Elevated CO 2 caused a shift in swimming patterns and increased lateralization in the small‐spotted cat sharks Scyliorhinus canicula (Green and Jutfelt ), reduced food odour tracking and attack behaviour in the smooth dogfish Mustelus canis (Dixson et al ), and reduced the ability of Port Jackson shark Heterodontus portusjacksoni to locate food through odour tracking (Pistevos et al ). However, no effect of high CO 2 was found on the foraging and sheltering behaviour of the epaulette shark Hemiscyllium ocellatum which also showed a high tolerance to hypoxia (Heinrich et al ). Furthermore, elevated temperature increased food consumption rates in the Port Jackson shark (Pistevos et al ).…”

“…The behaviour of marine animals is sensitive to ocean acidification (Nagelkerken and Munday ), including impaired decision‐making (Domenici et al ), reduced olfactory preferences (Munday et al , Cripps et al ) and auditory responses (Rossi et al ). In elasmobranchs, acidification causes a spectrum of behavioural and physiological responses that range from no effects (Heinrich et al ) to reduced odour tracking and hunting (Dixson et al , Pistevos et al ). Whilst elasmobranchs physiologically compensate for acid–base disturbances in similar ways to teleosts (Claiborne et al , Brauner and Baker ), they have mechanisms that involve stronger buffering capacity (Berenbrink et al , Heinrich et al ) and acid excretion processes (Wood et al ).…”

Exposure to elevated carbon dioxide does not impair short‐term swimming behaviour or shelter‐seeking in a predatory coral‐reef fish

“…Thus, although the observations made here were relatively acute, effects of exposure to high CO 2 were expected, especially in light of the large effect sizes reported in some of the previous studies (Dixson et al ., ; Munday et al ., ). Nevertheless, there is a growing number of studies that have failed to detect any statistically significant behavioural changes in coral‐reef fish acclimated to high CO 2 (Bender et al ., ; Heinrich et al ., ; Sundin et al ., ). The measurements made in this study primarily involved the rapidity with which fish could orient themselves upon release at the surface, identify a nearby shelter and swim towards and enter that shelter.…”