Behavioural impairment in reef fishes caused by ocean acidification at CO2 seeps

Munday, Philip L.; Cheal, Alistair J.; Dixson, Danielle L.; Rummer, Jodie L.; Fabricius, Katharina

doi:10.1038/nclimate2195

Cited by 157 publications

(148 citation statements)

References 30 publications

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“…The findings of these laboratory experiments have been recently confirmed in the field on natural CO 2 vents, where fish communities, continuously exposed to elevated CO 2 , failed to acclimate and showed striking behavioural abnormalities, such as attraction towards predator odour and increased boldness [6,7]. Nevertheless, CO 2 vents are not a perfect analogue for the future ocean because they are influenced by larval supply from nearby unaffected populations.…”

Section: Introductionmentioning

confidence: 54%

Lost at sea: ocean acidification undermines larval fish orientation via altered hearing and marine soundscape modification

et al. 2016

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The dispersal of larvae and their settlement to suitable habitat is fundamental to the replenishment of marine populations and the communities in which they live. Sound plays an important role in this process because for larvae of various species, it acts as an orientational cue towards suitable settlement habitat. Because marine sounds are largely of biological origin, they not only carry information about the location of potential habitat, but also information about the quality of habitat. While ocean acidification is known to affect a wide range of marine organisms and processes, its effect on marine soundscapes and its reception by navigating oceanic larvae remains unknown. Here, we show that ocean acidification causes a switch in role of present-day soundscapes from attractor to repellent in the auditory preferences in a temperate larval fish. Using natural CO 2 vents as analogues of future ocean conditions, we further reveal that ocean acidification can impact marine soundscapes by profoundly diminishing their biological sound production. An altered soundscape poorer in biological cues indirectly penalizes oceanic larvae at settlement stage because both control and CO 2 -treated fish larvae showed lack of any response to such future soundscapes. These indirect and direct effects of ocean acidification put at risk the complex processes of larval dispersal and settlement.

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Section: Introductionmentioning

confidence: 54%

Lost at sea: ocean acidification undermines larval fish orientation via altered hearing and marine soundscape modification

et al. 2016

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“…In addition to elevated sea surface temperature (SST), a growing body of literature has focused on the impacts ocean acidification will have on marine teleosts; however, the majority of these studies have focused primarily on tropical or temperate species (Melzner et al, 2009;Munday et al, 2009a;Munday et al, 2009b;Munday et al, 2010;Munday et al, 2011;Esbaugh et al, 2012;Heuer et al, 2012;Nowicki et al, 2012;Bignami et al, 2013;Chivers et al, 2014;Munday et al, 2014;Murray et al, 2014;Pope et al, 2014). Despite projections that indicate changes in SST and partial pressure of CO 2 (Ṗ CO2 ) in seawater will impact higher latitudes faster and to a greater Is warmer better?…”

Section: Introductionmentioning

confidence: 99%

Is warmer better? Decreased oxidative damage in notothenioid fish after long-term acclimation to multiple stressors

Enzor

Place

2014

Journal of Experimental Biology

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Antarctic fish of the suborder Notothenioidei have evolved several unique adaptations to deal with subzero temperatures. However, these adaptations may come with physiological trade-offs, such as an increased susceptibility to oxidative damage. As such, the expected environmental perturbations brought on by global climate change have the potential to significantly increase the level of oxidative stress and cellular damage in these endemic fish. Previous single stressor studies of the notothenioids have shown they possess the capacity to acclimate to increased temperatures, but the cellularlevel effects remain largely unknown. Additionally, there is little information on the ability of Antarctic fish to respond to ecologically relevant environmental changes where multiple variables change concomitantly. We have examined the potential synergistic effects that increased temperature and Ṗ CO2 have on the level of protein damage in Trematomus bernacchii, Pagothenia borchgrevinki and Trematomus newnesi, and combined these measurements with changes in total enzymatic activity of catalase (CAT) and superoxide dismutase (SOD) in order to gauge tissue-specific changes in antioxidant capacity. Our findings indicate that total SOD and CAT activity levels displayed only small changes across treatments and tissues. Short-term acclimation to decreased seawater pH and increased temperature resulted in significant increases in oxidative damage. Surprisingly, despite no significant change in antioxidant capacity, cellular damage returned to near-basal levels, and significantly decreased in T. bernacchii, after long-term acclimation. Overall, these data suggest that notothenioid fish currently maintain the antioxidant capacity necessary to offset predicted future ocean conditions, but it remains unclear whether this capacity comes with physiological trade-offs.

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“…Our results suggest that P. hypophthalmus retains functional GABA A receptor activity in high-CO 2 environments and consequently avoids the CO 2 -induced behavioural alterations observed in numerous normocapnia-native reef fishes . Assuming that P. hypophthalmus or its ancestors were at one point native to normocapnic environments, this would suggest that fish are indeed capable of adapting to increases in environmental CO 2 in a way that mitigates the adverse behaviours observed in recent studies (Welch et al, 2014; but see Munday et al, 2014). However, the ability of natural selection to adapt species to hypercapnia will of course depend on the presence of relevant gene variants in the gene pool and on the rate at which environmental CO 2 levels increase, and there is a considerable risk that the present rate is too high to allow adaptation through natural selection.…”

Section: Discussionmentioning

confidence: 99%

Ambient CO2, fish behaviour and altered GABAergic neurotransmission: exploring the mechanism of CO2-altered behaviour by taking a hypercapnia dweller down to low CO2 levels

Regan

Turko

Heras

et al. 2016

Journal of Experimental Biology

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Recent studies suggest that projected rises of aquatic CO 2 levels cause acid-base regulatory responses in fishes that lead to altered GABAergic neurotransmission and disrupted behaviour, threatening fitness and population survival. It is thought that changes in Cl − and HCO 3 − gradients across neural membranes interfere with the function of GABA-gated anion channels (GABA A receptors). So far, such alterations have been revealed experimentally by exposing species living in low-CO 2 environments, like many oceanic habitats, to high levels of CO 2 (hypercapnia). To examine the generality of this phenomenon, we set out to study the opposite situation, hypothesizing that fishes living in typically hypercapnic environments also display behavioural alterations if exposed to low CO 2 levels. This would indicate that ion regulation in the fish brain is fine-tuned to the prevailing CO 2 conditions. We quantified pH regulatory variables and behavioural responses of Pangasianodon hypophthalmus, a fish native to the hypercapnic Mekong River, acclimated to high-CO 2 (3.1 kPa) or low-CO 2 (0.04 kPa) water. We found that brain and blood pH was actively regulated and that the low-CO 2 fish displayed significantly higher activity levels, which were reduced after treatment with gabazine, a GABA A receptor blocker. This indicates an involvement of the GABA A receptor and altered Cl − and HCO 3 − ion gradients. Indeed, Goldman calculations suggest that low levels of environmental CO 2 may cause significant changes in neural ion gradients in P. hypophthalmus. Taken together, the results suggest that brain ion regulation in fishes is fine-tuned to the prevailing ambient CO 2 conditions and is prone to disruption if these conditions change.

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Behavioural impairment in reef fishes caused by ocean acidification at CO2 seeps

Cited by 157 publications

References 30 publications

Lost at sea: ocean acidification undermines larval fish orientation via altered hearing and marine soundscape modification

Lost at sea: ocean acidification undermines larval fish orientation via altered hearing and marine soundscape modification

Is warmer better? Decreased oxidative damage in notothenioid fish after long-term acclimation to multiple stressors

Ambient CO2, fish behaviour and altered GABAergic neurotransmission: exploring the mechanism of CO2-altered behaviour by taking a hypercapnia dweller down to low CO2 levels

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