Elevated carbon dioxide alters the plasma composition and behaviour of a shark

Abstract

Increased carbon emissions from fossil fuels are increasing the pCO 2 of the ocean surface waters in a process called ocean acidification. Elevated water pCO 2 can induce physiological and behavioural effects in teleost fishes, although there appear to be large differences in sensitivity between species. There is currently no information available on the possible responses to future ocean acidification in elasmobranch fishes. We exposed smallspotted catsharks (Scyliorhinus canicula) to either control conditions or a year 2100 scenario of 990 matm pCO 2 for four weeks. We did not detect treatment effects on growth, resting metabolic rate, aerobic scope, skin denticle ultrastructure or skin denticle morphology. However, we found that the elevated pCO 2 group buffered internal acidosis via HCO À 3 accumulation with an associated increase in Na þ , indicating that the blood chemistry remained altered despite the long acclimation period. The elevated pCO 2 group also exhibited a shift in their nocturnal swimming pattern from a pattern of many starts and stops to more continuous swimming. Although CO 2 -exposed teleost fishes can display reduced behavioural asymmetry (lateralization), the CO 2 -exposed sharks showed increased lateralization. These behavioural effects may suggest that elasmobranch neurophysiology is affected by CO 2 , as in some teleosts, or that the sharks detect CO 2 as a constant stressor, which leads to altered behaviour. The potential direct effects of ocean acidification should henceforth be considered when assessing future anthropogenic effects on sharks.

Intraspecific variation in physiological performance of a benthic elasmobranch challenged by ocean acidification and warming

“…It is possible that L. erinacea from GB might be already 'pre-adapted' to acidification because of the elevated and frequent fluctuations in pH in their environment as a consequence of strong upwelling in the area (Pershing et al, 2001). Alternatively, it is possible that given that GoM skates have a reduced aerobic capacity, they might be more strongly affected by elevated plasma P CO2 and HCO 3 − (as seen in other elasmobranch species; Green and Jutfelt, 2014) as a consequence of increased acidification.…”

“…Moreover, in both localities, low pH increased the recovery time after exhaustive exercise. Possibly, acidification may have caused an elevation in P CO2 and HCO 3 − in the plasma (Green and Jutfelt, 2014), thereby increasing the costs associated with maintaining homeostasis. It is therefore possible that these additional costs might have significantly prolonged the time to recovery as young skates had to 'pay off' the oxygen debt after exhaustive anaerobic exercise (Svendsen et al, 2012;Webb, 1994).…”

“…Temperature is an important ecological factor, known to have a profound effect on many metabolic processes in aquatic ectotherms, such as fishes (Di Santo and Bennett, 2011a;Fry, 1971;Magnuson et al, 1979). At the same time, although some studies report little to no effect (or even a positive effect) of CO 2 on fishes (see, for example, Green and Jutfelt, 2014;Heinrich et al, 2014;Jutfelt and Hedgärde, 2015;Rummer et al, 2013), several studies have presented data suggesting that increasing ocean acidification has the potential to exert several adverse effects on fish life history traits, such as malformation during skeletogenesis (Chambers et al, 2013), reduced survival (Baumann and Conover, 2011), reduced body condition and increased developmental time , as well as on several other important behavioral and physiological traits, such as alertness, predator avoidance and hunting (Ferrari et al, 2012a,b;Hamilton et al, 2014;Jutfelt et al, 2013;Munday et al, 2009;Näslund et al, 2015).…”

Acid–base physiology, neurobiology and behaviour in relation to CO2-induced ocean acidification

“…P CO2 between 600 and 2000 µatm). The pattern that emerged was complete regulation of blood plasma pH and a 2-5 mmol l −1 increase in blood plasma [HCO 3 − ] Esbaugh et al, 2016Esbaugh et al, , 2012Green and Jutfelt, 2014;Heinrich et al, 2014;Heuer et al, 2016;Strobel et al, 2012) (Table 1). Only three studies measured blood plasma [Cl − ], but none of them found significant changes after exposure to OA-like conditions Green and Jutfelt, 2014;Heinrich et al, 2014).…”

“…The pattern that emerged was complete regulation of blood plasma pH and a 2-5 mmol l −1 increase in blood plasma [HCO 3 − ] Esbaugh et al, 2016Esbaugh et al, , 2012Green and Jutfelt, 2014;Heinrich et al, 2014;Heuer et al, 2016;Strobel et al, 2012) (Table 1). Only three studies measured blood plasma [Cl − ], but none of them found significant changes after exposure to OA-like conditions Green and Jutfelt, 2014;Heinrich et al, 2014). The lack of change in plasma [Cl − ] in marine fish could be due to the difficulty in accurately measuring small changes in [Cl − ] compared with 'background' control levels of 140-200 mmol l −1 (see Genz et al, 2008;Erlacher-Reid et al, 2011;Esbaugh et al, 2016;Lin et al, 2003;Toews et al, 1983;reviewed in Evans et al, 2005).…”