Ocean acidification impacts on sperm mitochondrial membrane potential bring sperm swimming behaviour near its tipping point

Broadcast spawning marine invertebrates are susceptible to environmental stressors such as climate change, as their reproduction depends on the successful meeting and fertilization of gametes in the water column. Under near-future scenarios of ocean acidification, the swimming behaviour of marine invertebrate sperm is altered. We tested whether this was due to changes in sperm mitochondrial activity by investigating the effects of ocean acidification on sperm metabolism and swimming behaviour in the sea urchin Centrostephanus rodgersii. We used a fluorescent molecular probe (JC-1) and flow cytometry to visualize mitochondrial activity (measured as change in mitochondrial membrane potential, MMP). Sperm MMP was significantly reduced in delta pH -0.3 (35% reduction) and delta pH -0.5 (48% reduction) treatments, whereas sperm swimming behaviour was less sensitive with only slight changes (up to 11% decrease) observed overall. There was significant inter-individual variability in responses of sperm swimming behaviour and MMP to acidified seawater. We suggest it is likely that sperm exposed to these changes in pH are close to their tipping point in terms of physiological tolerance to acidity. Importantly, substantial inter-individual variation in responses of sperm swimming to ocean acidification may increase the scope for selection of resilient phenotypes, which, if heritable, could provide a basis for adaptation to future ocean acidification.

At surface behaviour, dive depth and dive duration and associated hydrographic data of adult male southern elephant seals from King George Island from expedition JUB2010 with links to datasets

Understanding the distribution and foraging ecology of major consumers within pelagic systems, specifically in relation to physical parameters, can be important for the management of bentho-pelagic systems undergoing rapid change associated with global climate change and other anthropogenic disturbances such as fishing (i.e., the Antarctic Peninsula and Scotia Sea). We tracked 11 adult male southern elephant seals (Mirounga leonina), during their five-month post-moult foraging migrations from King George Island (Isla 25 de Mayo), northern Antarctic Peninsula, using tags capable of recording and transmitting behavioural data and in situ temperature and salinity data. Seals foraged mostly within the Weddell-Scotia Confluence, while a few foraged along the western Antarctic Peninsula shelf of the Bellingshausen Sea. Mixed model outputs suggest that the at-sea behaviour of seals was associated with a number of environmental parameters, especially seafloor depth, sea-ice concentrations and the temperature structure of the water column. Seals increased dive bottom times and travelled at slower speeds in shallower areas and areas with increased sea-ice concentrations. Changes in dive depth and durations, as well as relative amount of time spent during the bottom phases of dives, were observed in relation to differences in overall temperature gradient, likely as a response to vertical changes in prey distribution associated with temperature stratification in the water column. Our results illustrate the likely complex influences of bathymetry, hydrography and sea ice on the behaviour of male southern elephant seals in a changing environment and highlight the need for region-specific approaches to studying environmental influences on behaviour.

Seawater carbonate chemistry and brown dottyback (Pseudochromis fuscus) movement and feeding behaviour during experiments, 2011

Changes in olfactory-mediated behaviour caused by elevated CO2 levels in the ocean could affect recruitment to reef fish populations because larval fish become more vulnerable to predation. However, it is currently unclear how elevated CO2 will impact the other key part of the predator-prey interaction - the predators. We investigated the effects of elevated CO2 and reduced pH on olfactory preferences, activity levels and feeding behaviour of a common coral reef meso-predator, the brown dottyback (Pseudochromis fuscus). Predators were exposed to either current-day CO2 levels or one of two elevated CO2 levels (~600 µatm or ~950 µatm) that may occur by 2100 according to climate change predictions. Exposure to elevated CO2 and reduced pH caused a shift from preference to avoidance of the smell of injured prey, with CO2treated predators spending approximately 20% less time in a water stream containing prey odour compared with controls. Furthermore, activity levels of fish was higher in the high CO2 treatment and feeding activity was lower for fish in the mid CO2treatment; indicating that future conditions may potentially reduce the ability of the fish to respond rapidly to fluctuations in food availability. Elevated activity levels of predators in the high CO2 treatment, however, may compensate for reduced olfactory ability, as greater movement facilitated visual detection of food. Our findings show that, at least for the species tested to date, both parties in the predator-prey relationship may be affected by ocean acidification. Although impairment of olfactory-mediated behaviour of predators might reduce the risk of predation for larval fishes, the magnitude of the observed effects of elevated CO2 acidification appear to be more dramatic for prey compared to predators. Thus, it is unlikely that the altered behaviour of predators is sufficient to fully compensate for the effects of ocean acidification on prey mortality.

Seawater carbonate chemistry and fish Amphiprion percula behaviour during experiments, 2012

Predicted future CO2 levels have been found to alter sensory responses and behaviour of marine fishes. Changes include increased boldness and activity, loss of behavioural lateralization, altered auditory preferences and impaired olfactory function. Impaired olfactory function makes larval fish attracted to odours they normally avoid, including ones from predators and unfavourable habitats. These behavioural alterations have significant effects on mortality that may have far-reaching implications for population replenishment, community structure and ecosystem function. However, the underlying mechanism linking high CO2 to these diverse responses has been unknown. Here we show that abnormal olfactory preferences and loss of behavioural lateralization exhibited by two species of larval coral reef fish exposed to high CO2 can be rapidly and effectively reversed by treatment with an antagonist of the GABA-A receptor. GABA-A is a major neurotransmitter receptor in the vertebrate brain. Thus, our results indicate that high CO2 interferes with neurotransmitter function, a hitherto unrecognized threat to marine populations and ecosystems. Given the ubiquity and conserved function of GABA-A receptors, we predict that rising CO2 levels could cause sensory and behavioural impairment in a wide range of marine species, especially those that tightly control their acid-base balance through regulatory changes in HCO3 and Cl levels.