Invited review - the effects of anthropogenic abiotic stressors on the sensory systems of fishes.

Climate change is a growing global issue with many countries and institutions declaring a climate state of emergency. Excess CO2 from anthropogenic sources and changes in land use practices are contributing to many detrimental changes, including increased global temperatures, ocean acidification and hypoxic zones along coastal habitats. All senses are important for aquatic animals, as it is how they can perceive and respond to their environment. Some of these environmental challenges have been shown to impair their sensory systems, including the olfactory, visual, and auditory systems. While most of the research is focused on how ocean acidification affects olfaction, there is also evidence that it negatively affects vision and hearing. The effects that temperature and hypoxia have on the senses have also been investigated, but to a much lesser extent in comparison to ocean acidification. This review assembles the known information on how these anthropogenic challenges affect the sensory systems of fishes, but also highlights what gaps in knowledge remain with suggestions for immediate action. Olfaction, vision, otolith, pH, freshwater, seawater, marine, central nervous system, electrophysiology, mechanism.

Positive feedback promotes terrestrial emergence behaviour in an amphibious fish.

Major ecological transitions such as the invasion of land by aquatic vertebrates may be facilitated by positive feedback between habitat choice and phenotypic plasticity. We used the amphibious fish Kryptolebias marmoratus to test the hypothesis that aquatic hypoxia, emergence behaviour and respiratory plasticity create this type of positive feedback loop that causes fish to spend increasing amounts of time on land. Terrestrially acclimated fish were more sensitive to aquatic hypoxia (emergence at higher PO2) and were less hypoxia tolerant (shorter time to loss of equilibrium) relative to water-acclimated fish, which are necessary conditions for positive feedback. Next, we tested the prediction that exposure to aquatic hypoxia causes fish to emerge frequently, reduce gill surface area, and become less hypoxia tolerant. Indeed, fish exposed to severe aquatic hypoxia spent almost 50% of the time out of water and coverage of the gill lamellae by an inter-lamellar cell mass almost doubled. Fish exposed to aquatic hypoxia that could emerge from water were also more sensitive to subsequent acute aquatic hypoxia and were less hypoxia tolerant than normoxia-exposed controls. These results are opposite those of fish that cannot escape from aquatic hypoxia and presumably arise owing to plastic changes that occur during air exposure. Together, these results indicate that emergence behaviour begets further emergence behaviour, driven by gill remodelling which reduces aquatic respiratory function. This type of positive feedback may explain how amphibious behaviour has repeatedly evolved in fishes that occupy hypoxic aquatic habitats despite the associated challenges of life on land.

Changes in gill neuroepithelial cells and morphology of threespine stickleback (Gasterosteus aculeatus) to hypoxia and simulated ocean acidification.

Coastal marine environments are characterized by daily, seasonal and long-term changes in both O2 and CO2, driven by local biotic and abiotic factors. The neuroepithelial cells (NECs) of fish are thought to be the putative chemoreceptors for sensing oxygen and CO2, and, thus, NECs play a key role in detecting these environmental changes. However, the role of NECs as chemosensors in marine fish remains largely understudied. In this study, the NECs of marine threespine sticklebacks (Gasterosteus aculeatus) were characterized using immunohistochemistry. We then determined if there were changes in NEC size and density, and in gill morphology in response to either mild (10 kPa) or moderate (6.8 kPa) hypoxia and two levels of elevated CO2 (1,500 and 3,000 µatm). We found that the NECs of stickleback contained synaptic vesicles and were innervated, and were 50-300% larger and 2 to 4 times more abundant than in other similar sized freshwater fishes. NEC size and density were largely unaffected by exposure to hypoxia, but there was a 50% decrease in interlamellar cell mass (ILCM) in response to mild and moderate hypoxia. NECs increased in size, but not abundance in response to elevated CO2. Moreover, fish exposed to moderate or elevated CO2 had 53-78% larger ILCMs compared to control fish. Our results demonstrated that adult marine sticklebacks have NECs that can respond to environmentally relevant pCO2 and likely hypoxia, which highlights the importance of NECs in marine fishes under the heterogeneity of environmental conditions in coastal areas.