Emersion behaviour underlies variation in gill morphology and aquatic respiratory function in the amphibious fish Kryptolebias marmoratus.

Fishes acclimated to hypoxic environments often increase gill surface area to improve O2 uptake. In some species, surface area is increased via reduction of an interlamellar cell mass (ILCM) that fills water channels between gill lamellae. Amphibious fishes, however, may not increase gill surface area in hypoxic water because these species can, instead, leave water and breathe air. To differentiate between these possibilities, we compared wild amphibious mangrove rivulus Kryptolebias marmoratus from two habitats that varied in O2 availability - a hypoxic freshwater pool versus nearly anoxic crab burrows. Fish captured from crab burrows had less gill surface area (as ILCMs were enlarged by ∼32%), increased rates of normoxic O2 consumption and increased critical O2 tension compared with fish from the freshwater pool. Thus, wild mangrove rivulus do not respond to near-anoxic water by decreasing metabolism or increasing O2 extraction. Instead, fish from the crab burrow habitat spent three times longer out of water, which probably caused the observed changes in gill morphology and respiratory phenotype. We also tested whether critical O2 tension is influenced by genetic heterozygosity, as K. marmoratus is one of only two hermaphroditic vertebrate species that can produce both self-fertilized (inbred) or out-crossed (more heterozygous) offspring. We found no evidence for inbreeding depression, suggesting that self-fertilization does not impair respiratory function. Overall, our results demonstrate that amphibious fishes that inhabit hypoxic aquatic habitats can use a fundamentally different strategy from that used by fully aquatic water-breathing fishes, relying on escape behaviour rather than metabolic depression or increased O2 extraction ability.

Evolution, ecology and physiology of amphibious killifishes (Cyprinodontiformes).

The order Cyprinodontiformes contains an exceptional diversity of amphibious taxa, including at least 34 species from six families. These cyprinodontiforms often inhabit intertidal or ephemeral habitats characterized by low dissolved oxygen or otherwise poor water quality, conditions that have been hypothesized to drive the evolution of terrestriality. Most of the amphibious species are found in the Rivulidae, Nothobranchiidae and Fundulidae. It is currently unclear whether the pattern of amphibiousness observed in the Cyprinodontiformes is the result of repeated, independent evolutions, or stems from an amphibious common ancestor. Amphibious cyprinodontiforms leave water for a variety of reasons: some species emerse only briefly, to escape predation or capture prey, while others occupy ephemeral habitats by living for months at a time out of water. Fishes able to tolerate months of emersion must maintain respiratory gas exchange, nitrogen excretion and water and salt balance, but to date knowledge of the mechanisms that facilitate homeostasis on land is largely restricted to model species. This review synthesizes the available literature describing amphibious lifestyles in cyprinodontiforms, compares the behavioural and physiological strategies used to exploit the terrestrial environment and suggests directions and ideas for future research.