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Integr Comp Biol. 2018 Dec 1;58(6):1064-1085. doi: 10.1093/icb/icy108.

Patterns of Fish Reproduction at the Interface between Air and Water.

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Organization for Marine Science and Technology, Nagasaki University, 1551-7 Tairamachi, Nagasaki 851-2213, Japan.
Graduate School of Fisheries and Environmental Sciences, Nagasaki University, 1-14 Bunkyomachi, Nagasaki 851-8521, Japan.
Department of Biology, Natural Science Division, Pepperdine University, 24255 Pacific Coast Highway, Malibu, CA 90263-4321, USA.


Although fishes by nature are aquatic, many species reproduce in such a way that their embryos are exposed to air either occasionally or constantly during incubation. We examine the ecological context and review specific examples of reproduction by fishes at the air-water interface, including fishes that do and do not breathe air. Four modes of reproduction at the air-water interface are described across 18 teleost orders, from fresh water, estuaries, and sea water. Mode 1, the most common type of reproduction by fishes at the air-water interface, includes 21 families of mostly marine teleosts that spawn in water onto a substrate surface, on vegetation, or into hollow objects such as shells that will later be continuously or occasionally exposed to air. Although the eggs are emerged into air, many of these species do not emerge into air as adults, and only about half of them breathe air. Mode 2 involves six families of freshwater fishes setting up and guarding a nest and guarding on the water surface, either with bubbles or in vegetation. Most of these species breathe air. In Mode 3, annual killifishes in at least two families in seasonally dry habitats bury eggs in mud in temporary pools, then die before the next generation emerges. These species neither guard nests nor breathe air. Mudskippers (Gobiidae) breathe air and use Mode 4, excavating burrows in a soft substrate and then storing air in a subterranean chamber. In a variation of Mode 4, eggs are placed on bubbles within a nesting burrow by swamp eels (Synbranchidae). No fishes from basal taxa are known to place their embryos where they will be exposed to air, although most of these species breathe air as adults. The widespread but still rare, diverse forms of fish reproduction at the air-water interface across a broad taxonomic spectrum suggest repeated independent evolutionary events and strong selection pressure for adult fishes to protect their embryos from hypoxic waters, aquatic predators, pathogens, and UV radiation. Air-breathing by adult fishes appears to be de-coupled from air exposure of developing embryos or aerial emersion of adults during spawning.


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