Behavioural osmoregulation during land invasion in fish: Prandial drinking and wetting of the dry skin

PLoS One. 2022 Dec 7;17(12):e0277968. doi: 10.1371/journal.pone.0277968. eCollection 2022.

Abstract

Osmoregulatory behaviours should have evolutionarily modified for terrestrialisation of vertebrates. In mammals, sensations of buccal food and drying have immediate effects on postprandial thirst to prevent future systemic dehydration, and is thereby considered to be 'anticipatory thirst'. However, it remains unclear whether such an anticipatory response has been acquired in the non-tetrapod lineage. Using the mudskipper goby (Periophthalmus modestus) as a semi-terrestrial ray-finned fish, we herein investigated postprandial drinking and other unique features like full-body 'rolling' over on the back although these behaviours had not been considered to have osmoregulatory functions. In our observations on tidal flats, mudskippers migrated into water areas within a minute after terrestrial eating, and exhibited rolling behaviour with accompanying pectoral-fin movements. In aquarium experiments, frequency of migration into a water area for drinking increased within a few minutes after eating onset, without systemic dehydration. During their low humidity exposure, frequency of the rolling behaviour and pectoral-fin movements increased by more than five times to moisten the skin before systemic dehydration. These findings suggest anticipatory responses which arise from oral/gastrointestinal and cutaneous sensation in the goby. These sensation and motivation seem to have evolved in distantly related species in order to solve osmoregulatory challenges during terrestrialisation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Water*

Substances

  • Water

Grants and funding

This work was supported by ‘JSPS KAKENHI’ Japan Society for the Promotion of Science (JSPS) KAKENHI Grant Number JP 16J01114 and 20K15604 to Y. K. [URL]https://www.jsps.go.jp/english/index.html The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.