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

• Published in: PloS one Vol. 17; no. 12; p. e0277968
• Main Authors: Katayama, Yukitoshi, Tsukada, Takehiro, Hyodo, Susumu, Sakamoto, Hirotaka, Sakamoto, Tatsuya
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 07.12.2022; Public Library of Science (PLoS)
• Subjects: Adaptation (Physiology); Behavior; Biological research; Biology and Life Sciences; Biology, Experimental; Dehydration; Drinking; Drinking water; Drying; Earth Sciences; Eating; Experiments; Fish; Flats (landforms); Gender differences; Hormones; Humidity; Land area; Low humidity; Medicine and Health Sciences; Motivation; Osmoregulation; Physiology; Plasma; Seawater; Sensation; Sensory adaptation; Skin; Social Sciences; Thirst; Tidal flats; Vertebrates; Water; Water area; Water-electrolyte balance (Physiology); Wetting; Japan; Germany
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0277968

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.