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

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'....

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Main Authors: Yukitoshi Katayama, Takehiro Tsukada, Susumu Hyodo, Hirotaka Sakamoto, Tatsuya Sakamoto
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0277968
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author Yukitoshi Katayama
Takehiro Tsukada
Susumu Hyodo
Hirotaka Sakamoto
Tatsuya Sakamoto
author_facet Yukitoshi Katayama
Takehiro Tsukada
Susumu Hyodo
Hirotaka Sakamoto
Tatsuya Sakamoto
author_sort Yukitoshi Katayama
collection DOAJ
description 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.
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spelling doaj.art-e1d547c1dc594e4c9f8ac727a76876292023-01-11T05:32:37ZengPublic Library of Science (PLoS)PLoS ONE1932-62032022-01-011712e027796810.1371/journal.pone.0277968Behavioural osmoregulation during land invasion in fish: Prandial drinking and wetting of the dry skin.Yukitoshi KatayamaTakehiro TsukadaSusumu HyodoHirotaka SakamotoTatsuya SakamotoOsmoregulatory 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.https://doi.org/10.1371/journal.pone.0277968
spellingShingle Yukitoshi Katayama
Takehiro Tsukada
Susumu Hyodo
Hirotaka Sakamoto
Tatsuya Sakamoto
Behavioural osmoregulation during land invasion in fish: Prandial drinking and wetting of the dry skin.
PLoS ONE
title Behavioural osmoregulation during land invasion in fish: Prandial drinking and wetting of the dry skin.
title_full Behavioural osmoregulation during land invasion in fish: Prandial drinking and wetting of the dry skin.
title_fullStr Behavioural osmoregulation during land invasion in fish: Prandial drinking and wetting of the dry skin.
title_full_unstemmed Behavioural osmoregulation during land invasion in fish: Prandial drinking and wetting of the dry skin.
title_short Behavioural osmoregulation during land invasion in fish: Prandial drinking and wetting of the dry skin.
title_sort behavioural osmoregulation during land invasion in fish prandial drinking and wetting of the dry skin
url https://doi.org/10.1371/journal.pone.0277968
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