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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’. However,...

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Detalles Bibliográficos
Autores principales: Katayama, Yukitoshi, Tsukada, Takehiro, Hyodo, Susumu, Sakamoto, Hirotaka, Sakamoto, Tatsuya
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9728915/
https://www.ncbi.nlm.nih.gov/pubmed/36477197
http://dx.doi.org/10.1371/journal.pone.0277968
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author Katayama, Yukitoshi
Tsukada, Takehiro
Hyodo, Susumu
Sakamoto, Hirotaka
Sakamoto, Tatsuya
author_facet Katayama, Yukitoshi
Tsukada, Takehiro
Hyodo, Susumu
Sakamoto, Hirotaka
Sakamoto, Tatsuya
author_sort Katayama, Yukitoshi
collection PubMed
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 pubmed-97289152022-12-08 Behavioural osmoregulation during land invasion in fish: Prandial drinking and wetting of the dry skin Katayama, Yukitoshi Tsukada, Takehiro Hyodo, Susumu Sakamoto, Hirotaka Sakamoto, Tatsuya PLoS One Research Article 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. Public Library of Science 2022-12-07 /pmc/articles/PMC9728915/ /pubmed/36477197 http://dx.doi.org/10.1371/journal.pone.0277968 Text en © 2022 Katayama et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Katayama, Yukitoshi
Tsukada, Takehiro
Hyodo, Susumu
Sakamoto, Hirotaka
Sakamoto, Tatsuya
Behavioural osmoregulation during land invasion in fish: Prandial drinking and wetting of the dry skin
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
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9728915/
https://www.ncbi.nlm.nih.gov/pubmed/36477197
http://dx.doi.org/10.1371/journal.pone.0277968
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