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Ontogenetic transitions, biomechanical trade-offs and macroevolution of scyphozoan medusae swimming patterns

Ephyrae, the early stages of scyphozoan jellyfish, possess a conserved morphology among species. However, ontogenetic transitions lead to morphologically different shapes among scyphozoan lineages, with important consequences for swimming biomechanics, bioenergetics and ecology. We used high-speed i...

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Autores principales: von Montfort, Guilherme M., Costello, John H., Colin, Sean P., Morandini, André C., Migotto, Alvaro E., Maronna, Maximiliano M., Reginato, Marcelo, Miyake, Hiroshi, Nagata, Renato M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10276012/
https://www.ncbi.nlm.nih.gov/pubmed/37328506
http://dx.doi.org/10.1038/s41598-023-34927-w
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author von Montfort, Guilherme M.
Costello, John H.
Colin, Sean P.
Morandini, André C.
Migotto, Alvaro E.
Maronna, Maximiliano M.
Reginato, Marcelo
Miyake, Hiroshi
Nagata, Renato M.
author_facet von Montfort, Guilherme M.
Costello, John H.
Colin, Sean P.
Morandini, André C.
Migotto, Alvaro E.
Maronna, Maximiliano M.
Reginato, Marcelo
Miyake, Hiroshi
Nagata, Renato M.
author_sort von Montfort, Guilherme M.
collection PubMed
description Ephyrae, the early stages of scyphozoan jellyfish, possess a conserved morphology among species. However, ontogenetic transitions lead to morphologically different shapes among scyphozoan lineages, with important consequences for swimming biomechanics, bioenergetics and ecology. We used high-speed imaging to analyse biomechanical and kinematic variables of swimming in 17 species of Scyphozoa (1 Coronatae, 8 “Semaeostomeae” and 8 Rhizostomeae) at different developmental stages. Swimming kinematics of early ephyrae were similar, in general, but differences related to major lineages emerged through development. Rhizostomeae medusae have more prolate bells, shorter pulse cycles and higher swimming performances. Medusae of “Semaeostomeae”, in turn, have more variable bell shapes and most species had lower swimming performances. Despite these differences, both groups travelled the same distance per pulse suggesting that each pulse is hydrodynamically similar. Therefore, higher swimming velocities are achieved in species with higher pulsation frequencies. Our results suggest that medusae of Rhizostomeae and “Semaeostomeae” have evolved bell kinematics with different optimized traits, rhizostomes optimize rapid fluid processing, through faster pulsations, while “semaeostomes” optimize swimming efficiency, through longer interpulse intervals that enhance mechanisms of passive energy recapture.
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spelling pubmed-102760122023-06-18 Ontogenetic transitions, biomechanical trade-offs and macroevolution of scyphozoan medusae swimming patterns von Montfort, Guilherme M. Costello, John H. Colin, Sean P. Morandini, André C. Migotto, Alvaro E. Maronna, Maximiliano M. Reginato, Marcelo Miyake, Hiroshi Nagata, Renato M. Sci Rep Article Ephyrae, the early stages of scyphozoan jellyfish, possess a conserved morphology among species. However, ontogenetic transitions lead to morphologically different shapes among scyphozoan lineages, with important consequences for swimming biomechanics, bioenergetics and ecology. We used high-speed imaging to analyse biomechanical and kinematic variables of swimming in 17 species of Scyphozoa (1 Coronatae, 8 “Semaeostomeae” and 8 Rhizostomeae) at different developmental stages. Swimming kinematics of early ephyrae were similar, in general, but differences related to major lineages emerged through development. Rhizostomeae medusae have more prolate bells, shorter pulse cycles and higher swimming performances. Medusae of “Semaeostomeae”, in turn, have more variable bell shapes and most species had lower swimming performances. Despite these differences, both groups travelled the same distance per pulse suggesting that each pulse is hydrodynamically similar. Therefore, higher swimming velocities are achieved in species with higher pulsation frequencies. Our results suggest that medusae of Rhizostomeae and “Semaeostomeae” have evolved bell kinematics with different optimized traits, rhizostomes optimize rapid fluid processing, through faster pulsations, while “semaeostomes” optimize swimming efficiency, through longer interpulse intervals that enhance mechanisms of passive energy recapture. Nature Publishing Group UK 2023-06-16 /pmc/articles/PMC10276012/ /pubmed/37328506 http://dx.doi.org/10.1038/s41598-023-34927-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
von Montfort, Guilherme M.
Costello, John H.
Colin, Sean P.
Morandini, André C.
Migotto, Alvaro E.
Maronna, Maximiliano M.
Reginato, Marcelo
Miyake, Hiroshi
Nagata, Renato M.
Ontogenetic transitions, biomechanical trade-offs and macroevolution of scyphozoan medusae swimming patterns
title Ontogenetic transitions, biomechanical trade-offs and macroevolution of scyphozoan medusae swimming patterns
title_full Ontogenetic transitions, biomechanical trade-offs and macroevolution of scyphozoan medusae swimming patterns
title_fullStr Ontogenetic transitions, biomechanical trade-offs and macroevolution of scyphozoan medusae swimming patterns
title_full_unstemmed Ontogenetic transitions, biomechanical trade-offs and macroevolution of scyphozoan medusae swimming patterns
title_short Ontogenetic transitions, biomechanical trade-offs and macroevolution of scyphozoan medusae swimming patterns
title_sort ontogenetic transitions, biomechanical trade-offs and macroevolution of scyphozoan medusae swimming patterns
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10276012/
https://www.ncbi.nlm.nih.gov/pubmed/37328506
http://dx.doi.org/10.1038/s41598-023-34927-w
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