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Energy acquisition strategy for reproduction in a semelparous squid

BACKGROUND: Energy demand for reproduction leads to a wide diversity of foraging and life-history strategy among wild animals, linking to a common objective to maximize reproductive success. Semelparous squid species in particular can use up to 50% of the total energy intake for reproduction. Howeve...

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Autores principales: Lin, Dongming, Zang, Na, Zhu, Kai, Li, Gang, Chen, Xinjun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9670511/
https://www.ncbi.nlm.nih.gov/pubmed/36384560
http://dx.doi.org/10.1186/s12983-022-00473-w
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author Lin, Dongming
Zang, Na
Zhu, Kai
Li, Gang
Chen, Xinjun
author_facet Lin, Dongming
Zang, Na
Zhu, Kai
Li, Gang
Chen, Xinjun
author_sort Lin, Dongming
collection PubMed
description BACKGROUND: Energy demand for reproduction leads to a wide diversity of foraging and life-history strategy among wild animals, linking to a common objective to maximize reproductive success. Semelparous squid species in particular can use up to 50% of the total energy intake for reproduction. However, the energy acquisition strategy for reproduction is still a controversial issue regarding whether the squid shift in diet ontogenetically. Here we used Argentinean shortfin squid (Illex argentinus) as a case study to investigate the strategy of energy acquisition for reproduction, by analyzing energy density of the squid’s reproductive tissues including ovary, nidamental glands and oviduct eggs, and stable isotopes and fatty acids of the squid’s ovary. RESULTS: The reproductive energy (the sum of the energy accumulated in ovary, nidamental glands and oviduct eggs) increased significantly with maturation. The ovary nitrogen stable isotopes (δ(15)N) showed a significant increase with maturation, but the increase by maturity stage was not equal to the typical enrichment of about 3‰ per trophic level. Isotopic niche width showed an increasing trend with maturation, and isotopic niche space exhibited greater overlap at advanced maturity stages. The relative amounts of 16:0, 20:5n3 and 20:4n6 in the ovary, tracing for carnivores and top predators, increased after the onset of maturation. The overall fatty acid profiles of the ovary showed significant differences among maturity stages, but obvious overlaps were found for mature squids. Mixed-effects model results revealed that reproductive energy was positively correlated with δ(15)N values. The reproductive energy was also positively related to the relative amounts of 18:0 and 20:4n6, respectively tracing for herbivores and top predators. CONCLUSIONS: Our results validate that the squid shifts to feed on higher trophic prey for reproduction as energy demand increases once maturation commences. However, the squid does not shift feeding habits at a trophic level but instead broadens prey spectrum, coupled with increasing intake of higher trophic prey items, to meet the energy demand for reproduction. Such energy acquisition strategy may be selected by the squid to maximize reproductive success by balancing energy intake and expenditure from foraging, warranting future studies that aim to clarify such strategy for reproduction among semelparous species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12983-022-00473-w.
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spelling pubmed-96705112022-11-18 Energy acquisition strategy for reproduction in a semelparous squid Lin, Dongming Zang, Na Zhu, Kai Li, Gang Chen, Xinjun Front Zool Research BACKGROUND: Energy demand for reproduction leads to a wide diversity of foraging and life-history strategy among wild animals, linking to a common objective to maximize reproductive success. Semelparous squid species in particular can use up to 50% of the total energy intake for reproduction. However, the energy acquisition strategy for reproduction is still a controversial issue regarding whether the squid shift in diet ontogenetically. Here we used Argentinean shortfin squid (Illex argentinus) as a case study to investigate the strategy of energy acquisition for reproduction, by analyzing energy density of the squid’s reproductive tissues including ovary, nidamental glands and oviduct eggs, and stable isotopes and fatty acids of the squid’s ovary. RESULTS: The reproductive energy (the sum of the energy accumulated in ovary, nidamental glands and oviduct eggs) increased significantly with maturation. The ovary nitrogen stable isotopes (δ(15)N) showed a significant increase with maturation, but the increase by maturity stage was not equal to the typical enrichment of about 3‰ per trophic level. Isotopic niche width showed an increasing trend with maturation, and isotopic niche space exhibited greater overlap at advanced maturity stages. The relative amounts of 16:0, 20:5n3 and 20:4n6 in the ovary, tracing for carnivores and top predators, increased after the onset of maturation. The overall fatty acid profiles of the ovary showed significant differences among maturity stages, but obvious overlaps were found for mature squids. Mixed-effects model results revealed that reproductive energy was positively correlated with δ(15)N values. The reproductive energy was also positively related to the relative amounts of 18:0 and 20:4n6, respectively tracing for herbivores and top predators. CONCLUSIONS: Our results validate that the squid shifts to feed on higher trophic prey for reproduction as energy demand increases once maturation commences. However, the squid does not shift feeding habits at a trophic level but instead broadens prey spectrum, coupled with increasing intake of higher trophic prey items, to meet the energy demand for reproduction. Such energy acquisition strategy may be selected by the squid to maximize reproductive success by balancing energy intake and expenditure from foraging, warranting future studies that aim to clarify such strategy for reproduction among semelparous species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12983-022-00473-w. BioMed Central 2022-11-16 /pmc/articles/PMC9670511/ /pubmed/36384560 http://dx.doi.org/10.1186/s12983-022-00473-w Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Lin, Dongming
Zang, Na
Zhu, Kai
Li, Gang
Chen, Xinjun
Energy acquisition strategy for reproduction in a semelparous squid
title Energy acquisition strategy for reproduction in a semelparous squid
title_full Energy acquisition strategy for reproduction in a semelparous squid
title_fullStr Energy acquisition strategy for reproduction in a semelparous squid
title_full_unstemmed Energy acquisition strategy for reproduction in a semelparous squid
title_short Energy acquisition strategy for reproduction in a semelparous squid
title_sort energy acquisition strategy for reproduction in a semelparous squid
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9670511/
https://www.ncbi.nlm.nih.gov/pubmed/36384560
http://dx.doi.org/10.1186/s12983-022-00473-w
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