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Under pressure—exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions

BACKGROUND: Life history theory predicts trade-offs between reproduction and survival in species like the northern gannet (Morus bassanus). During breeding, demanding foraging conditions lead them to expand their foraging range and diversify their diet, increasing the risk of reproductive failure. C...

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Autores principales: Pelletier, David, Blier, Pierre U., Vézina, François, Dufresne, France, Paquin, Frédérique, Christen, Felix, Guillemette, Magella
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10695113/
http://dx.doi.org/10.7717/peerj.16457
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author Pelletier, David
Blier, Pierre U.
Vézina, François
Dufresne, France
Paquin, Frédérique
Christen, Felix
Guillemette, Magella
author_facet Pelletier, David
Blier, Pierre U.
Vézina, François
Dufresne, France
Paquin, Frédérique
Christen, Felix
Guillemette, Magella
author_sort Pelletier, David
collection PubMed
description BACKGROUND: Life history theory predicts trade-offs between reproduction and survival in species like the northern gannet (Morus bassanus). During breeding, demanding foraging conditions lead them to expand their foraging range and diversify their diet, increasing the risk of reproductive failure. Changing partners may enhance breeding success but lead to more physiological costs. METHODS: To investigate the physiological costs of reproduction upon partner changes, we measured and compared 21 biomarkers related to telomere dynamics, oxidative stress, inflammation, hematology, nutritional status, and muscle damage. We used a longitudinal approach with gannets (n = 38) over three contrasting years (2017, 2018 and 2019). RESULTS: Our results suggest that annual breeding conditions exert a greater influence on physiological changes than partnership status. Individuals that changed partner experienced greater short-term stress than retained partners. This transient increase in stress was marked by short-term increases in oxidative lipid damage, lower antioxidant capacity, signs of inflammation, and greater weight loss than individuals that retained partners. During favorable conditions, individuals that changed mates had stabilized telomere length, decreased antioxidant capacity, glucose concentration, and muscle damage, along with increased oxygen transport capacity. Conversely, unfavorable breeding conditions led to increased telomere attrition, stabilized antioxidant capacity, decreased inflammation susceptibility, diminished oxygen transport capacity, and increased muscle damage. In the cases where partners were retained, distinct physiological changes were observed depending on the year’s conditions, yet the telomere dynamics remained consistent across both partnership status categories. During the favorable year, there was an increase in unsaturated fatty acids and oxygen transport capacity in the blood, coupled with a reduction in inflammation potential and protein catabolism. In contrast, during the unfavorable year in the retained mates, we observed an increase in oxidative DNA damage, antioxidant capacity, weight loss, but a decrease in inflammation susceptibility as observed in changed mates. DISCUSSION: Our study shows that behavioral flexibility such as mate switching can help seabirds cope with the challenges of food scarcity during reproduction, but these coping strategies may have a negative impact on physiological status at the individual level. In addition, the marked reduction in telomere length observed during harsh conditions, coupled with the stabilization of telomere length in favorable conditions, highlights the long-term physiological impact of annual breeding conditions on seabirds. These findings underscore the effect on their potential survival and fitness, emphasizing that the influence of annual breeding conditions is greater than that of partnership status.
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spelling pubmed-106951132023-12-05 Under pressure—exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions Pelletier, David Blier, Pierre U. Vézina, François Dufresne, France Paquin, Frédérique Christen, Felix Guillemette, Magella PeerJ Animal Behavior BACKGROUND: Life history theory predicts trade-offs between reproduction and survival in species like the northern gannet (Morus bassanus). During breeding, demanding foraging conditions lead them to expand their foraging range and diversify their diet, increasing the risk of reproductive failure. Changing partners may enhance breeding success but lead to more physiological costs. METHODS: To investigate the physiological costs of reproduction upon partner changes, we measured and compared 21 biomarkers related to telomere dynamics, oxidative stress, inflammation, hematology, nutritional status, and muscle damage. We used a longitudinal approach with gannets (n = 38) over three contrasting years (2017, 2018 and 2019). RESULTS: Our results suggest that annual breeding conditions exert a greater influence on physiological changes than partnership status. Individuals that changed partner experienced greater short-term stress than retained partners. This transient increase in stress was marked by short-term increases in oxidative lipid damage, lower antioxidant capacity, signs of inflammation, and greater weight loss than individuals that retained partners. During favorable conditions, individuals that changed mates had stabilized telomere length, decreased antioxidant capacity, glucose concentration, and muscle damage, along with increased oxygen transport capacity. Conversely, unfavorable breeding conditions led to increased telomere attrition, stabilized antioxidant capacity, decreased inflammation susceptibility, diminished oxygen transport capacity, and increased muscle damage. In the cases where partners were retained, distinct physiological changes were observed depending on the year’s conditions, yet the telomere dynamics remained consistent across both partnership status categories. During the favorable year, there was an increase in unsaturated fatty acids and oxygen transport capacity in the blood, coupled with a reduction in inflammation potential and protein catabolism. In contrast, during the unfavorable year in the retained mates, we observed an increase in oxidative DNA damage, antioxidant capacity, weight loss, but a decrease in inflammation susceptibility as observed in changed mates. DISCUSSION: Our study shows that behavioral flexibility such as mate switching can help seabirds cope with the challenges of food scarcity during reproduction, but these coping strategies may have a negative impact on physiological status at the individual level. In addition, the marked reduction in telomere length observed during harsh conditions, coupled with the stabilization of telomere length in favorable conditions, highlights the long-term physiological impact of annual breeding conditions on seabirds. These findings underscore the effect on their potential survival and fitness, emphasizing that the influence of annual breeding conditions is greater than that of partnership status. PeerJ Inc. 2023-12-01 /pmc/articles/PMC10695113/ http://dx.doi.org/10.7717/peerj.16457 Text en ©2023 Pelletier 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, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Animal Behavior
Pelletier, David
Blier, Pierre U.
Vézina, François
Dufresne, France
Paquin, Frédérique
Christen, Felix
Guillemette, Magella
Under pressure—exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions
title Under pressure—exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions
title_full Under pressure—exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions
title_fullStr Under pressure—exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions
title_full_unstemmed Under pressure—exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions
title_short Under pressure—exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions
title_sort under pressure—exploring partner changes, physiological responses and telomere dynamics in northern gannets across varying breeding conditions
topic Animal Behavior
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10695113/
http://dx.doi.org/10.7717/peerj.16457
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