Stressed tadpoles mount more efficient glucocorticoid negative feedback in anthropogenic habitats due to phenotypic plasticity

Coping with anthropogenic environmental change is among the greatest challenges faced by wildlife, and endocrine flexibility is a potentially crucial coping mechanism. Animals may adapt to anthropogenic environments by dampening their glucocorticoid stress response, but empirical tests of this hypot...

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Autores: Bókony, Veronika, Ujhegyi, Nikolett, Hamow, Kamirán Á., Bosch, Jaime, Thumsová, Barbora, Vörös, Judit, Aspbury, Andrea S., Gabor, Caitlin R.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2021
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/226183
Acceso en línea:http://hdl.handle.net/10261/226183
Access Level:acceso abierto
Palabra clave:Amphibian stress physiology
Human-induced environmental change
Carbamazepine
Corticoid-disrupting contaminants
Batrachochytrium dendrobatidis
Ranavirus
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spelling Stressed tadpoles mount more efficient glucocorticoid negative feedback in anthropogenic habitats due to phenotypic plasticityBókony, VeronikaUjhegyi, NikolettHamow, Kamirán Á.Bosch, JaimeThumsová, BarboraVörös, JuditAspbury, Andrea S.Gabor, Caitlin R.Amphibian stress physiologyHuman-induced environmental changeCarbamazepineCorticoid-disrupting contaminantsBatrachochytrium dendrobatidisRanavirusCoping with anthropogenic environmental change is among the greatest challenges faced by wildlife, and endocrine flexibility is a potentially crucial coping mechanism. Animals may adapt to anthropogenic environments by dampening their glucocorticoid stress response, but empirical tests of this hypothesis have provided mixed evidence. An alternative hypothesis is that a non-attenuated stress response and efficient negative feedback are favored in anthropogenic habitats. To test this idea, we non-invasively sampled corticosterone release rates of common toad (Bufo bufo) tadpoles in agricultural, urban, and natural habitats, and quantified their stress response and negative feedback by a standardized stress-and-recovery protocol. We repeated the same sampling with tadpoles raised from eggs from the same ponds in a common-garden experiment to infer if the differences observed between populations in different habitats were due to individual phenotypic plasticity rather than microevolution or transgenerational effects. We found that, compared to tadpoles in natural ponds, urban tadpoles had higher baseline and stressed corticosterone release rates, and tadpoles in agricultural ponds had similar corticosterone release rates but greater stress-induced change, indicating stronger stress responses in both types of anthropogenic habitats. As predicted, tadpoles in both agricultural and urban ponds showed more efficient negative feedback than did tadpoles in natural ponds. Water pollution levels, as indicated by the concentrations of carbamazepine and corticoid-disrupting compounds in pond water, contributed to elevating the stress response regardless of land use. Infection by neither Batrachochytrium dendrobatidis nor Ranavirus was detected in free-living tadpoles. No habitat-related glucocorticoid differences persisted in the common-garden experiment. These results suggest that toad tadpoles in anthropogenic habitats increased their glucocorticoid flexibility via phenotypic plasticity. The coupling of stronger stress response and stronger negative feedback in these habitats supports the importance of rapidly “turning on and off” the stress response as a mechanism for coping with anthropogenic environmental change.The study was supported by a Fulbright Research Grant to CRG, and by the NRDI Fund of the National Research, Development and Innovation Office of Hungary (grants "OTKA"-115402 and 2019-2.1.11-TÉT2019-00026 to VB). GINOP-2.3.3-15-2016-00018 supported the UPLCMS/MS analysis.ElsevierNational Research, Development and Innovation Office (Hungary)Fulbright CommissionConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2021202120212021info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/226183reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Ingléshttp://dx.doi.org/10.1016/j.scitotenv.2020.141896Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2261832026-05-22T06:33:51Z
dc.title.none.fl_str_mv Stressed tadpoles mount more efficient glucocorticoid negative feedback in anthropogenic habitats due to phenotypic plasticity
title Stressed tadpoles mount more efficient glucocorticoid negative feedback in anthropogenic habitats due to phenotypic plasticity
spellingShingle Stressed tadpoles mount more efficient glucocorticoid negative feedback in anthropogenic habitats due to phenotypic plasticity
Bókony, Veronika
Amphibian stress physiology
Human-induced environmental change
Carbamazepine
Corticoid-disrupting contaminants
Batrachochytrium dendrobatidis
Ranavirus
title_short Stressed tadpoles mount more efficient glucocorticoid negative feedback in anthropogenic habitats due to phenotypic plasticity
title_full Stressed tadpoles mount more efficient glucocorticoid negative feedback in anthropogenic habitats due to phenotypic plasticity
title_fullStr Stressed tadpoles mount more efficient glucocorticoid negative feedback in anthropogenic habitats due to phenotypic plasticity
title_full_unstemmed Stressed tadpoles mount more efficient glucocorticoid negative feedback in anthropogenic habitats due to phenotypic plasticity
title_sort Stressed tadpoles mount more efficient glucocorticoid negative feedback in anthropogenic habitats due to phenotypic plasticity
dc.creator.none.fl_str_mv Bókony, Veronika
Ujhegyi, Nikolett
Hamow, Kamirán Á.
Bosch, Jaime
Thumsová, Barbora
Vörös, Judit
Aspbury, Andrea S.
Gabor, Caitlin R.
author Bókony, Veronika
author_facet Bókony, Veronika
Ujhegyi, Nikolett
Hamow, Kamirán Á.
Bosch, Jaime
Thumsová, Barbora
Vörös, Judit
Aspbury, Andrea S.
Gabor, Caitlin R.
author_role author
author2 Ujhegyi, Nikolett
Hamow, Kamirán Á.
Bosch, Jaime
Thumsová, Barbora
Vörös, Judit
Aspbury, Andrea S.
Gabor, Caitlin R.
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv National Research, Development and Innovation Office (Hungary)
Fulbright Commission
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Amphibian stress physiology
Human-induced environmental change
Carbamazepine
Corticoid-disrupting contaminants
Batrachochytrium dendrobatidis
Ranavirus
topic Amphibian stress physiology
Human-induced environmental change
Carbamazepine
Corticoid-disrupting contaminants
Batrachochytrium dendrobatidis
Ranavirus
description Coping with anthropogenic environmental change is among the greatest challenges faced by wildlife, and endocrine flexibility is a potentially crucial coping mechanism. Animals may adapt to anthropogenic environments by dampening their glucocorticoid stress response, but empirical tests of this hypothesis have provided mixed evidence. An alternative hypothesis is that a non-attenuated stress response and efficient negative feedback are favored in anthropogenic habitats. To test this idea, we non-invasively sampled corticosterone release rates of common toad (Bufo bufo) tadpoles in agricultural, urban, and natural habitats, and quantified their stress response and negative feedback by a standardized stress-and-recovery protocol. We repeated the same sampling with tadpoles raised from eggs from the same ponds in a common-garden experiment to infer if the differences observed between populations in different habitats were due to individual phenotypic plasticity rather than microevolution or transgenerational effects. We found that, compared to tadpoles in natural ponds, urban tadpoles had higher baseline and stressed corticosterone release rates, and tadpoles in agricultural ponds had similar corticosterone release rates but greater stress-induced change, indicating stronger stress responses in both types of anthropogenic habitats. As predicted, tadpoles in both agricultural and urban ponds showed more efficient negative feedback than did tadpoles in natural ponds. Water pollution levels, as indicated by the concentrations of carbamazepine and corticoid-disrupting compounds in pond water, contributed to elevating the stress response regardless of land use. Infection by neither Batrachochytrium dendrobatidis nor Ranavirus was detected in free-living tadpoles. No habitat-related glucocorticoid differences persisted in the common-garden experiment. These results suggest that toad tadpoles in anthropogenic habitats increased their glucocorticoid flexibility via phenotypic plasticity. The coupling of stronger stress response and stronger negative feedback in these habitats supports the importance of rapidly “turning on and off” the stress response as a mechanism for coping with anthropogenic environmental change.
publishDate 2021
dc.date.none.fl_str_mv 2021
2021
2021
2021
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/226183
url http://hdl.handle.net/10261/226183
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv http://dx.doi.org/10.1016/j.scitotenv.2020.141896
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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