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Hidden impacts of conservation management on fertility of the critically endangered kākāpō

BACKGROUND: Animal conservation often requires intensive management actions to improve reproductive output, yet any adverse effects of these may not be immediately apparent, particularly in threatened species with small populations and long lifespans. Hand-rearing is an example of a conservation man...

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Autores principales: Digby, Andrew, Eason, Daryl, Catalina, Alejandro, Lierz, Michael, Galla, Stephanie, Urban, Lara, Le Lec, Marissa F., Guhlin, Joseph, Steeves, Tammy E., Dearden, Peter K., Joustra, Tineke, Lees, Caroline, Davis, Tane, Vercoe, Deidre
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9901309/
https://www.ncbi.nlm.nih.gov/pubmed/36755872
http://dx.doi.org/10.7717/peerj.14675
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author Digby, Andrew
Eason, Daryl
Catalina, Alejandro
Lierz, Michael
Galla, Stephanie
Urban, Lara
Le Lec, Marissa F.
Guhlin, Joseph
Steeves, Tammy E.
Dearden, Peter K.
Joustra, Tineke
Lees, Caroline
Davis, Tane
Vercoe, Deidre
author_facet Digby, Andrew
Eason, Daryl
Catalina, Alejandro
Lierz, Michael
Galla, Stephanie
Urban, Lara
Le Lec, Marissa F.
Guhlin, Joseph
Steeves, Tammy E.
Dearden, Peter K.
Joustra, Tineke
Lees, Caroline
Davis, Tane
Vercoe, Deidre
author_sort Digby, Andrew
collection PubMed
description BACKGROUND: Animal conservation often requires intensive management actions to improve reproductive output, yet any adverse effects of these may not be immediately apparent, particularly in threatened species with small populations and long lifespans. Hand-rearing is an example of a conservation management strategy which, while boosting populations, can cause long-term demographic and behavioural problems. It is used in the recovery of the critically endangered kākāpō (Strigops habroptilus), a flightless parrot endemic to New Zealand, to improve the slow population growth that is due to infrequent breeding, low fertility and low hatching success. METHODS: We applied Bayesian mixed models to examine whether hand-rearing and other factors were associated with clutch fertility in kākāpō. We used projection predictive variable selection to compare the relative contributions to fertility from the parents’ rearing environment, their age and previous copulation experience, the parental kinship, and the number of mates and copulations for each clutch. We also explored how the incidence of repeated copulations and multiple mates varied with kākāpō density. RESULTS: The rearing status of the clutch father and the number of mates and copulations of the clutch mother were the dominant factors in predicting fertility. Clutches were less likely to be fertile if the father was hand-reared compared to wild-reared, but there was no similar effect for mothers. Clutches produced by females copulating with different males were more likely to be fertile than those from repeated copulations with one male, which in turn had a higher probability of fertility than those from a single copulation. The likelihood of multiple copulations and mates increased with female:male adult sex ratio, perhaps as a result of mate guarding by females. Parental kinship, copulation experience and age all had negligible associations with clutch fertility. CONCLUSIONS: These results provide a rare assessment of factors affecting fertility in a wild threatened bird species, with implications for conservation management. The increased fertility due to multiple mates and copulations, combined with the evidence for mate guarding and previous results of kākāpō sperm morphology, suggests that an evolutionary mechanism exists to optimise fertility through sperm competition in kākāpō. The high frequency of clutches produced from single copulations in the contemporary population may therefore represent an unnatural state, perhaps due to too few females. This suggests that opportunity for sperm competition should be maximised by increasing population densities, optimising sex ratios, and using artificial insemination. The lower fertility of hand-reared males may result from behavioural defects due to lack of exposure to conspecifics at critical development stages, as seen in other taxa. This potential negative impact of hand-rearing must be balanced against the short-term benefits it provides.
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spelling pubmed-99013092023-02-07 Hidden impacts of conservation management on fertility of the critically endangered kākāpō Digby, Andrew Eason, Daryl Catalina, Alejandro Lierz, Michael Galla, Stephanie Urban, Lara Le Lec, Marissa F. Guhlin, Joseph Steeves, Tammy E. Dearden, Peter K. Joustra, Tineke Lees, Caroline Davis, Tane Vercoe, Deidre PeerJ Animal Behavior BACKGROUND: Animal conservation often requires intensive management actions to improve reproductive output, yet any adverse effects of these may not be immediately apparent, particularly in threatened species with small populations and long lifespans. Hand-rearing is an example of a conservation management strategy which, while boosting populations, can cause long-term demographic and behavioural problems. It is used in the recovery of the critically endangered kākāpō (Strigops habroptilus), a flightless parrot endemic to New Zealand, to improve the slow population growth that is due to infrequent breeding, low fertility and low hatching success. METHODS: We applied Bayesian mixed models to examine whether hand-rearing and other factors were associated with clutch fertility in kākāpō. We used projection predictive variable selection to compare the relative contributions to fertility from the parents’ rearing environment, their age and previous copulation experience, the parental kinship, and the number of mates and copulations for each clutch. We also explored how the incidence of repeated copulations and multiple mates varied with kākāpō density. RESULTS: The rearing status of the clutch father and the number of mates and copulations of the clutch mother were the dominant factors in predicting fertility. Clutches were less likely to be fertile if the father was hand-reared compared to wild-reared, but there was no similar effect for mothers. Clutches produced by females copulating with different males were more likely to be fertile than those from repeated copulations with one male, which in turn had a higher probability of fertility than those from a single copulation. The likelihood of multiple copulations and mates increased with female:male adult sex ratio, perhaps as a result of mate guarding by females. Parental kinship, copulation experience and age all had negligible associations with clutch fertility. CONCLUSIONS: These results provide a rare assessment of factors affecting fertility in a wild threatened bird species, with implications for conservation management. The increased fertility due to multiple mates and copulations, combined with the evidence for mate guarding and previous results of kākāpō sperm morphology, suggests that an evolutionary mechanism exists to optimise fertility through sperm competition in kākāpō. The high frequency of clutches produced from single copulations in the contemporary population may therefore represent an unnatural state, perhaps due to too few females. This suggests that opportunity for sperm competition should be maximised by increasing population densities, optimising sex ratios, and using artificial insemination. The lower fertility of hand-reared males may result from behavioural defects due to lack of exposure to conspecifics at critical development stages, as seen in other taxa. This potential negative impact of hand-rearing must be balanced against the short-term benefits it provides. PeerJ Inc. 2023-02-03 /pmc/articles/PMC9901309/ /pubmed/36755872 http://dx.doi.org/10.7717/peerj.14675 Text en ©2023 Digby 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
Digby, Andrew
Eason, Daryl
Catalina, Alejandro
Lierz, Michael
Galla, Stephanie
Urban, Lara
Le Lec, Marissa F.
Guhlin, Joseph
Steeves, Tammy E.
Dearden, Peter K.
Joustra, Tineke
Lees, Caroline
Davis, Tane
Vercoe, Deidre
Hidden impacts of conservation management on fertility of the critically endangered kākāpō
title Hidden impacts of conservation management on fertility of the critically endangered kākāpō
title_full Hidden impacts of conservation management on fertility of the critically endangered kākāpō
title_fullStr Hidden impacts of conservation management on fertility of the critically endangered kākāpō
title_full_unstemmed Hidden impacts of conservation management on fertility of the critically endangered kākāpō
title_short Hidden impacts of conservation management on fertility of the critically endangered kākāpō
title_sort hidden impacts of conservation management on fertility of the critically endangered kākāpō
topic Animal Behavior
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9901309/
https://www.ncbi.nlm.nih.gov/pubmed/36755872
http://dx.doi.org/10.7717/peerj.14675
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