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Relationship between reproductive hormones and migration distance in a polygynous songbird, the Red-winged Blackbird (Agelaius phoeniceus)

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Abstract

Many bird species migrate to southern overwintering locations to avoid harsh conditions at their breeding grounds, but at the cost of an energetically demanding migration that may delay their spring reproductive development. Previous work on the relationship between migration distance and reproductive readiness has primarily focused on early season baseline testosterone in both males and females. However, for females, testosterone alone may not be the appropriate measurement of reproductive development. Estradiol, a metabolite of testosterone that is essential for breeding behaviors and reproduction, should also be measured. Furthermore, baseline testosterone varies throughout the day and may change due to social interactions that occurred prior to sampling. Injection of gonadotropin-releasing hormone (GnRH) elicits an individual’s maximum potential testosterone production, minimizing daily and social variation. We explored relationships between migration distance and reproductive status after arrival to the breeding ground in Red-winged Blackbirds (Agelaius phoeniceus). We predicted that individuals that travel a shorter distance will have higher levels of reproductive hormones upon arrival given they are able to invest less in migration and more in reproduction. This is important because individuals that breed earlier often have higher reproductive success. In females, we measured baseline estradiol and testosterone. In males, we assessed baseline and GnRH-induced testosterone. Hormone values were related to migration distance, estimated by stable isotope analysis of claw samples collected before breeding began in eastern North Dakota. We found that males with shorter inferred migration distances have higher baseline testosterone upon arrival. However, inferred migration distance was not correlated with GnRH-induced testosterone. Female inferred migration distance was not correlated with baseline testosterone, but it was correlated with baseline estradiol. Females with higher testosterone had lower estradiol, suggesting that testosterone in females is not a reliable indicator of estradiol levels, thus readiness to breed. Our observations suggest that baseline hormone levels were related to migration distance, but baseline testosterone alone may not provide a complete assessment of a male or female’s preparedness to breed following spring migration.

Zusammenfassung

Beziehung zwischen Fortpflanzungshormonen und Zugstrecke bei einem polygynen Singvogel, dem Rotflügelstärling (Agelaius phoeniceus).

Viele Vogelarten ziehen in südliche Überwinterungsgebiete, um den rauhen Bedingungen in ihren Brutgebieten zu entgehen, allerdings um den Preis eines energieaufwendigen Zuges, der ihre Fortpflanzung im Frühjahr verzögern kann. Frühere Arbeiten über den Zusammenhang zwischen Zugstrecke und Fortpflanzungsbereitschaft konzentrierten sich in erster Linie auf den Testosteron-Basiswert von Männchen und Weibchen zu Beginn der Saison. Aber bei Weibchen ist Testosteron allein möglicherweise nicht das geeignete Maß für die Entwicklung der Fortpflanzung. Östradiol, ein Testosteron-Metabolit, der für das Brutverhalten und die Fortpflanzung wichtig ist, sollte ebenfalls gemessen werden. Außerdem schwankt der Testosteron-Basiswert im Laufe des Tages und kann sich aufgrund von sozialen Interaktionen kurz vor der Probenentnahme ändern. Durch die Injektion von Gonadotropin-Releasing-Hormon (GnRH) wird die für ein Einzeltier maximal mögliche Testosteronproduktion ausgelöst, wobei die täglichen und sozialen Schwankungen minimiert werden. Wir untersuchten den Zusammenhang zwischen der Zugstrecke und dem Fortpflanzungsstatus vom Rotflügelstärling (Agelaius phoeniceus) nach der Ankunft im Brutgebiet und sagten voraus, dass Individuen, die eine kürzere Strecke zurücklegen, bei ihrer Ankunft einen höheren Gehalt an Fortpflanzungshormonen aufweisen, da sie weniger in den Zug und mehr in die Fortpflanzung investieren können. Dies ist deshalb wichtig, weil Tiere, die sich früher fortpflanzen, oft einen höheren Fortpflanzungserfolg haben. Bei den Weibchen bestimmten wir den Basiswert von Östradiol und Testosteron, bei den Männchen den Basiswert und das GnRH-induzierte Testosteron. Die Hormonwerte wurden zur Zugstrecke in Relation gesetzt, die anhand der Analyse stabiler Isotope von Krallenproben, gesammelt vor dem Brutbeginn im östlichen North Dakota, geschätzt wurde. Wir stellen fest, dass der Basiswert des Testosterons bei Männchen mit kürzeren Zugstrecken bei der Ankunft auf einem höheren Niveau lag. Aber die ermittelte Zugstrecke korrelierte nicht mit dem GnRH-induzierten Testosteron. Bei den Weibchen korrelierte die Zugstrecke nicht mit dem Testosteron-Basiswert, wohl aber mit dem Basiswert des Östradiols. Weibchen mit einem höheren Testosteronspiegel wiesen einen niedrigeren Östradiolspiegel auf, was darauf hindeutet, dass Testosteron bei weiblichen Tieren kein zuverlässiger Indikator für den Östradiolspiegel und damit für die Bereitschaft zur Fortpflanzung ist. Unsere Ergebnisse deuten darauf hin, dass die Hormon-Basiswerte mit der Zugstrecke zusammenhängen, der Testosteron-Basiswert allein aber vermutlich keinen vollständigen Aufschluss über die Brutbereitschaft eines Männchens oder Weibchens direkt nach dem Frühjahrszug gibt.

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Acknowledgements

We would like to thank S. Grillo, B. Weber, M. Cremers, and K. Adkins for getting up at 4:00 am and spending countless hours in the wetlands of North Dakota chasing blackbirds. We are also grateful for the members of ‘Team Bird’ at NDSU. They have been there for technical and emotion support throughout this project. Drs. S. DeKeyser and G. Linz provided invaluable feedback during the planning of this study. We owe thanks to K. Tompkins and T. Gwilliams at the U.S. Fish and Wildlife Service in Valley City for allowing us to work at the Alice Waterfowl Production Area.

Funding

Funding for this project was provided by the Biological Sciences Department at North Dakota State University and the United States Department of Agriculture (USDA), Animal and Plant Health Inspection Service (APHIS), Wildlife Services (WS), and National Wildlife Research Center.

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ME, TG, and PK contributed to the experimental design and data analysis. ME, EM-V, and TG conducted the field work. BW analyzed stable isotopes in claw samples. All authors contributed to the writing of this manuscript.

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Correspondence to Page E. Klug.

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The data collected on this project was approved by the North Dakota State University Institutional Animal Care and Use Committee, North Dakota Game and Fish Department, the United States Geological Survey Bird Banding Laboratory, the US Fish and Wildlife Service in Valley City, and the USDA-APHIS-WS NWRC. Experiments comply with the current laws of the country in which they were performed.

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Eshleman, M.A., Klug, P.E., Morales-Vega, E. et al. Relationship between reproductive hormones and migration distance in a polygynous songbird, the Red-winged Blackbird (Agelaius phoeniceus). J Ornithol 163, 425–436 (2022). https://doi.org/10.1007/s10336-021-01940-7

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