Feather steroid hormone concentrations in relation to age, sex, and molting time in a long-distance migratory passerine

. 2019 Aug ; 9 (16) : 9018-9026. [epub] 20190723

Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31463000

In birds, concentrations of testosterone (T) and corticosterone (Cort) are closely connected with many morphological, behavioral, and other physiological traits, including reproduction, metabolism, immunity, and fitness. The direction of the effect of these hormones on above-mentioned traits, and the potential feedback between hormones are in general unclear; in addition, knowledge on how age and sex can affect T and Cort concentrations is still inconsistent. Our study used a novel method to analyze testosterone and corticosterone in feathers (Tf, Cortf) based on the precolumn chemical derivatization of hormones before liquid chromatography-tandem mass spectrometry (LC-MS/MS) analysis. Unlike previously used methods (RIA, EIA), our analytical procedure allows simultaneous analysis of both hormones from small amounts of feathers (4-25 mg) and, thus, overcomes the problem of insufficient detection limits. We applied this method to reveal associations between Tf and Cortf hormone concentrations and feather growth, age, and sex in feathers grown during the postbreeding (flanks) and prebreeding (tails) periods in barn swallows (Hirundo rustica). There was neither a correlation between prebreeding and postbreeding Tf, nor between prebreeding and postbreeding Cortf. Tail Cortf concentrations were negatively associated with tail feather growth rates. Feather hormone concentrations were correlated in the prebreeding period, negatively in males but positively in females. Both Cortf and Tf were higher in young birds compared to older ones, indicating either an age-related decrease in hormone concentrations within individuals, or the selective disappearance of individuals with high steroid concentrations. Males and females did not differ in Cortf, but Tf concentrations were higher in males than females, particularly during the prebreeding period. In this study, we provide an effective method for analyzing hormones in feathers in an ecological context, especially in situations when the total amount of feathers available for the analysis is limited.

Zobrazit více v PubMed

Adkins‐Regan, E. (2005). Hormones and animal social behavior. Princeton, NJ: Princeton University Press.

Angelier, F. , Shaffer, S. A. , Weimerskirch, H. , & Chastel, O. (2006). Effect of age, breeding experience and senescence on corticosterone and prolactin levels in a long‐lived seabird: The wandering albatross. General and Comparative Endocrinology, 149, 1–9. 10.1016/j.ygcen.2006.04.006 PubMed DOI

Bautista, L. M. , Silván, G. , Cáceres, S. , Martínez‐Fernández, L. , Bravo, C. , Illera, J. C. , … Blanco, G. (2013). Faecal sexual steroids in sex typing and endocrine status of great bustards. European Journal of Wildlife Research, 59, 815–822. 10.1007/s10344-013-0735-6 DOI

Berk, S. , McGettrick, J. , Hansen, W. , & Breuner, C. (2016). Methodological considerations for measuring glucocorticoid metabolites in feathers. Conservation Physiology, 4(1), cow020 10.1093/conphys/cow020 PubMed DOI PMC

Bílková, Z. , Adámková, M. , Albrecht, T. , & Šimek, Z. (2019). Determination of testosterone and corticosterone in feathers using liquid chromatography‐mass spectrometry. Journal of Chromatography A, 1590, 96–103. 10.1016/j.chroma.2018.12.069 PubMed DOI

Bonier, F. , Martin, P. , Moore, I. , & Wingfield, J. (2009). Do baseline glucocorticoids predict fitness? Trends in Ecology and Evolution, 24(11), 634–642. 10.1016/j.tree.2009.04.013 PubMed DOI

Bortolotti, G. R. , Marchant, T. A. , Blas, J. , & German, T. (2008). Corticosterone in feathers is a long‐term, integrated measure of avian stress physiology. Functional Ecology, 22, 494–500. 10.1111/j.1365-2435.2008.01387.x DOI

Boves, T. , Fairhurst, G. , Rushing, C. , & Buehler, D. (2016). Feather corticosterone levels are related to age and future body condition, but not to subsequent fitness, in a declining migratory songbird. Conservation Physiology, 4(1), cow041 10.1093/conphys/cow041 PubMed DOI PMC

Braude, S. , Tang‐Martinez, Z. , & Taylor, G. (1999). Stress, testosterone, and the immunoredistribution hypothesis. Behavioral Ecology, 10, 345–350. 10.1093/beheco/10.3.345 DOI

Buchanan, K. (2000). Stress and the evolution of condition‐dependent signals. Trends in Ecology & Evolution, 15, 156–160. 10.1016/S0169-5347(99)01812-1 PubMed DOI

Crawley, M. (2013). The R book. Chichester, UK: Wiley.

Day, L. , McBroom, J. , & Schlinger, B. (2006). Testosterone increases display behaviors but does not stimulate growth of adult plumage in male golden‐collared manakins (Manacus vitellinus). Hormones and Behavior, 49, 223–232. 10.1016/j.yhbeh.2005.07.006 PubMed DOI

De Ridder, E. , Pinxten, R. , Mees, V. , & Eens, M. (2002). Short‐ and long‐term effects of male‐like concentrations of testosterone on female European Starlings (Sturnus vulgaris). Auk, 119, 487–497. 10.1642/0004-8038(2002)119[0487:SALTEO]2.0.CO;2 DOI

Duckworth, R. , Mendonca, M. , & Hill, G. (2001). A condition dependent link between testosterone and disease resistance in the house finch. Proceedings of the Royal Society B: Biological Sciences, 268(1484), 2467–2472. 10.1098/rspb.2001.1827 PubMed DOI PMC

Ducrest, A. , Keller, L. , & Roulin, A. (2008). Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends in Ecology & Evolution, 23, 502–510. 10.1016/j.tree.2008.06.001 PubMed DOI

Duffy, D. , Bentley, G. , Drazen, D. , & Ball, G. (2000). Effects of testosterone on cell‐mediated and humoral immunity in non‐breeding adult European starlings. Behavioral Ecology, 11(6), 654–662. 10.1093/beheco/11.6.654 DOI

Evans, M. , Goldsmith, A. , & Norris, S. (2000). The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behavioral Ecology and Sociobiology, 47(3), 156–163. 10.1007/s002650050006 DOI

Fairhurst, G. D. , Berzins, L. L. , Bradley, D. W. , Laughlin, A. J. , Romano, A. , Romano, M. , … Clark, R. G. (2015). Assessing costs of carrying geolocators using feather corticosterone in two species of aerial insectivore. Royal Society Open Science, 2, 150004–150004. 10.1098/rsos.150004 PubMed DOI PMC

Fairhurst, G. , Dawson, R. , van Oort, H. , & Bortolotti, G. (2014). Synchronizing feather‐based measures of corticosterone and carotenoid‐dependent signals: What relationships do we expect? Oecologia, 174(3), 689–698. 10.1007/s00442-013-2830-5 PubMed DOI

Folstad, I. , & Karter, A. (1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist, 139(3), 603–622. 10.1086/285346 DOI

Goutte, A. , Antoine, É. , Weimerskirch, H. , & Chastel, O. (2010). Age and the timing of breeding in a long‐lived bird: A role for stress hormones? Functional Ecology, 24, 1007–1016. 10.1111/j.1365-2435.2010.01712.x DOI

Goymann, W. , & Wingfield, J. (2014). Male‐to‐female testosterone ratios, dimorphism, and life history—what does it really tell us? Behavioral Ecology, 25, 685–699. 10.1093/beheco/aru019 DOI

Grunst, M. , Grunst, A. , Parker, C. , Romero, M. , & Rotenberry, J. (2014). Pigment‐specific relationships between feather corticosterone concentrations and sexual coloration. Behavioral Ecology, 26(3), 706–715. 10.1093/beheco/aru210 DOI

Harms, N. J. , Legagneux, P. , Gilchrist, H. G. , Bety, J. , Love, O. P. , Forbes, M. R. , … Soos, C. (2015). Feather corticosterone reveals effect of moulting conditions in the autumn on subsequent reproductive output and survival in an Arctic migratory bird. Proceedings of the Royal Society B: Biological Sciences, 282(1800), 20142085 10.1098/rspb.2014.2085 PubMed DOI PMC

Hau, M. , & Goymann, W. (2015). Endocrine mechanisms, behavioral phenotypes and plasticity: Known relationships and open questions. Frontiers in Zoology, 12, S7 10.1186/1742-9994-12-S1-S7 PubMed DOI PMC

Hau, M. , Ricklefs, R. , Wikelski, M. , Lee, K. , & Brawn, J. (2010). Corticosterone, testosterone and life‐history strategies of birds. Proceedings of the Royal Society B: Biological Sciences, 277(1697), 3203–3212. 10.1098/rspb.2010.0673 PubMed DOI PMC

Heidinger, B. , Nisbet, I. , & Ketterson, E. (2006). Older parents are less responsive to a stressor in a long‐lived seabird: A mechanism for increased reproductive performance with age? Proceedings of the Royal Society B: Biological Sciences, 273, 2227–2231. 10.1098/rspb.2006.3557 PubMed DOI PMC

Jenni, L. , & Winkler, R. (1994). Moult and ageing of European Passerines. London, UK: Academic Press.

Jenni‐Eiermann, S. , Helfenstein, F. , Vallat, A. , Glauser, G. , & Jenni, L. (2015). Corticosterone: Effects on feather quality and deposition into feathers. Methods in Ecology and Evolution, 6(2), 237–246. 10.1111/2041-210X.12314 DOI

Kempenaers, B. , Peters, A. , & Foerster, K. (2008). Sources of individual variation in plasma testosterone levels. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1497), 1711–1723. 10.1098/rstb.2007.0001 PubMed DOI PMC

Koren, L. , Nakagawa, S. , Burke, T. , Soma, K. , Wynne‐Edwards, K. , & Geffen, E. (2012). Non‐breeding feather concentrations of testosterone, corticosterone and cortisol are associated with subsequent survival in wild house sparrows. Proceedings of the Royal Society B: Biological Sciences, 279(1733), 1560–1566. 10.1098/rspb.2011.2062 PubMed DOI PMC

Lattin, C. , Reed, J. , DesRochers, D. , & Romero, L. (2011). Elevated corticosterone in feathers correlates with corticosterone‐induced decreased feather quality: A validation study. Journal of Avian Biology, 42(3), 247–252. 10.1111/j.1600-048X.2010.05310.x DOI

Lendvai, Á. , Giraudeau, M. , Bókony, V. , Angelier, F. , & Chastel, O. (2015). Within‐individual plasticity explains age‐related decrease in stress response in a short‐lived bird. Biology Letters, 11(7), 20150272 10.1098/rsbl.2015.0272 PubMed DOI PMC

Lendvai, Á. , Giraudeau, M. , Németh, J. , Bakó, V. , & McGraw, K. (2013). Carotenoid‐based plumage coloration reflects feather corticosterone levels in male house finches (Haemorhous mexicanus). Behavioral Ecology and Sociobiology, 67(11), 1817–1824. 10.1007/s00265-013-1591-9 DOI

Lessells, C. , & Boag, P. (1987). Unrepeatable repeatabilities: A common mistake. Auk, 104, 116–121. 10.2307/4087240 DOI

López‐Jiménez, L. , Blas, J. , Tanferna, A. , Cabezas, S. , Marchant, T. , Hiraldo, F. , & Sergio, F. (2016). Lifetime variation in feather corticosterone levels in a long‐lived raptor. Oecologia, 183, 315–326. 10.1007/s00442-016-3708-0 PubMed DOI

Møller, A. , Mousseau, T. , Rudolfsen, G. , Balbontín, J. , Marzal, A. , Hermosell, I. , & De Lope, F. (2009). Senescent sperm performance in old male birds. Journal of Evolutionary Biology, 22, 334–344. 10.1111/j.1420-9101.2008.01650.x PubMed DOI

Monclús, L. , Carbajal, A. , Tallo‐Parra, O. , Sabés‐Alsina, M. , Darwich, L. , Molina‐López, R. , & Lopez‐Bejar, M. (2017). Relationship between feather corticosterone and subsequent health status and survival in wild Eurasian Sparrowhawk. Journal of Ornithology, 158, 773–783. 10.1007/s10336-016-1424-5 DOI

Palme, R. (2005). Measuring fecal steroids: Guidelines for practical application. Annals of the New York Academy of Sciences, 1046(1), 75–80. 10.1196/annals.1343.007 PubMed DOI

Quillfeldt, P. , Masello, J. , Strange, I. , & Buchanan, K. (2006). Begging and provisioning of thin‐billed prions, Pachyptila belcheri, are related to testosterone and corticosterone. Animal Behaviour, 71(6), 1359–1369. 10.1016/j.anbehav.2005.09.015 DOI

R Core Team (2016). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; Retrieved from http://www.R-project.org/

Reed, T. , Kruuk, L. , Wanless, S. , Frederiksen, M. , Cunningham, E. , & Harris, M. (2008). Reproductive senescence in a long‐lived seabird: Rates of decline in late‐life performance are associated with varying costs of early reproduction. American Naturalist, 171, E89–E101. 10.1086/524957 PubMed DOI

Roberts, M. , Buchanan, K. , & Evans, M. (2004). Testing the immunocompetence handicap hypothesis: A review of the evidence. Animal Behaviour, 68, 227–239. 10.1016/j.anbehav.2004.05.001 DOI

Romero, L. , Ramenofsky, M. , & Wingfield, J. (1997). Season and migration alters the corticosterone response to capture and handling in an Arctic Migrant, the White‐Crowned Sparrow (Zonotrichia leucophrys gambelii). Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, 116(2), 171–177. 10.1016/S0742-8413(96)00208-3 PubMed DOI

Romero, L. , & Reed, J. (2005). Collecting baseline corticosterone samples in the field: Is under 3 min good enough? Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 140(1), 73–79. 10.1016/j.cbpb.2004.11.004 PubMed DOI

Romero, L. , Strochlic, D. , & Wingfield, J. (2005). Corticosterone inhibits feather growth: Potential mechanism explaining seasonal down regulation of corticosterone during molt. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology, 142(1), 65–73. 10.1016/j.cbpa.2005.07.014 PubMed DOI

Rubolini, D. , Massi, A. , & Spina, F. (2002). Replacement of body feathers is associated with low pre‐migratory energy stores in a long‐distance migratory bird, the barn swallow (Hirundo rustica). Journal of Zoology, 258(4), 441–447. 10.1017/S0952836902001590 DOI

Rutkowska, J. , Cichoń, M. , Puerta, M. , & Gil, D. (2005). Negative effects of elevated testosterone on female fecundity in zebra finches. Hormones and Behavior, 47(5), 585–591. 10.1016/j.yhbeh.2004.12.006 PubMed DOI

Safran, R. , Adelman, J. , McGraw, K. , & Hau, M. (2008). Sexual signal exaggeration affects physiological state in male barn swallows. Current Biology, 18, R461–R462. https://linkinghub.elsevier.com/retrieve/pii/S0960982208003722 PubMed

Saino, N. , & Møller, A. (1994). Secondary sexual characters, parasites and testosterone in the barn swallow, Hirundo rustica . Animal Behaviour, 48, 1325–1333. 10.1006/anbe.1994.1369 DOI

Saino, N. , Romano, M. , Caprioli, M. , Ambrosini, R. , Rubolini, D. , Scandolara, C. , & Romano, A. (2012). A ptilochronological study of carry‐over effects of conditions during wintering on breeding performance in the barn swallow Hirundo rustica . Journal of Avian Biology, 43(6), 513–524. 10.1111/j.1600-048X.2012.05622.x DOI

Star‐Weinstock, M. , Williamson, B. , Dey, S. , Pillai, S. , & Purkayastha, S. (2012). LC‐ESI‐MS/MS analysis of testosterone at sub‐picogram levels using a novel derivatization reagent. Analytical Chemistry, 84, 9310–9317. 10.1021/ac302036r PubMed DOI

Strong, R. , Pereira, G. , Shore, R. , Henrys, P. , & Pottinger, T. (2015). Feather corticosterone content in predatory birds in relation to body condition and hepatic metal concentration. General and Comparative Endocrinology, 214, 47–55. 10.1016/j.ygcen.2015.03.002 PubMed DOI

Wilcoxen, T. , Bridge, E. , Boughton, R. , Hahn, T. , & Schoech, S. (2013). Physiology of reproductive senescence in Florida scrub‐jays: Results from a long‐term study and GnRH challenge. General and Comparative Endocrinology, 194, 168–174. 10.1016/j.ygcen.2013.09.016 PubMed DOI

Zobrazit více v PubMed

Dryad
10.5061/dryad.v4bf803

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...