Skip to main content
Log in

Seasonal modulation of the adrenocortical stress responses in Chilean populations of Zonotrichia capensis

  • Original Article
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

Abstract

To persist in a landscape, organisms are often faced with evolutionary tradeoffs between individual survival and reproduction. In environments where breeding opportunities are brief, it has been hypothesized that individuals will decrease investments in self-preservation in favor of reproductive success. Many avian species in the Northern Hemisphere have been shown to diminish their physiological response to perturbations of the environment by decreasing the adrenocortical response to acute stress during the parental care phase of reproduction. We present results from three populations of Rufous-collared Sparrow (Zonotrichia capensis) in the Southern Hemisphere in which we compared the dynamics of changes in plasma levels of corticosterone after capture, handling and restraint in pre-breeding and nesting phases. The results suggest that the degree of seasonal reduction of the adrenocortical stress response in parental birds is different from that of congeners in the Northern Hemisphere. Males of all three populations of Z. capensis in our study attenuated the adrenocortical stress response equally between the early breeding and parental sub-phases of nesting despite breeding at very different altitudes and latitudes. In contrast, females from all three populations showed no seasonal attenuation of the adrenocortical stress response over the seasons examined in this study. These findings suggest that further comparative investigations are needed to compare Northern Hemisphere-based endocrine patterns in different, global contexts.

Zusammenfassung

Saisonale Modulation der adrenokortikalen Reaktion auf Stress in chilenischen Populationen von Zonotrichia capensis

Um in einer Landschaft bestehen zu können, müssen Organismen häufig evolutionäre Kompromisse zwischen ihrem eigenen Überleben und ihrer Fortpflanzung eingehen. Es wurde die Hypothese aufgestellt, dass in einer Umwelt, in der Brutmöglichkeiten knapp sind, Individuen zu Gunsten ihres Reproduktionserfolges die Investition in ihre eigene Selbsterhaltung reduzieren. Es konnte für viele Vogelarten der nördlichen Hemisphäre nachgewiesen werden, dass sie ihre physiologische Reaktion auf Umweltstörungen durch eine Herabsenkung der adrenokortikalen Reaktion auf Stress während der Zeit der elterlichen Fürsorge vermindern. Wir präsentieren hier Ergebnisse für drei Populationen der Morgenammer (Zonotrichia capensis) der südlichen Hemisphäre, für die während der Vorbrut-und Nistzeit die Veränderungsdynamik des Corticosteronspiegels im Plasma nach dem jeweiligen Fang und dem Handling des Vogels verglichen wurden. Die Ergebnisse lassen vermuten, dass der Grad der saisonalen Reduktion der adrenokortikalen Reaktion auf Stress in Elternvögeln unterschiedlich zu dem der Artgenossen der nördlichen Hemisphäre ist. In unserer Studie verminderten die Männchen aller drei Populationen von Z. capensis gleichermaßen die adrenokortikale Reaktion zwischen der frühen Brutphase und den Teilphasen der elterlichen Fürsorge während der Nistzeit, unabhängig von der Lage der Bruten in unterschiedlichen Höhen-und Breitengraden. Im Gegenteil dazu zeigte keines der Weibchen der drei Populationen während des Untersuchungszeitraumes eine saisonale Verringerung der adrenokortikalen Reaktion. Diese Ergebnisse deuten darauf hin, dass weitere Studien nötig sind, um die auf der nördlichen Hemisphäre basierenden endokrinen Muster in verschiedenen globalen Kontexten zu vergleichen.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Addis EA, Clark AD, Wingfield JC (2011) Modulation of androgens in southern hemisphere temperate breeding sparrows (Zonotrichia capensis): an altitudinal comparison. Horm Behav 60:195–201

    Article  CAS  PubMed  Google Scholar 

  • Addis EA, Clark AD, Vasquez RA, Wingfield JC (2013) Seasonal modulation of testosterone during breeding of the Rufous-collared Sparrow (Zonotrichia capensis australis) in Southern Patagonia. Physiol Biochem Zool 86:782–790

    Article  PubMed  Google Scholar 

  • Bears H, Smith JNM, Wingfield JC (2003) Adrenocortical sensitivity to stress in Dark-eyed Juncos (Junco hyemalis oregonus) breeding in low and high elevation habitat. Ecoscience 10:127–133

    Article  Google Scholar 

  • Bokony V, Lendvai AZ, Liker A, Angelier F, Wingfield JC, Chastel O (2009) Stress response and the value of reproduction: are birds prudent parents? Am Nat 173:589–598

    Article  PubMed  Google Scholar 

  • Breuner CW, Orchinik M, Hahn TP, Meddle SL, Moore IT, Owen-Ashley NT, Sperry TS, Wingfield JC (2003) Differential mechanisms for regulation of the stress response across latitudinal gradients. Am J Physiol Reg Integ Comp Physiol 285:R594–R600

    Article  CAS  Google Scholar 

  • Busch DS, Addis EA, Clark AD, Wingfield JC (2010) Disentangling the effects of environment and life-history stage on corticosterone modulation in Costa Rican Rufous-collared Sparrows, Zonotrichia capensis costaricensis. Physiol Biochem Zool 83:87–96

    Article  CAS  PubMed  Google Scholar 

  • Chapman FM (1941) The post-glacial history of Zonotrichia capensis. Bull Am Mus Nat Hist 57:381–438

    Google Scholar 

  • González-Goméz PL, Merrill L, Ellis VA, Venegas C, Pantoja JI, Vásquez RA, Wingfield JC (2013) Breaking down seasonality: androgen modulation and stress response in a highly stable environment. Gen Comp Endocrinol 191:1–12

    Article  CAS  PubMed  Google Scholar 

  • Hau M, Wingfeld JC (2011) Hormonallyregulated trade-offs: evolutionary variability and phenotypic plasticity in testosterone signaling pathways. In: Flatt T, Heyland A (eds) Mechanisms of life history evolution. Oxford University Press, Oxford, pp 349–361

    Chapter  Google Scholar 

  • Hau M, Ricklefs RE, Wikelski M, Lee KA, Brawn JD (2010) Corticosterone, testosterone and life-history strategies in birds. Proc R Soc B 277:3203–3212

    Article  CAS  PubMed  Google Scholar 

  • Holberton RL, Wingfield JC (2003) Modulating the corticosterone stress response: a mechanism for balancing individual risk and reproductive success in Arctic-breeding sparrows? Auk 120:1140–1150

    Article  Google Scholar 

  • King JR (1973) Annual cycle of Rufous-collared Sparrow (Zonotrichia capensis) in three biotopes in northwestern Argentina. J Zool Lond 170:163–188

    Article  Google Scholar 

  • King JR (1974) Notes on geographical variation and annual cycle in Patagonian populations of Rufous-collared Sparrow Zonotrichia capensis. Ibis 116:74–83

    Article  Google Scholar 

  • Lisovski S, Ramenofsky M, Wingfield JC (2017) Defining the degree of seasonality and its significance for future research. Integr Comp Biol. https://doi.org/10.1093/icb/icx040

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin K, Wiebe KL (2004) Coping mechanisms of alpine and Arctic breeding birds: extreme weather and limitations to reproductive resilience. Integr Comp Biol 44:177–185

    Article  PubMed  Google Scholar 

  • McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43:2–15

    Article  Google Scholar 

  • Meddle SL, Owen-Ashley NT, Richardson MI, Wingfield JC (2003) Modulation of the hypothalamic-pituitary-adrenal axis of an Arctic-breeding polygynandrous songbird, the Smith’s Longspur, Calcarius pictus. Proc R Soc Lond B 270:1849–1856

    Article  CAS  Google Scholar 

  • Pereyra ME, Wingfield JC (2003) Changes in plasma corticosterone and adrenocortical response to stress during the breeding cycle in high altitude flycatchers. Gen Comp Endocrinol 130:222–231

    Article  CAS  PubMed  Google Scholar 

  • Poblete Y, Gutiérez V, Cid V, Newsome S, Sabat P, Vasquez RA (2018) Intraspecific variation in exploratory behavior and elevational affinity in a widely distributed songbird. Oecologia. https://doi.org/10.1007/s00442-018-4076-8

    Article  PubMed  Google Scholar 

  • Quirici V, Venegas CI, Gonzalez-Gomez PL, Castano-Villa GJ, Wingfield JC, Vásquez RA (2014) Baseline corticosterone and stress response in the Thorn-tailed Rayadito (Aphrastura spinicauda) along a latitudinal gradient. Gen Comp Endocrinol 198:39–46

    Article  CAS  PubMed  Google Scholar 

  • Quirici V, Guerrero J, Krause J, Wingfield JC, Vásquez RA (2016) The relationship of telomere length to baseline corticosterone levels in nestlings of an altricial passerine bird in natural populations. Front Zool 13:1. https://doi.org/10.1186/s12983-016-0133-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24

    Article  CAS  Google Scholar 

  • Romero LM, Wingfield JC (2016) Tempests, poxes, predators and people: stress in wild animals and how they cope. Oxford University Press, Oxford, p 624

    Google Scholar 

  • Rozzi R, Jimenez JE (2014) A summary of the birds captured with mist-nets and/or censused in the southernmost forests of the world. In: Rozzi R, Jimenez JE (eds) Magellanic sub-Antartic ornithology: first decade of long-term studies at the Omora Ethnobotanical Park, Chile. Universidad de Magallanes and University of North Texas, Cape Horn Biosphere Reserve, South Chile, pp 41–97

    Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrin Rev 21:55–89

    CAS  Google Scholar 

  • Schoech SJ, Romero LM, Moore IT, Bonier F (2013) Constraints, concerns and considerations about the necessity of estimating free glucococorticoid concentrations for field endocrine studies. Funct Ecol. https://doi.org/10.1111/1365=2435.12142

    Article  Google Scholar 

  • Schwabl P, Bonaccorso E, Goymann W (2016) Diurnal variation in corticosterone release among wild tropical forest birds. Front Zool 13:19. https://doi.org/10.1186/s12983-016-0152-3

    Article  PubMed  PubMed Central  Google Scholar 

  • Silverin B, Arvidsson B, Wingfield JC (1997) The adrenocortical responses to stress in breeding Willow Warblers Phylloscopus trochilus in Sweden: effects of latitude and gender. Funct Ecol 11:376–384

    Article  Google Scholar 

  • Wada H, Moore IT, Breuner CW, Wingfield JC (2006) Stress responses in tropical sparrows: comparing tropical and temperate Zonotrichia. Physiol Biochem Zool 79:784–792

    Article  PubMed  Google Scholar 

  • Walker BG, Meddle SL, Romero LM, Landys MM, Reneerkens J, Wingfield JC (2015) Breeding on the extreme edge: modulation of the adrenocortical response to acute stress in two High Arctic passerines. J Exp Zool 323A:266–275

    Article  Google Scholar 

  • Wilson CM, Holberton RL (2004) Individual risk versus immediate reproductive success: a basis for latitudinal differences in the adrenocortical response to stress in Yellow Warblers (Dendroica petechia). Auk 121:1238–1249

    Article  Google Scholar 

  • Wingfield JC (2003) Control of behavioural strategies for capricious environments. Anim Behav 66:807–816

    Article  Google Scholar 

  • Wingfield JC (2013) The comparative biology of environmental stress: behavioral endocrinology and variation in ability to cope with novel, changing environments. Anim Behav 85:1127–1133

    Article  Google Scholar 

  • Wingfield JC (2015) Coping with change: a framework for environmental signals and how neuroendocrine pathways might respond. Front Neuroendocrinol. https://doi.org/10.1016/j.ymfe.2014.11.005

    Article  PubMed  Google Scholar 

  • Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15:711–724

    Article  CAS  PubMed  Google Scholar 

  • Wingfield JC, Vleck CM, Moore MC (1992) Seasonal-changes of the adrenocortical-response to stress in birds of the Sonoran desert. J Exp Zool 264:419–428

    Article  CAS  PubMed  Google Scholar 

  • Wingfield JC, O’Reilly KM, Astheimer LB (1995) Modulation of the adrenocortical responses to acute stress in arctic birds—a possible ecological basis. Amer Zool 35:285–294

    Article  CAS  Google Scholar 

  • Wingfield JC, Owen-Ashley NT, Benowitz-Fredericks ZM, Lynn SE, Hahn TP, Wada H, Breuner CM, Meddle SL, Romero LM (2004) Arctic spring: the arrival biology of migrant birds. Acta Zool Sin 50:948–960

    CAS  Google Scholar 

  • Wingfield JC, Moore IT, Vásquez RA, Sabat P, Busch S, Clark A, Addis E, Prado F, Wada H (2008) Modulation of the adrenocortical responses to acute stress in northern and southern populations of Zonotrichia. Ornitol Neotrop 19:241–251

    Google Scholar 

Download references

Acknowledgments

We would like to thank the Universidad de Chile, the Omora Foundation, Cristobal Venegas, Pablo Sabat, Stephen McGhee, Chris Anderson and Ricardo Rozzi for their help and support in Chile. This research was funded by National Science Foundation grants to J. C. Wingfield (IBN-0317141 and IOS-0712882), and grants to R. A. Vásquez (FONDECYT 1140548, ICM-P05-002, and PFB-23-CONICYT-Chile). All procedures in this manuscript comply with current laws and were approved by Institutional Animal Care and Use Committees.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John C. Wingfield.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Additional information

Communicated by L. Fusani.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 271 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Clark, A.D., Addis, E.A., Vásquez, R.A. et al. Seasonal modulation of the adrenocortical stress responses in Chilean populations of Zonotrichia capensis. J Ornithol 160, 61–70 (2019). https://doi.org/10.1007/s10336-018-1589-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-018-1589-1

Keywords

Navigation