Advertisement

Hormonal responses to non-mimetic eggs: is brood parasitism a physiological stressor during incubation?

  • Francisco Ruiz-RayaEmail author
  • Manuel Soler
  • Teresa Abaurrea
  • Olivier Chastel
  • Gianluca Roncalli
  • Juan Diego Ibáñez-Álamo
Original Article

Abstract

Many host species have evolved sophisticated defences to mitigate the high fitness costs imposed by brood parasitism. Even though the physiological mechanisms behind such defences can offer important insights into the evolutionary relationship between brood parasites and hosts, they have received little attention so far. Hormones play a critical role in the regulation of bird reproduction, which make them a key element when investigating the physiological effects of brood parasitism on hosts. Here, we experimentally parasitized Eurasian blackbird (Turdus merula) nests with non-mimetic eggs to study its impact on the hormonal levels (corticosterone and prolactin) of females during incubation, as well as the magnitude of the response to the standardized stress protocol in parasitized and non-parasitized individuals. Parasitized females had higher baseline corticosterone levels and showed a poorer body condition than non-parasitized birds, while we found no differences for prolactin levels. Both parasitized and non-parasitized females responded to the standardized-stress protocol with a significant increase in corticosterone levels. However, the decrease in prolactin after the standardized stress protocol was significantly more pronounced in parasitized individuals. Our results suggest that the presence of a non-mimetic parasitic egg involves a stressful situation for hosts, negatively affecting the physical state of parasitized females. Unaffected prolactin levels of parasitized individuals could explain the absence of nest desertion found in this species in response to parasitism. Finally, both hormones were not correlated in blackbirds, confirming that their combined study provides valuable pieces of information on the endocrine mechanisms underlying behavioural responses in animals, including hosts of brood parasites.

Significance statement

Physiological mechanisms behind avian brood parasitism remain unclear. In this study, we assessed the effect of experimental parasitism on the hormonal profiles of hosts. We found that the presence of a non-mimetic egg in the nest modified baseline corticosterone levels, but not prolactin levels, of parasitized females and negatively impacted their body condition. Moreover, experimental parasitism affected the prolactin response to stress. These results expand previous information on the endocrine consequences of brood parasitism at other stages of the breeding cycle (nestling and fledgling stage) and might shed light on the hormonal mechanisms that underlie the host response against parasitic eggs.

Keywords

Body condition Corticosterone Egg rejection Hormonal stress response Prolactin Standardized stress protocol 

Notes

Acknowledgments

At the CEBC, we thank Charline Parenteau and Colette Trouvé for their excellent technical assistance in hormonal assays. We would also like to thank the two anonymous reviewers whose advices and constructive comments improved the manuscript.

Funding

Financial support has been provided by the Consejería de Economía, Innovación, Ciencia y Empleo; Junta de Andalucía (research project CVI-6653 to MS). FRR stay at the CEBC (France) was financed by a mobility grant from the University of Granada/CEI BioTic Granada 2014/2015 (cofounded by Consejería de Economía, Innovación, Ciencia y Empleo from Junta de Andalucía; Fondo Europeo de Desarrollo Regional FEDER; and CEI BioTic Granada).

Compliance with ethical standards

Ethical approval

We performed the study following all relevant Spanish national (Decreto 105/2011, 19 de Abril) and regional guidelines. Ethical approval for this study was not required. Research disturbance, due to blood sampling protocol (details provided above), was minimized by using only those females that did not ejected the parasitic egg. The time spent at each nest was the minimum necessary for blood sampling. No female deserted their nest during the 3 days after to our experimental manipulation and none exhibited any long-term effects of the study.

Competing interests

The authors declare that they have no conflict of interest.

References

  1. Adams NJ, Farnworth MJ, Rickett J, Parker KA, Cockrem JF (2011) Behavioural and corticosterone responses to capture and confinement of wild blackbirds (Turdus merula). Appl Anim Behav Sci 134:246–255.  https://doi.org/10.1016/j.applanim.2011.07.001 CrossRefGoogle Scholar
  2. Addis EA, Davis JE, Miner BE, Wingfield JC (2011) Variation in circulating corticosterone levels is associated with altitudinal range expansion in a passerine bird. Oecologia 167:369–378.  https://doi.org/10.1007/s00442-011-2001-5 CrossRefPubMedGoogle Scholar
  3. Angelier F, Chastel O (2009) Stress, prolactin and parental investment in birds: a review. Gen Comp Endocrinol 163:142–148.  https://doi.org/10.1016/j.ygcen.2009.03.028 CrossRefPubMedGoogle Scholar
  4. Angelier F, Wingfield JC (2013) Importance of the glucocorticoid stress response in a changing world: theory, hypotheses and perspectives. Gen Comp Endocrinol 190:118–128.  https://doi.org/10.1016/j.ygcen.2013.05.022 CrossRefPubMedGoogle Scholar
  5. Angelier F, Moe B, Weimerskirch H, Chastel O (2007) Age-specific reproductive success in a long-lived bird: do older parents resist stress better? J Anim Ecol 76:1181–1191.  https://doi.org/10.1111/j.1365-2656.2007.01295.x CrossRefPubMedGoogle Scholar
  6. Angelier F, Clément-Chastel C, Welcker J, Gabrielsen GW, Chastel O (2009a) How does corticosterone affect parental behaviour and reproductive success? A study of prolactin in black-legged kittiwakes. Funct Ecol 23:784–793.  https://doi.org/10.1111/j.1365-2435.2009.01545.x CrossRefGoogle Scholar
  7. Angelier F, Moe B, Blanc S, Chastel O (2009b) What factors drive prolactin and corticosterone responses to stress in a long-lived bird species (snow petrel Pagodroma nivea)? Physiol Biochem Zool 82:590–602.  https://doi.org/10.1086/603634 CrossRefPubMedGoogle Scholar
  8. Angelier F, Wingfield JC, Trouvé C, de Grissas S, Chastel O (2013) Modulation of the prolactin and the corticosterone stress responses: do they tell the same story in a long-lived bird, the cape petrel? Gen Comp Endocrinol 182:7–15.  https://doi.org/10.1016/j.ygcen.2012.10.008 CrossRefPubMedGoogle Scholar
  9. Angelier F, Wingfield JC, Parenteau C, Pellé M, Chastel O (2015) Does short-term fasting lead to stressed-out parents? A study of incubation commitment and the hormonal stress responses and recoveries in snow petrels. Horm Behav 67:28–37.  https://doi.org/10.1016/j.yhbeh.2014.11.009 CrossRefPubMedGoogle Scholar
  10. Angelier F, Wingfield JC, Tartu S, Chastel O (2016a) Does prolactin mediate parental and life-history decisions in response to environmental conditions in birds? A review. Horm Behav 77:18–29.  https://doi.org/10.1016/j.yhbeh.2015.07.014 CrossRefPubMedGoogle Scholar
  11. Angelier F, Parenteau C, Ruault S, Angelier N (2016b) Endocrine consequences of an acute stress under different thermal conditions: a study of corticosterone, prolactin, and thyroid hormones in the pigeon (Columbia livia). Comp Biochem Physiol A 196:38–45.  https://doi.org/10.1016/j.cbpa.2016.02.010 CrossRefGoogle Scholar
  12. Avilés JM, Soler JJ, Soler M, Møller AP (2004) Rejection of parasitic eggs in relation to egg appearance in magpies. Anim Behav 67:951–958.  https://doi.org/10.1016/j.anbehav.2003.08.022 CrossRefGoogle Scholar
  13. Breuner CW, Patterson SH, Hahn TP (2008) In search of relationships between the acute adrenocortical response and fitness. Gen Comp Endocrinol 157:288–295.  https://doi.org/10.1016/j.ygcen.2008.05.017 CrossRefPubMedGoogle Scholar
  14. Buntin JD (1996) Neural and hormonal control of parental behavior in birds. Adv Stud Behav 25:161–213.  https://doi.org/10.1016/S0065-3454(08)60333-2 CrossRefGoogle Scholar
  15. Chastel O, Lormée H (2002) Patterns of prolactin secretion in relation to incubation failure in a tropical seabird, the red-footed booby. Condor 104:873–876. https://doi.org/10.1650/0010-5422(2002)104[0873:popsir]2.0.co;2Google Scholar
  16. Chastel O, Lacroix A, Weimerskirch H, Gabrielsen GW (2005) Modulation of prolactin but not corticosterone responses to stress in relation to parental effort in a long-lived bird. Horm Behav 47:459–466.  https://doi.org/10.1016/j.yhbeh.2004.10.009 CrossRefPubMedGoogle Scholar
  17. Cherel Y, Mauget R, Lacroix A, Gilles J (1994) Seasonal and fasting-related changes in circulating gonadal steroids and prolactin in king penguins, Aptenodytes patagonicus. Physiol Zool 67:1154–1173CrossRefGoogle Scholar
  18. Criscuolo F, Chastel O, Gabrielsen GW, Lacroix A, Le Maho Y (2002) Factors affecting plasma concentrations of prolactin in the common eider Somateria mollissima. Gen Comp Endocrinol 125:399–409.  https://doi.org/10.1006/gcen.2001.7767 CrossRefPubMedGoogle Scholar
  19. Davies NB (2000) Cuckoos, cowbirds and other cheats. Poyser, LondonGoogle Scholar
  20. Goutte A, Antoine É, Chastel O (2011) Experimentally delayed hatching triggers a magnified stress response in a long-lived bird. Horm Behav 59:167–173.  https://doi.org/10.1016/j.yhbeh.2010.11.004 CrossRefPubMedGoogle Scholar
  21. Grim T, Samas P, Moskát C, Kelven O, Honza M, Moksnes A, Roskaft E, Stokke B (2011) Constraints on host choice: why do parasitic birds rarely exploit some common potential hosts? J Anim Ecol 80:508–518.  https://doi.org/10.1111/j.1365-2656.2010.01798.x CrossRefPubMedGoogle Scholar
  22. Groscolas R, Lacroix A, Robin JP (2008) Spontaneous egg or chick abandonment in energy-depleted king penguins: a role for corticosterone and prolactin? Horm Behav 53:51–60.  https://doi.org/10.1016/j.yhbeh.2007.08.010 CrossRefPubMedGoogle Scholar
  23. Hahn DC, Wingfield JC, Fox DM, Walker BG, Thomley JE (2017) Maternal androgens in avian brood parasites and their hosts: responses to parasitism and competition? Gen Comp Endocrinol 240:143–152.  https://doi.org/10.1016/j.ygcen.2016.10.004 CrossRefPubMedGoogle Scholar
  24. Hall TR, Harvey S, Chadwick A (1986) Control of prolactin secretion in birds: a review. Gen Comp Endocrinol 62:171–184.  https://doi.org/10.1016/0016-6480(86)90107-3 CrossRefPubMedGoogle Scholar
  25. Hau M, Ricklefs RE, Wikelski M, Lee KA, Brawn JD (2010) Corticosterone, testosterone and life-history strategies of birds. Proc R Soc Lond B 277:3203–3212.  https://doi.org/10.1098/rspb.2010.0673 CrossRefGoogle Scholar
  26. Heidinger BJ, Chastel O, Nisbet ICT, Ketterson ED (2010) Mellowing with age: older parents are less responsive to a stressor in a long-lived seabird. Funct Ecol 24:1037–1044.  https://doi.org/10.1111/j.1365-2435.2010.01733.x CrossRefGoogle Scholar
  27. Ibáñez-Álamo JD, Soler M (2010) Does urbanization affect selective pressures and life-history strategies in the common blackbird (Turdus merula L.)? Biol J Linn Soc 101:759–766.  https://doi.org/10.1111/j.1095-8312.2010.01543.x CrossRefGoogle Scholar
  28. Ibáñez-Álamo JD, Chastel O, Soler M (2011) Hormonal response of nestlings to predator calls. Gen Comp Endocrinol 171:232–236.  https://doi.org/10.1016/j.ygcen.2011.01.016 CrossRefPubMedGoogle Scholar
  29. Ibáñez-Álamo JD, De Neve L, Roldán M, Rodríguez J, Trouvé C, Chastel O, Soler M (2012) Corticosterone levels in host and parasite nestlings: is brood parasitism a hormonal stressor? Horm Behav 61:590–597.  https://doi.org/10.1016/j.yhbeh.2012.02.008 CrossRefPubMedGoogle Scholar
  30. Jessop TS (2001) Modulation of the adrenocortical stress response in marine turtles (Cheloniidae): evidence for a hormonal tactic maximizing maternal reproductive investment. J Zool 254:57–65.  https://doi.org/10.1017/S0952836901000553 CrossRefGoogle Scholar
  31. Krause JS, Dorsa D, Wingfield JC (2014) Changes in plasma concentrations of progesterone, dehydroepiandrosterone and corticosterone in response to acute stress of capture, handling and restraint in two subspecies of white-crowned sparrows. Comp Biochem Physiol A 177:35–40.  https://doi.org/10.1016/j.cbpa.2014.07.019 CrossRefGoogle Scholar
  32. Krause JS, Meddle SL, Wingfield JC (2015) The effects of acute restraint stress on plasma levels of prolactin and corticosterone across life-history stages in a short-lived bird: Gambel’s white-crowned sparrow (Zonotrichia leucophrys gambelii). Physiol Biochem Zool 88:589–598.  https://doi.org/10.1086/683321 CrossRefPubMedGoogle Scholar
  33. Landys MM, Ramenofsky M, Wingfield JC (2006) Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen Comp Endocrinol 148:132–149.  https://doi.org/10.1016/j.ygcen.2006.02.013 CrossRefPubMedGoogle Scholar
  34. Lendvai AZ, Chastel O (2008) Experimental mate-removal increases the stress response of female house sparrows: the effects of offspring value? Horm Behav 53:395–401.  https://doi.org/10.1016/j.yhbeh.2007.11.011 CrossRefPubMedGoogle Scholar
  35. Lendvai AZ, Chastel O (2010) Natural variation in stress response is related to post-stress parental effort in male house sparrows. Horm Behav 58:936–942.  https://doi.org/10.1016/j.yhbeh.2010.09.004 CrossRefPubMedGoogle Scholar
  36. Lendvai AZ, Giraudeau M, Chastel O (2007) Reproduction and modulation of the stress response: an experimental test in the house sparrow. Proc R Soc Lond B 274:391–397.  https://doi.org/10.1098/rspb.2006.3735 CrossRefGoogle Scholar
  37. Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33.  https://doi.org/10.18637/jss.v069.i01 CrossRefGoogle Scholar
  38. Lormée H, Jouventin P, Lacroix A, Lallemand J, Chastel O (2000) Reproductive endocrinology of tropical seabirds: sex-specific patterns in LH, steroids, and prolactin secretion in relation to parental care. Gen Comp Endocrinol 117:413–426.  https://doi.org/10.1006/gcen.1999.7434 CrossRefPubMedGoogle Scholar
  39. Lormée H, Jouventin P, Trouvé C, Chastel O (2003) Sex-specific patterns in baseline corticosterone and body condition changes in breeding red-footed boobies Sula sula. Ibis 145:212–219.  https://doi.org/10.1046/j.1474-919X.2003.00106.x CrossRefGoogle Scholar
  40. Macleod R, Bernett P, Clark JA, Cresswell W (2005) Body mass change strategies in blackbirds Turdus merula: the starvation-predation risk trade-off. J Anim Ecol 74:292–302.  https://doi.org/10.1111/j.1365-2656.2005.00923.x CrossRefGoogle Scholar
  41. Mark MM (2013) Host-specific parasitism in the central American striped cuckoo, Tapera naevia. J Avian Biol 44:445–450.  https://doi.org/10.1111/j.1600-048X.2013.00100.x CrossRefGoogle Scholar
  42. Mark MM, Rubenstein DR (2013) Physiological costs and carry-over effects of avian interspecific brood parasitism influence reproductive tradeoffs. Horm Behav 63:717–722CrossRefPubMedGoogle Scholar
  43. Martín-Vivaldi M, Soler JJ, Møller AP, Pérez-Contreras T, Soler M (2012) The importance of nest-site and habitat in egg recognition ability of potential hosts of the common cuckoo Cuculus canorus. Ibis 155:140–155.  https://doi.org/10.1111/ibi.12000 CrossRefGoogle Scholar
  44. Miller DA, Vleck CM, Otis DL (2009) Individual variation in baseline and stress-induced corticosterone and prolactin levels predicts parental effort by nesting mourning doves. Horm Behav 56:457–464.  https://doi.org/10.1016/j.yhbeh.2009.08.001 CrossRefPubMedGoogle Scholar
  45. Mundry R, Nunn CL (2009) Stepwise model fitting and statistical inference: turning noise into signal pollution. Am Nat 173:119–123.  https://doi.org/10.1086/593303 CrossRefPubMedGoogle Scholar
  46. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142.  https://doi.org/10.1111/j.2041-210x.2012.00261.x CrossRefGoogle Scholar
  47. Nakagawa S, Johnson PCD, Schielzeth H (2017) The coefficient of determination R 2 and intra-class correlation coefficient from generalized linear mixed-effects models revisited and expanded. J R Soc Interface 14:20170213.  https://doi.org/10.1098/rsif.2017.0213 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Nord A, Williams JB (2015) The energetic costs of incubation. In: Deeming DC, Reynolds SJ (eds) Nests, eggs, and incubation: new ideas about avian reproduction. Oxford University Press, Oxford, pp 152–170CrossRefGoogle Scholar
  49. O’Dwyer TW, Buttemer WA, Priddel DM, Downing JA (2006) Prolactin, body condition and the cost of good parenting: an interyear study in a long-lived seabird, Gould’s petrel (Pterodroma leucoptera). Funct Ecol 20:806–811.  https://doi.org/10.1111/j.1365-2435.2006.01168.x CrossRefGoogle Scholar
  50. O’Reilly KM, Wingfield JC (2001) Ecological factors underlying the adrenocortical response to capture stress in arctic-breeding shorebirds. Gen Comp Endocrinol 124:1–11.  https://doi.org/10.1006/gcen.2001.7676 CrossRefPubMedGoogle Scholar
  51. Ouyang JQ, Sharp PJ, Dawson A, Quettin M, Hau M (2011) Hormone levels predict individual differences in reproductive success in a passerine bird. Proc R Soc Lond B 278:2537–2545.  https://doi.org/10.1098/rspb.2010.2490 CrossRefGoogle Scholar
  52. Partecke J, Schwabl I, Gwinner E (2006) Stress and the city: urbanization and its effects on the stress physiology in european blackbirds. Ecology 87:1945–1952CrossRefPubMedGoogle Scholar
  53. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891.  https://doi.org/10.1111/j.1600-0706.2009.17643.x CrossRefGoogle Scholar
  54. Peig J, Green AJ (2010) The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct Ecol 24:1323–1332.  https://doi.org/10.1111/j.1365-2435.2010.01751.x CrossRefGoogle Scholar
  55. Pinheiro J, Bates D, Debroy S, Sarkar D (2014) nmle: Linear and nonlinear mixed effects models. R package version 3.1–117, http://CRAN.R project.org/package=nlme>
  56. Polačiková L, Grim T (2010) Blunt egg pole holds cues for alien egg discrimination: experimental evidence. J Avian Biol 41:111–116.  https://doi.org/10.1111/j.1600-048X.2010.04983.x CrossRefGoogle Scholar
  57. Préault M, Chastel O, Cézilly F, Faivre B (2005) Male bill colour and age are associated with parental abilities and breeding performance in blackbirds. Behav Ecol Sociobiol 58:497–505.  https://doi.org/10.1007/s00265-005-0937-3 CrossRefGoogle Scholar
  58. R Core Team (2014) R: a language and environment for statistical computing. In: R Foundation for statistical computing, Vienna, Austria http://www.R-project.org Google Scholar
  59. Riechert J, Chastel O, Becker PH (2014) Regulation of breeding behavior: do energy-demanding periods induce a change in prolactin or corticosterone baseline levels in the common tern (Sterna hirundo)? Physiol Biochem Zool 87:420–431.  https://doi.org/10.1086/675682 CrossRefPubMedGoogle Scholar
  60. Roldán M, Soler M (2011) Parental-care parasitism: how do unrelated offspring attain acceptance by foster parents? Behav Ecol 22:679–691.  https://doi.org/10.1093/beheco/arr041 CrossRefGoogle Scholar
  61. Ruiz-Raya F, Soler M, Sánchez-Pérez LL, Ibáñez-Álamo JD (2015) Could a factor that does not affect egg recognition influence the decision of rejection? PLoS One 10:e0135624. doi:  https://doi.org/10.1371/journal.pone.0135624
  62. Ruiz-Raya F, Soler M, Roncalli G, Abaurrea T, Ibáñez-Álamo JD (2016) Egg rejection in blackbirds Turdus merula: a by-product of conspecific parasitism or successful resistance against interspecific brood parasites? Front Zool 13:16.  https://doi.org/10.1186/s12983-016-0148-y CrossRefPubMedPubMedCentralGoogle Scholar
  63. Samas P, Hauber ME, Cassey P, Grim T (2011) Repeatability of foreign egg rejection: testing the assumptions of co-evolutionary theory. Ethology 117:606–619.  https://doi.org/10.1111/j.1439-0310.2011.01917.x CrossRefGoogle Scholar
  64. Samas P, Hauber ME, Cassey P, Grim T (2014) Host responses to interspecific brood parasitism: a by-product of adaptations to conspecific parasitism ? Front Zool 11:34.  https://doi.org/10.1186/1742-9994-11-34 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Preparative actions Endocr Rev 21:55–89.  https://doi.org/10.1210/er.21.1.55 PubMedCrossRefGoogle Scholar
  66. Sharp PJ, Macnamee MC, Sterling RJ, Lea RW, Pedersen HC (1988) Relationships between prolactin, LH and broody behaviour in bantam hens. J Endocrinol 118:279–286.  https://doi.org/10.1677/joe.0.1180279 CrossRefPubMedGoogle Scholar
  67. Silver R (1984) Prolactin and parenting in the pigeon family. J Exp Zool 232:617–625CrossRefPubMedGoogle Scholar
  68. Skaug H, Fournier DA, Nielsen A, Magnusson A, Bolker BM (2016) Generalized linear mixed models using AD model builder. R package v 0.8.3.3 http://glmmadmb.r-forge.r-project.org
  69. Sockman KW, Sharp PJ, Schwabl H (2006) Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility in clutch size, incubation behaviour, and yolk androgen deposition. Biol Rev 81:629–666.  https://doi.org/10.1017/S1464793106007147 CrossRefPubMedGoogle Scholar
  70. Soler M (2014) Long-term coevolution between avian brood parasites and their hosts. Biol Rev 89:688–704.  https://doi.org/10.1111/brv.12075 CrossRefPubMedGoogle Scholar
  71. Soler M, Møller AP (1990) Duration of sympatry and coevolution between the great spotted cuckoo and its magpie host. Nature 343:748–750.  https://doi.org/10.1038/343748a0 CrossRefGoogle Scholar
  72. Soler M, Ruiz-Raya F, Roncalli G, Ibáñez-Álamo JD (2015) Nest desertion cannot be considered an egg-rejection mechanism in a medium-sized host: an experimental study with the common blackbird Turdus merula. J Avian Biol 46:369–377.  https://doi.org/10.1111/jav.00571 CrossRefGoogle Scholar
  73. Soler M, Ruiz-Raya F, Roncalli G, Ibáñez-Álamo JD (2017) Relationships between egg-recognition and egg-ejection in a grasp-ejector species. PLoS One 12:e0166283.  https://doi.org/10.1371/journal.pone.0166283 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Spée M, Beaulieu M, Dervaux A, Chastel O, Le Maho Y, Laclot T (2010) Should I stay or should I go? Hormonal control of nest abandonment in a long-lived bird, the Adélie penguin. Horm Behav 58:762–768.  https://doi.org/10.1016/j.yhbeh.2010.07.011 CrossRefPubMedGoogle Scholar
  75. Tartu S, Angelier F, Wingfield JC, Bustamante P, Labadie P, Budzinski H, Weimerskirch H, Bustnes JO, Chastel O (2015) Corticosterone, prolactin and egg neglect behavior in relation to mercury and legacy POPs in a long-lived Antarctic bird. Sci Total Environ 505:180–188.  https://doi.org/10.1016/j.scitotenv.2014.10.008 CrossRefPubMedGoogle Scholar
  76. Whittingham MJ, Stephens PA, Bradbury RB, Freckleton RP (2006) Why do we still use stepwise modelling in ecology and behaviour? J Anim Ecol 75:1182–1189.  https://doi.org/10.1111/j.1365-2656.2006.01141.x CrossRefPubMedGoogle Scholar
  77. Wingfield JC (1994) Modulation of the adrenocortical response in birds. In: Davey KG, Peter RE, Tobe SS (eds) Perspectives in comparative endocrinology. National Research Council of Canada, Ottawa, pp 520–528Google Scholar
  78. Wingfield JC, Hunt KE (2002) Arctic spring: hormone–behavior interactions in a severe environment. Comp Biochem Physiol B 132:275–286.  https://doi.org/10.1016/S1096-4959(01)00540-1 CrossRefPubMedGoogle Scholar
  79. Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15:711–724.  https://doi.org/10.1046/j.1365-2826.2003.01033.x CrossRefPubMedGoogle Scholar
  80. Wingfield JC, Manney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone-behavior interactions: the “emergency life history stage.”. Am Zool 38:191–206.  https://doi.org/10.1093/icb/38.1.191 CrossRefGoogle Scholar
  81. Wingfield JC, Kelley JP, Angelier F (2011) What are extreme environmental conditions and how do organisms cope with them? Curr Zool 57:363–374CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Departamento de Zoología, Facultad de CienciasUniversidad de GranadaGranadaSpain
  2. 2.School of Psychology and NeuroscienceUniversity of St AndrewsSt AndrewsScotland, UK
  3. 3.Centre d’Études Biologiques de Chizé (CEBC)UMR7372-CNRS/Univ. La RochelleLa RochelleFrance
  4. 4.Groningen Institute for Evolutionary Life SciencesUniversity of GroningenGroningenThe Netherlands

Personalised recommendations