Compensating for a stressful start: maternal corticosterone, offspring survival, and size at fledging in the Zebra Finch, Taeniopygia guttata
Nicola Khan A B C , Richard A. Peters A and Kylie Robert A
+ Author Affiliations
- Author Affiliations
A Department of Ecology, Environment and Evolution, La Trobe University, Bundoora, Vic. 3086, Australia.
B Department of Poultry Science, University of Georgia, Athens, GA 30602, USA.
C Corresponding author. Email: nykhan@uga.edu
Emu 116(3) 262-272 https://doi.org/10.1071/MU15095
Submitted: 11 February 2015 Accepted: 24 December 2015 Published: 13 April 2016
Abstract
All organisms are exposed to a variety of physical, environmental and psychological challenges throughout their lives. We administered repeated oral doses of the stress hormone corticosterone (CORT) to ovulating Zebra Finches (Taeniopygia guttata) in order to mimic a disruptive environment, and investigated the effect on their reproductive output as well as outcomes for their offspring. Although females treated with CORT produced larger clutches than control females, hatching success was significantly reduced in the CORT-treated group, though there was no evidence of bias in offspring sex-ratio. Both treatment and sex had an effect on the size of chicks at hatching and their growth rate. Chicks from the experimental group were smaller at hatching than control chicks but grew faster. Similarly, male chicks were smaller than female chicks at hatching but grew faster than females. However, there was no significant difference in overall condition at nutritional independence, indicating that increased growth rates resulted from compensatory growth. These results have broad evolutionary implications, as maternal CORT is capable of affecting viability of eggs and offspring phenotype, even when maternal diet and body condition remain unchanged. As such, glucocorticoids may play a role in regulating population productivity and offspring phenotype, which provides a promising area for further research into the effects of maternal stress on adult offspring in successive generations.
Additional keywords: compensatory growth, embryo mortality, glucocorticoids, repeated stress, survivorship.
References
Almasi, B., Roulin, A., Jenni-Eiermann, S., and Jenni, L. (2008). Parental investment and its sensitivity to corticosterone is linked to melanin-based coloration in Barn Owls. Hormones and Behavior 54, 217–223.| Parental investment and its sensitivity to corticosterone is linked to melanin-based coloration in Barn Owls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlWisLc%3D&md5=bf29d170e2af3bc2da11cee1265461c7CAS | 18413149PubMed |
Almasi, B., Rettenbacher, S., Müller, C., Brill, S., Wagner, H., and Jenni, L. (2012). Maternal corticosterone is transferred into the egg yolk. General and Comparative Endocrinology 178, 139–144.
| Maternal corticosterone is transferred into the egg yolk.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpsV2qsro%3D&md5=ffd7202c4b077bc8d54c087c992b2c8aCAS | 22580154PubMed |
Alonso-Alvarez, C., Bertrand, S., Faivre, B., and Sorci, G. (2007). Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in Zebra Finches. Functional Ecology 21, 873–879.
| Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in Zebra Finches.Crossref | GoogleScholarGoogle Scholar |
Arendt, J. D. (1997). Adaptive intrinsic growth rates: an integration across taxa. Quarterly Review of Biology 72, 149–177.
| Adaptive intrinsic growth rates: an integration across taxa.Crossref | GoogleScholarGoogle Scholar |
Arnold, K. E., Griffiths, R., Stevens, D. J., Orr, K. J., Adam, A., and Houston, D. C. (2003). Subtle manipulation of egg sex ratio in birds. Proceedings of the Royal Society B: Biological Sciences 270, S216–S219.
| Subtle manipulation of egg sex ratio in birds.Crossref | GoogleScholarGoogle Scholar | 14667387PubMed |
Banerjee, S. B., and Adkins-Regan, E. (2011). Effect of isolation and conspecific presence in a novel environment on corticosterone concentrations in a social avian species, the Zebra Finch (Taeniopygia guttata). Hormones and Behavior 60, 233–238.
| Effect of isolation and conspecific presence in a novel environment on corticosterone concentrations in a social avian species, the Zebra Finch (Taeniopygia guttata).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptlSrsbg%3D&md5=6e6f9f4caa3ac38dd8e33e897392cbc1CAS | 21704627PubMed |
Banerjee, S. B., Arterbery, A. S., Fergus, D. J., and Adkins-Regan, E. (2011). Deprivation of maternal care has long-lasting consequences for the hypothalamic–pituitary–adrenal axis of Zebra Finches. Proceedings of the Royal Society B: Biological Sciences 279, 759–766.
| Deprivation of maternal care has long-lasting consequences for the hypothalamic–pituitary–adrenal axis of Zebra Finches.Crossref | GoogleScholarGoogle Scholar | 21775332PubMed |
Bates, D., and Sarkar, D. (2007). lme4: linear mixed-effects models using S4 classes. R package version 0.99875–6.
Baumgartner, A. P., and Chrisman, C. L. (1987). Embryonic mortality caused by maternal heat stress during mouse oocyte maturation. Animal Reproduction Science 14, 309–316.
| Embryonic mortality caused by maternal heat stress during mouse oocyte maturation.Crossref | GoogleScholarGoogle Scholar |
Birkhead, T. R., Hall, J., Schut, E., and Hemmings, N. (2008). Unhatched eggs: methods for discriminating between infertility and early embryo mortality. Ibis 150, 508–517.
| Unhatched eggs: methods for discriminating between infertility and early embryo mortality.Crossref | GoogleScholarGoogle Scholar |
Bonier, F., Martin, P. R., and Wingfield, J. C. (2007). Maternal corticosteroids influence primary offspring sex ratio in a free-ranging passerine bird. Behavioral Ecology 18, 1045–1050.
| Maternal corticosteroids influence primary offspring sex ratio in a free-ranging passerine bird.Crossref | GoogleScholarGoogle Scholar |
Bradbury, R. B., and Blakey, J. K. (1998). Diet, maternal condition, and offspring sex ratio in the Zebra Finch, Poephila guttata. Proceedings of the Royal Society B: Biological Sciences 265, 895–899.
| Diet, maternal condition, and offspring sex ratio in the Zebra Finch, Poephila guttata.Crossref | GoogleScholarGoogle Scholar |
Brunton, P. J., and Russell, J. A. (2010). Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: sex-specific effects. Journal of Neuroendocrinology 22, 258–271.
| Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: sex-specific effects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktFOnsLY%3D&md5=0fd6b694ed65ac6e176d254d40e3148aCAS | 20136688PubMed |
Carere, C., Groothuis, T. G. G., Möstl, E., Daan, S., and Koolhaas, J. M. (2003). Fecal corticosteroids in a territorial bird selected for different personalities: daily rhythm and the response to social stress. Hormones and Behavior 43, 540–548.
| Fecal corticosteroids in a territorial bird selected for different personalities: daily rhythm and the response to social stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksVGmtr0%3D&md5=b83e9532410b81ff8f7ebe7c6f58f588CAS | 12799170PubMed |
Casolini, P., Cigliana, G., Alemà, G. S., Ruggieri, V., Angelucci, L., and Catalani, A. (1997). Effect of increased maternal corticosterone during lactation on hippocampal corticosteroid receptors, stress response and learning in offspring in the early stages of life. Neuroscience 79, 1005–1012.
| Effect of increased maternal corticosterone during lactation on hippocampal corticosteroid receptors, stress response and learning in offspring in the early stages of life.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXksVCktLk%3D&md5=aeb7f069d834705dc8db1e749dd03c22CAS | 9219963PubMed |
Charnov, E. L. (1982). ‘The Theory of Sex Allocation.’ (Princeton University Press: Princeton, NJ.)
Coslovsky, M., and Richner, H. (2011). Predation risk affects offspring growth via maternal effects. Functional Ecology 25, 878–888.
| Predation risk affects offspring growth via maternal effects.Crossref | GoogleScholarGoogle Scholar |
Criscuolo, F., Monaghan, P., Nasir, L., and Metcalfe, N. B. (2008). Early nutrition and phenotypic development: ‘catch-up’ growth leads to elevated metabolic rate in adulthood. Proceedings of the Royal Society B: Biological Sciences 275, 1565–1570.
| Early nutrition and phenotypic development: ‘catch-up’ growth leads to elevated metabolic rate in adulthood.Crossref | GoogleScholarGoogle Scholar | 18397870PubMed |
Criscuolo, F., Monaghan, P., Proust, A., Škorpilová, J., Laurie, J., and Metcalfe, N. (2011). Costs of compensation: effect of early life conditions and reproduction on flight performance in Zebra Finches. Oecologia 167, 315–323.
| Costs of compensation: effect of early life conditions and reproduction on flight performance in Zebra Finches.Crossref | GoogleScholarGoogle Scholar | 21472417PubMed |
Cyr, N. E., and Romero, L. M. (2007). Chronic stress in free-living European Starlings reduces corticosterone concentrations and reproductive success. General and Comparative Endocrinology 151, 82–89.
| Chronic stress in free-living European Starlings reduces corticosterone concentrations and reproductive success.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitFeks7w%3D&md5=9a2f2d15c9879fcd74692c17ec575c4aCAS | 17280663PubMed |
De Fraipont, M., Clobert, J., John-Alder, H., and Meylan, S (2000). Increased pre-natal maternal corticosterone promotes philopatry of offspring in Common Lizards Lacerta vivipara. Journal of Animal Ecology 69, 404–413.
| Increased pre-natal maternal corticosterone promotes philopatry of offspring in Common Lizards Lacerta vivipara.Crossref | GoogleScholarGoogle Scholar |
Denver, R. J. (2009). Structural and functional evolution of vertebrate neuroendocrine stress systems. Annals of the New York Academy of Sciences 1163, 1–16.
| Structural and functional evolution of vertebrate neuroendocrine stress systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvVSqurk%3D&md5=21320b56d6df16d7dffbbb80eca15596CAS | 19456324PubMed |
Ellegren, H., and Fridolfsson, A.-K. (1997). Male-driven evolution of DNA sequences in birds. Nature Genetics 17, 182–184.
| Male-driven evolution of DNA sequences in birds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmsFant7c%3D&md5=1b643940bb4810dbde6fee8644345833CAS | 9326938PubMed |
Ellenberg, U., Setiawan, A. N., Cree, A., Houston, D. M., and Seddon, P. J. (2007). Elevated hormonal stress response and reduced reproductive output in Yellow-eyed Penguins exposed to unregulated tourism. General and Comparative Endocrinology 152, 54–63.
| Elevated hormonal stress response and reduced reproductive output in Yellow-eyed Penguins exposed to unregulated tourism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFOitrg%3D&md5=1e2fb8ab7402ab22f606eb89e7e2a7edCAS | 17400221PubMed |
Eriksen, M. S., Haug, A., Torjesen, P. A., and Bakken, M. (2003). Prenatal exposure to corticosterone impairs embryonic development and increases fluctuating asymmetry in Chickens (Gallus gallus domesticus). British Poultry Science 44, 690–697.
| Prenatal exposure to corticosterone impairs embryonic development and increases fluctuating asymmetry in Chickens (Gallus gallus domesticus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvV2guw%3D%3D&md5=187a1e74bd0e1895ddc0728bf722d425CAS | 14965089PubMed |
Eriksen, M. S., Bakken, M., Espmark, Å., Braastad, B. O., and Salte, R. (2006). Prespawning stress in farmed Atlantic Salmon Salmo salar: maternal cortisol exposure and hyperthermia during embryonic development affect offspring survival, growth and incidence of malformations. Journal of Fish Biology 69, 114–129.
| Prespawning stress in farmed Atlantic Salmon Salmo salar: maternal cortisol exposure and hyperthermia during embryonic development affect offspring survival, growth and incidence of malformations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptVKnurs%3D&md5=660068efb4b87b87aecebe9eedc7a044CAS |
Fisher, M. O., Nager, R. G., and Monaghan, P. (2006). Compensatory growth impairs adult cognitive performance. PLoS Biology 4, e251.
| Compensatory growth impairs adult cognitive performance.Crossref | GoogleScholarGoogle Scholar | 16834460PubMed |
Gagliano, M., and McCormick, M. (2009). Hormonally mediated maternal effects shape offspring survival potential in stressful environments. Oecologia 160, 657–665.
| Hormonally mediated maternal effects shape offspring survival potential in stressful environments.Crossref | GoogleScholarGoogle Scholar | 19352712PubMed |
Gam, A. E., Mendonça, M. T., and Navara, K. J. (2011). Acute corticosterone treatment prior to ovulation biases offspring sex ratios towards males in Zebra Finches Taeniopygia guttata. Journal of Avian Biology 42, 253–258.
| Acute corticosterone treatment prior to ovulation biases offspring sex ratios towards males in Zebra Finches Taeniopygia guttata.Crossref | GoogleScholarGoogle Scholar |
Gorman, H. E., and Nager, R. G. (2004). Prenatal developmental conditions have long-term effects on offspring fecundity. Proceedings of the Royal Society B: Biological Sciences 271, 1923–1928.
| Prenatal developmental conditions have long-term effects on offspring fecundity.Crossref | GoogleScholarGoogle Scholar | 15347515PubMed |
Groscolas, R., Lacroix, A., and Robin, J.-P. (2008). Spontaneous egg or chick abandonment in energy-depleted King Penguins: a role for corticosterone and prolactin? Hormones and Behavior 53, 51–60.
| Spontaneous egg or chick abandonment in energy-depleted King Penguins: a role for corticosterone and prolactin?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1ymuw%3D%3D&md5=cf26bcc8b8ec4009fc61fb18268714ebCAS | 17920597PubMed |
Haussmann, M. F., Longenecker, A. S., Marchetto, N. M., Juliano, S. A., and Bowden, R. M. (2012). Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length. Proceedings of the Royal Society B: Biological Sciences 279, 1447–1456.
| Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvFGrtbc%3D&md5=bc84284482fee23ff472e478ffb4b8e8CAS | 22072607PubMed |
Hayward, L. S., and Wingfield, J. C. (2004). Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. General and Comparative Endocrinology 135, 365–371.
| Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtVCitA%3D%3D&md5=92e672e12ae8ba763b6be67d9d0534bfCAS | 14723888PubMed |
Hayward, L., Satterlee, D., and Wingfield, J. (2005). Japanese Quail selected for high plasma corticosterone response deposit high levels of corticosterone in their eggs. Physiological and Biochemical Zoology 78, 1026–1031.
| Japanese Quail selected for high plasma corticosterone response deposit high levels of corticosterone in their eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlWhu7rK&md5=f1817fd800bb07beeef80345ba1a541fCAS | 16228941PubMed |
Hayward, L. S., Richardson, J. B., Grogan, M. N., and Wingfield, J. C. (2006). Sex differences in the organizational effects of corticosterone in the egg yolk of quail. General and Comparative Endocrinology 146, 144–148.
| Sex differences in the organizational effects of corticosterone in the egg yolk of quail.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xit1CitLg%3D&md5=ce08be9dcaf228252ef16bd1e0a48fc9CAS | 16430891PubMed |
Haywood, S., and Perrins, C. M. (1992). Is clutch size in birds affected by environmental conditions during growth? Proceedings of the Royal Society B: Biological Sciences 249, 195–197.
| Is clutch size in birds affected by environmental conditions during growth?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s%2FoslGqtQ%3D%3D&md5=f80e73338069876cbea2ba5d2fd3b519CAS | 1360680PubMed |
Henriksen, R., Rettenbacher, S., and Groothuis, T. G. G. (2013). Maternal corticosterone elevation during egg formation in Chickens (Gallus gallus domesticus) influences offspring traits, partly via prenatal undernutrition. General and Comparative Endocrinology 191, 83–91.
| Maternal corticosterone elevation during egg formation in Chickens (Gallus gallus domesticus) influences offspring traits, partly via prenatal undernutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlWjtbbM&md5=2e15ea8984a289eb6f27756c0da26bfeCAS | 23791762PubMed |
Janczak, A. M., Braastad, B. O., and Bakken, M. (2006). Behavioural effects of embryonic exposure to corticosterone in Chickens. Applied Animal Behaviour Science 96, 69–82.
| Behavioural effects of embryonic exposure to corticosterone in Chickens.Crossref | GoogleScholarGoogle Scholar |
Khan, N., and Robert, K. (2013). Does sex matter? Differential responses to corticosterone administration in the Zebra Finch. Zoology (Jena, Germany) 116, 293–299.
| Does sex matter? Differential responses to corticosterone administration in the Zebra Finch.Crossref | GoogleScholarGoogle Scholar |
Kilner, R. (1998). Primary and secondary sex ratio manipulation by Zebra Finches. Animal Behaviour 56, 155–164.
| Primary and secondary sex ratio manipulation by Zebra Finches.Crossref | GoogleScholarGoogle Scholar | 9710473PubMed |
Kitaysky, A. S., Wingfield, J. C., and Piatt, J. F. (1999). Dynamics of food availability, body condition and physiological stress response in breeding Black-legged Kittiwakes. Functional Ecology 13, 577–584.
| Dynamics of food availability, body condition and physiological stress response in breeding Black-legged Kittiwakes.Crossref | GoogleScholarGoogle Scholar |
Kitaysky, A. S., Wingfield, J. C., and Piatt, J. F. (2001). Corticosterone facilitates begging and affects resource allocation in the Black-legged Kittiwake. Behavioral Ecology 12, 619–625.
| Corticosterone facilitates begging and affects resource allocation in the Black-legged Kittiwake.Crossref | GoogleScholarGoogle Scholar |
Kitaysky, A. S., Kitaiskaia, E. V., Piatt, J. F., and Wingfield, J. C. (2003). Benefits and costs of increased levels of corticosterone in seabird chicks. Hormones and Behavior 43, 140–149.
| Benefits and costs of increased levels of corticosterone in seabird chicks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsVCgtLc%3D&md5=a3589cb06e01faf969436caba1b5e112CAS | 12614644PubMed |
Koenig, J. I., Elmer, G. I., Shepard, P. D., Lee, P. R., Mayo, C., Joy, B., Hercher, E., and Brady, D. L. (2005). Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia. Behavioural Brain Research 156, 251–261.
| Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia.Crossref | GoogleScholarGoogle Scholar | 15582111PubMed |
Krause, E. T., and Naguib, M. (2011). Compensatory growth affects exploratory behaviour in Zebra Finches, Taeniopygia guttata. Animal Behaviour 81, 1295–1300.
| Compensatory growth affects exploratory behaviour in Zebra Finches, Taeniopygia guttata.Crossref | GoogleScholarGoogle Scholar |
Lattin, C. R., Bauer, C. M., de Bruijn, R., and Michael Romero, L. (2012). Hypothalamus–pituitary–adrenal axis activity and the subsequent response to chronic stress differ depending upon life history stage. General and Comparative Endocrinology 178, 494–501.
| Hypothalamus–pituitary–adrenal axis activity and the subsequent response to chronic stress differ depending upon life history stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Glu7rM&md5=3c2c3da1cd306d976d5a95ea22fd8a40CAS | 22841762PubMed |
Loiseau, C., Sorci, G., Dano, S., and Chastel, O. (2008). Effects of experimental increase of corticosterone levels on begging behavior, immunity and parental provisioning rate in House Sparrows. General and Comparative Endocrinology 155, 101–108.
| Effects of experimental increase of corticosterone levels on begging behavior, immunity and parental provisioning rate in House Sparrows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlGiurbI&md5=6178884d5f9c13f72ff570d0e009d930CAS | 17448473PubMed |
Love, O. P., and Williams, T. D. (2008). The adaptive value of stress‐induced phenotypes: effects of maternally derived corticosterone on sex‐biased investment, cost of reproduction, and maternal fitness. American Naturalist 172, E135–E149.
| The adaptive value of stress‐induced phenotypes: effects of maternally derived corticosterone on sex‐biased investment, cost of reproduction, and maternal fitness.Crossref | GoogleScholarGoogle Scholar | 18793091PubMed |
Love, O. P., Breuner, C. W., Vézina, F., and Williams, T. D. (2004). Mediation of a corticosterone-induced reproductive conflict. Hormones and Behavior 46, 59–65.
| Mediation of a corticosterone-induced reproductive conflict.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlt1emt70%3D&md5=7dda4eeb589fe11136a8261449833ffcCAS | 15215043PubMed |
Love, O. P., Chin, E. H., Wynne‐Edwards, K. E., and Williams, T. D. (2005). Stress hormones: a link between maternal condition and sex‐biased reproductive investment. American Naturalist 166, 751–766.
| Stress hormones: a link between maternal condition and sex‐biased reproductive investment.Crossref | GoogleScholarGoogle Scholar | 16475090PubMed |
Mangel, M., and Munch, S. B. (2005). A life‐history perspective on short‐ and long‐term consequences of compensatory growth. American Naturalist 166, E155–E176.
| A life‐history perspective on short‐ and long‐term consequences of compensatory growth.Crossref | GoogleScholarGoogle Scholar | 16475079PubMed |
Martins, T. L. F. (2004). Sex-specific growth rates in Zebra Finch nestlings: a possible mechanism for sex ratio adjustment. Behavioral Ecology 15, 174–180.
| Sex-specific growth rates in Zebra Finch nestlings: a possible mechanism for sex ratio adjustment.Crossref | GoogleScholarGoogle Scholar |
McCormick, M. I. (1999). Experimental test of the effect of maternal hormones on larval quality of a coral reef fish. Oecologia 118, 412–422.
| Experimental test of the effect of maternal hormones on larval quality of a coral reef fish.Crossref | GoogleScholarGoogle Scholar |
McCormick, M. I. (2006). Mothers matter: crowding leads to stressed mothers and smaller offspring in marine fish. Ecology 87, 1104–1109.
| Mothers matter: crowding leads to stressed mothers and smaller offspring in marine fish.Crossref | GoogleScholarGoogle Scholar | 16761587PubMed |
Metcalfe, N. B., and Monaghan, P. (2001). Compensation for a bad start: grow now, pay later? Trends in Ecology & Evolution 16, 254–260.
| Compensation for a bad start: grow now, pay later?Crossref | GoogleScholarGoogle Scholar |
Metcalfe, N. B., and Monaghan, P. (2003). Growth versus lifespan: perspectives from evolutionary ecology. Experimental Gerontology 38, 935–940.
| Growth versus lifespan: perspectives from evolutionary ecology.Crossref | GoogleScholarGoogle Scholar | 12954479PubMed |
Müller, C., Jenni-Eiermann, S., and Jenni, L. (2009). Effects of a short period of elevated circulating corticosterone on postnatal growth in free-living Eurasian Kestrels Falco tinnunculus. Journal of Experimental Biology 212, 1405–1412.
| Effects of a short period of elevated circulating corticosterone on postnatal growth in free-living Eurasian Kestrels Falco tinnunculus.Crossref | GoogleScholarGoogle Scholar | 19376961PubMed |
Müllner, A., Eduard Linsenmair, K., and Wikelski, M. (2004). Exposure to ecotourism reduces survival and affects stress response in Hoatzin chicks (Opisthocomus hoazin). Biological Conservation 118, 549–558.
| Exposure to ecotourism reduces survival and affects stress response in Hoatzin chicks (Opisthocomus hoazin).Crossref | GoogleScholarGoogle Scholar |
Naguib, M., and Gil, D. (2005). Transgenerational effects on body size caused by early developmental stress in Zebra Finches. Biology Letters 1, 95–97.
| Transgenerational effects on body size caused by early developmental stress in Zebra Finches.Crossref | GoogleScholarGoogle Scholar | 17148137PubMed |
Ouyang, J. Q., Quetting, M., and Hau, M. (2012). Corticosterone and brood abandonment in a passerine bird. Animal Behaviour 84, 261–268.
| Corticosterone and brood abandonment in a passerine bird.Crossref | GoogleScholarGoogle Scholar |
Pianka, E. R. (1970). On r- and K-selection. American Naturalist 104, 592–597.
| On r- and K-selection.Crossref | GoogleScholarGoogle Scholar |
Pike, T. W., and Petrie, M. (2005). Maternal body condition and plasma hormones affect offspring sex ratio in Peafowl. Animal Behaviour 70, 745–751.
| Maternal body condition and plasma hormones affect offspring sex ratio in Peafowl.Crossref | GoogleScholarGoogle Scholar |
Pike, T. W., and Petrie, M. (2006). Experimental evidence that corticosterone affects offspring sex ratios in quail. Proceedings of the Royal Society B: Biological Sciences 273, 1093–1098.
| Experimental evidence that corticosterone affects offspring sex ratios in quail.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht12mtr7P&md5=d4d9bf34ab59399ceb32f449057ba4e7CAS | 16600886PubMed |
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., and R Core Team (2013). nlme: linear and nonlinear mixed effects models. Version 3.1-111. Available at http://CRAN.R-project.org/package=nlme [Verified 11 February 2016].
Pinson, S. E., Parr, C. M., Wilson, J. L., and Navara, K. J. (2011). Acute corticosterone administration during meiotic segregation stimulates females to produce more male offspring. Physiological and Biochemical Zoology 84, 292–298.
| Acute corticosterone administration during meiotic segregation stimulates females to produce more male offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFSgs7c%3D&md5=490cf2423bcbde03721b8c4ac9cc01a0CAS | 21527820PubMed |
Potvin, D. A., and MacDougall‐Shackleton, S. A. (2015). Traffic noise affects embryo mortality and nestling growth rates in captive Zebra Finches. Journal of Experimental Zoology A: Ecological Genetics and Physiology 323, 722–730.
| Traffic noise affects embryo mortality and nestling growth rates in captive Zebra Finches.Crossref | GoogleScholarGoogle Scholar |
Pravosudov, V. V., Kitaysky, A. S., Wingfield, J. C., and Clayton, N. S. (2001). Long-term unpredictable foraging conditions and physiological stress response in Mountain Chickadees (Poecile gambeli). General and Comparative Endocrinology 123, 324–331.
| Long-term unpredictable foraging conditions and physiological stress response in Mountain Chickadees (Poecile gambeli).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntlWqsbs%3D&md5=4ce83b64b3f41e42303b4b5ab08b5b5eCAS | 11589632PubMed |
Ramenofsky, M. (2011). Hormones in migration and reproductive cycles of birds. In ‘Hormones and Reproduction of Vertebrates. Vol. 4’. (Eds D. O. Norris and K. H. Lopez.) pp. XX–XX. (Academic Press: London.)
Rettenbacher, S., Möstl, E., Hackl, R., and Palme, R. (2005). Corticosterone in Chicken eggs. Annals of the New York Academy of Sciences 1046, 193–203.
| Corticosterone in Chicken eggs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWjtLzL&md5=d8ddf39626101f6cfa42eac88f6ab400CAS | 16055852PubMed |
Robert, K., Vleck, C. M., and Bronikowski, A. M. (2009). The effects of maternal corticosterone levels on offspring behaviour in fast- and slow-growth Garter Snakes (Thamnophis elegans). Hormones and Behavior 55, 24–32.
| The effects of maternal corticosterone levels on offspring behaviour in fast- and slow-growth Garter Snakes (Thamnophis elegans).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvF2hsg%3D%3D&md5=1e96e878d793728bdd4b42e40291b633CAS | 18721809PubMed |
Rollo, C. D. (2002). Growth negatively impacts the life span of mammals. Evolution & Development 4, 55–61.
| Growth negatively impacts the life span of mammals.Crossref | GoogleScholarGoogle Scholar |
Romero, L. M., and Romero, R. C. (2002). Corticosterone responses in wild birds: the importance of rapid initial sampling. Condor 104, 129–135.
| Corticosterone responses in wild birds: the importance of rapid initial sampling.Crossref | GoogleScholarGoogle Scholar |
Romero, L. M., Strochlic, D., and Wingfield, J. C. (2005). Corticosterone inhibits feather growth: potential mechanism explaining seasonal down regulation of corticosterone during molt. Comparative Biochemistry and Physiology A: Molecular & Integrative Physiology 142, 65–73.
| Corticosterone inhibits feather growth: potential mechanism explaining seasonal down regulation of corticosterone during molt.Crossref | GoogleScholarGoogle Scholar |
Rubolini, D., Romano, M., Boncoraglio, G., Ferrari, R. P., Martinelli, R., Galeotti, P., Fasola, M., and Saino, N. (2005). Effects of elevated egg corticosterone levels on behavior, growth, and immunity of Yellow-legged Gull (Larus michahellis) chicks. Hormones and Behavior 47, 592–605.
| Effects of elevated egg corticosterone levels on behavior, growth, and immunity of Yellow-legged Gull (Larus michahellis) chicks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivF2jsLw%3D&md5=887b33a53bf7dfa911df1c1aa4a6fe48CAS | 15811362PubMed |
Rutkowska, J., and Cichon, M. (2002). Maternal investment during egg laying and offspring sex: an experimental study of Zebra Finches. Animal Behaviour 64, 817–822.
| Maternal investment during egg laying and offspring sex: an experimental study of Zebra Finches.Crossref | GoogleScholarGoogle Scholar |
Rutkowska, J., and Cichon, M. (2006). Maternal testosterone affects the primary sex ratio and offspring survival in Zebra Finches. Animal Behaviour 71, 1283–1288.
| Maternal testosterone affects the primary sex ratio and offspring survival in Zebra Finches.Crossref | GoogleScholarGoogle Scholar |
Rutstein, A. N., Slater, P. J. B., and Graves, J. A. (2004). Diet quality and resource allocation in the zebra finch. Proceedings of the Royal Society B: Biological Sciences 271, S286–S289.
| Diet quality and resource allocation in the zebra finch.Crossref | GoogleScholarGoogle Scholar | 15503996PubMed |
Saino, N., Romano, M., Ferrari, R. P., Martinelli, R., and Møller, A. P. (2005). Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring. Journal of Experimental Zoology A: Comparative Experimental Biology 303A, 998–1006.
| Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1ensrbL&md5=34e5266834bc299f72866ce2d15cebdfCAS |
Salvante, K. G., and Williams, T. D. (2003). Effects of corticosterone on the proportion of breeding females, reproductive output and yolk precursor levels. General and Comparative Endocrinology 130, 205–214.
| Effects of corticosterone on the proportion of breeding females, reproductive output and yolk precursor levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsVCgtro%3D&md5=9ae84851714e97fb578566bd992db7b4CAS | 12606263PubMed |
Satterlee, D. G., Cole, C. A., and Castille, S. A. (2007). Maternal corticosterone further reduces the reproductive function of male offspring hatched from eggs laid by quail hens selected for exaggerated adrenocortical stress responsiveness. Poultry Science 86, 572–581.
| Maternal corticosterone further reduces the reproductive function of male offspring hatched from eggs laid by quail hens selected for exaggerated adrenocortical stress responsiveness.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s%2FpvVantg%3D%3D&md5=c5b155d5907b14c236fbd9792d55a454CAS | 17297171PubMed |
Schneider, M. L., Roughton, E. C., Koehler, A. J., and Lubach, G. R. (1999). Growth and development following prenatal stress exposure in primates: an examination of ontogenetic vulnerability. Child Development 70, 263–274.
| Growth and development following prenatal stress exposure in primates: an examination of ontogenetic vulnerability.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M3jsVykug%3D%3D&md5=42356db3dc02243606f024348623bb91CAS | 10218255PubMed |
Sheriff, M. J., Krebs, C. J., and Boonstra, R. (2009). The sensitive hare: sublethal effects of predator stress on reproduction in Snowshoe Hares. Journal of Animal Ecology 78, 1249–1258.
| The sensitive hare: sublethal effects of predator stress on reproduction in Snowshoe Hares.Crossref | GoogleScholarGoogle Scholar | 19426257PubMed |
Silverin, B. (1986). Corticosterone-binding proteins and behavioral effects of high plasma levels of corticosterone during the breeding period in the Pied Flycatcher. General and Comparative Endocrinology 64, 67–74.
| Corticosterone-binding proteins and behavioral effects of high plasma levels of corticosterone during the breeding period in the Pied Flycatcher.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xls12gt7o%3D&md5=492a2e814d24fc5fea56ae9ae93fde62CAS | 3557081PubMed |
Southwood, T. R. E., May, R. M., Hassell, M. P., and Conway, G. R. (1974). Ecological strategies and population parameters. American Naturalist 108, 791–804.
| Ecological strategies and population parameters.Crossref | GoogleScholarGoogle Scholar |
Spée, M., Beaulieu, M., Dervaux, A., Chastel, O., Le Maho, Y., and Raclot, T. (2010). Should I stay or should I go? Hormonal control of nest abandonment in a long-lived bird, the Adélie Penguin. Hormones and Behavior 58, 762–768.
| Should I stay or should I go? Hormonal control of nest abandonment in a long-lived bird, the Adélie Penguin.Crossref | GoogleScholarGoogle Scholar | 20691185PubMed |
Spée, M., Marchal, L., Lazin, D., Le Maho, Y., Chastel, O., Beaulieu, M., and Raclot, T. (2011). Exogenous corticosterone and nest abandonment: a study in a long-lived bird, the Adélie Penguin. Hormones and Behavior 60, 362–370.
| Exogenous corticosterone and nest abandonment: a study in a long-lived bird, the Adélie Penguin.Crossref | GoogleScholarGoogle Scholar | 21763694PubMed |
Spencer, K. A., and Verhulst, S. (2007). Delayed behavioral effects of postnatal exposure to corticosterone in the Zebra Finch (Taeniopygia guttata). Hormones and Behavior 51, 273–280.
| Delayed behavioral effects of postnatal exposure to corticosterone in the Zebra Finch (Taeniopygia guttata).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltVWhsQ%3D%3D&md5=719a7d77a741b08c403490e9cfeff581CAS | 17196201PubMed |
Spencer, K. A., and Verhulst, S. (2008). Post-natal exposure to corticosterone affects standard metabolic rate in the Zebra Finch (Taeniopygia guttata). General and Comparative Endocrinology 159, 250–256.
| Post-natal exposure to corticosterone affects standard metabolic rate in the Zebra Finch (Taeniopygia guttata).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVSjsrbF&md5=6603a22dcf8ea2af16112c64ead0d440CAS | 18854187PubMed |
Spencer, K. A., Buchanan, K. L., Goldsmith, A. R., and Catchpole, C. K. (2003). Song as an honest signal of developmental stress in the Zebra Finch (Taeniopygia guttata). Hormones and Behavior 44, 132–139.
| Song as an honest signal of developmental stress in the Zebra Finch (Taeniopygia guttata).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3svjsFemtQ%3D%3D&md5=7a7e8717712383163fad396eb3af6cecCAS | 13129485PubMed |
Thierry, A.-M., Massemin, S., Handrich, Y., and Raclot, T. (2013a). Elevated corticosterone levels and severe weather conditions decrease parental investment of incubating Adélie Penguins. Hormones and Behavior 63, 475–483.
| Elevated corticosterone levels and severe weather conditions decrease parental investment of incubating Adélie Penguins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXovFCjsg%3D%3D&md5=e52f82dc7bd66c1d65f7aeb0c2dbbe09CAS | 23291423PubMed |
Thierry, A.-M., Ropert-Coudert, Y., and Raclot, T. (2013b). Elevated corticosterone levels decrease reproductive output of chick-rearing Adélie Penguins but do not affect chick mass at fledging. Conservation Physiology 1, cot007.
| Elevated corticosterone levels decrease reproductive output of chick-rearing Adélie Penguins but do not affect chick mass at fledging.Crossref | GoogleScholarGoogle Scholar |
Thompson, L. U., Boucher, B. A., Liu, Z., Cotterchio, M., and Kreiger, N. (2006). Phytoestrogen content of foods consumed in Canada, including isoflavones, lignans, and coumestan. Nutrition and Cancer 54, 184–201.
| Phytoestrogen content of foods consumed in Canada, including isoflavones, lignans, and coumestan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvFOluro%3D&md5=09a22ed62e647dc0a46fd8c15797bfb7CAS | 16898863PubMed |
Trivers, R. L., and Willard, D. E. (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science 179, 90–92.
| Natural selection of parental ability to vary the sex ratio of offspring.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3s%2Fls1Wqsg%3D%3D&md5=52874b3b9b0a847bb4f70a567bf5af99CAS | 4682135PubMed |
Vercken, E., de Fraipont, M., Dufty, A. M., and Clobert, J. (2007). Mother’s timing and duration of corticosterone exposure modulate offspring size and natal dispersal in the Common Lizard (Lacerta vivipara). Hormones and Behavior 51, 379–386.
| Mother’s timing and duration of corticosterone exposure modulate offspring size and natal dispersal in the Common Lizard (Lacerta vivipara).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXis1Okt78%3D&md5=d1ce004a668862977f5e5b9d351e2620CAS | 17274995PubMed |
Weinstock, M., Matlina, E., Maor, G. I., Rosen, H., and McEwen, B. S. (1992). Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat. Brain Research 595, 195–200.
| Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhs1Gltw%3D%3D&md5=0b2d063078ab370cb72cb68349c5a98aCAS | 1467966PubMed |
Wikelski, M., and Cooke, S. J. (2006). Conservation physiology. Trends in Ecology & Evolution 21, 38–46.
| Conservation physiology.Crossref | GoogleScholarGoogle Scholar |
Wilson, P. N., and Osbourn, D. F. (1960). Compensatory growth after undernutrition in mammals and birds. Biological Reviews of the Cambridge Philosophical Society 35, 324–361.
| Compensatory growth after undernutrition in mammals and birds.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF3c7gsF2ltw%3D%3D&md5=c8d6344e22a1f3305b99e1ff109a8ea5CAS | 13785698PubMed |
Wingfield, J. C., and Kitaysky, A. S. (2002). Endocrine responses to unpredictable environmental events: stress or anti-stress hormones? Integrative and Comparative Biology 42, 600–609.
| Endocrine responses to unpredictable environmental events: stress or anti-stress hormones?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFyhsb0%3D&md5=dc66fbc8726935ce7661390891db24c0CAS | 21708756PubMed |
Wingfield, J. C., and Sapolsky, R. M. (2003). Reproduction and resistance to stress: when and how. Journal of Neuroendocrinology 15, 711–724.
| Reproduction and resistance to stress: when and how.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVOqtLw%3D&md5=62706f0cb157ee3f44786cfd4e216870CAS | 12834431PubMed |
Wingfield, J., Hunt, K., Breuner, C., Dunlap, K., Fowler, G., Freed, L., and Lepson, J. (1997). Environmental stress, field endocrinology, and conservation biology. In ‘Behavioral Approaches to Conservation in the Wild’. (Eds J. R. Clemmons and R. Buchholz.) pp. 95–131. (Cambridge University Press: Cambridge, UK)
Wingfield, J. C., Maney, D., Breuner, C. W., Jacobs, J., Lynn, S., Ramenofsky, M., and Richardson, R. (1998). Ecological bases of hormone–behavior interactions: the “emergency life history stage”. American Zoologist 38, 191–206.
| Ecological bases of hormone–behavior interactions: the “emergency life history stage”.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXislCjtbc%3D&md5=d159e81f764a8ce63c40be7e09d29d3aCAS |
Yearsley, J. M., Kyriazakis, I., and Gordon, I. J. (2004). Delayed costs of growth and compensatory growth rates. Functional Ecology 18, 563–570.
| Delayed costs of growth and compensatory growth rates.Crossref | GoogleScholarGoogle Scholar |