Social environment during egg laying. Changes in plasma hormones with no consequences for yolk hormones or fecundity in female Japanese quail, Coturnix japonica

Langen E, von Engelhardt N, Goerlich-Jansson V (2017)
PLOS ONE 12(5): e0176146.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
OA 2.02 MB
Langen, EstherUniBi; von Engelhardt, Nikolaus ; Goerlich-Jansson, Vivian
Abstract / Bemerkung
The social environment can have profound effects on an individual’s physiology and behaviour and on the transfer of resources to the next generation, with potential consequences for fecundity and reproduction. However, few studies investigate all of these aspects at once. The present study housed female Japanese quail (Coturnix japonica) in pairs or groups to examine the effects on hormone concentrations in plasma and yolk and on reproductive performance. Circulating levels of androgens (testosterone and 5-α-dihydrotestosterone) and corticosterone were measured in baseline samples and after standardised challenges to assess the responsiveness of the females’ endocrine axes. Effects of the social environment on female fecundity were analysed by measuring egg production, egg mass, fertilization rates, and number of hatched offspring. Counter to expectation, females housed in pairs had higher plasma androgen concentrations and slightly higher corticosterone concentrations than females housed in groups, although the latter was not statistically significant. Pair vs. group housing did not affect the females’ hormonal response to standardised challenges or yolk testosterone levels. In contrast to previous studies, the females’ androgen response to a gonadotropin-releasing hormone challenge was not related to yolk testosterone levels. Non-significant trends emerged for pair-housed females to have higher egg-laying rates and higher fertility, but no differences arose in egg weight or in the number, weight or size of hatchlings. We propose that our unexpected findings are due to differences in the adult sex ratio in our social treatments. In pairs, the male may stimulate female circulating hormone levels more strongly than in groups where effects are diluted due to the presence of several females. Future studies should vary both group size and sex composition to disentangle the significance of sexual, competitive and affiliative social interactions for circulating and yolk hormone levels, and their consequences for subsequent generations.
Open-Access-Publikationskosten wurden durch die Deutsche Forschungsgemeinschaft und die Universität Bielefeld gefördert.
Page URI


Langen E, von Engelhardt N, Goerlich-Jansson V. Social environment during egg laying. Changes in plasma hormones with no consequences for yolk hormones or fecundity in female Japanese quail, Coturnix japonica. PLOS ONE. 2017;12(5): e0176146.
Langen, E., von Engelhardt, N., & Goerlich-Jansson, V. (2017). Social environment during egg laying. Changes in plasma hormones with no consequences for yolk hormones or fecundity in female Japanese quail, Coturnix japonica. PLOS ONE, 12(5), e0176146. doi:10.1371/journal.pone.0176146
Langen, Esther, von Engelhardt, Nikolaus, and Goerlich-Jansson, Vivian. 2017. “Social environment during egg laying. Changes in plasma hormones with no consequences for yolk hormones or fecundity in female Japanese quail, Coturnix japonica”. PLOS ONE 12 (5): e0176146.
Langen, E., von Engelhardt, N., and Goerlich-Jansson, V. (2017). Social environment during egg laying. Changes in plasma hormones with no consequences for yolk hormones or fecundity in female Japanese quail, Coturnix japonica. PLOS ONE 12:e0176146.
Langen, E., von Engelhardt, N., & Goerlich-Jansson, V., 2017. Social environment during egg laying. Changes in plasma hormones with no consequences for yolk hormones or fecundity in female Japanese quail, Coturnix japonica. PLOS ONE, 12(5): e0176146.
E. Langen, N. von Engelhardt, and V. Goerlich-Jansson, “Social environment during egg laying. Changes in plasma hormones with no consequences for yolk hormones or fecundity in female Japanese quail, Coturnix japonica”, PLOS ONE, vol. 12, 2017, : e0176146.
Langen, E., von Engelhardt, N., Goerlich-Jansson, V.: Social environment during egg laying. Changes in plasma hormones with no consequences for yolk hormones or fecundity in female Japanese quail, Coturnix japonica. PLOS ONE. 12, : e0176146 (2017).
Langen, Esther, von Engelhardt, Nikolaus, and Goerlich-Jansson, Vivian. “Social environment during egg laying. Changes in plasma hormones with no consequences for yolk hormones or fecundity in female Japanese quail, Coturnix japonica”. PLOS ONE 12.5 (2017): e0176146.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Creative Commons Namensnennung 4.0 International Public License (CC-BY 4.0):
Access Level
OA Open Access
Zuletzt Hochgeladen
MD5 Prüfsumme

108 References

Daten bereitgestellt von Europe PubMed Central.

Hormones and animal social behavior
E, 2005
The ecology of stress: effects of the social environment
S, Funct Ecol 27(), 2013
Social Modulation of Androgens in Vertebrates: Mechanisms and Function
RF, Adv Study Behav 34(), 2004
LEHRMAN DS., Sci. Am. 211(), 1964
PMID: 14224495
Hormones, developmental plasticity and adaptation
AM, Trends Ecol Evol 17(), 2002
Hormones and life histories: an integrative approach.
Ketterson ED, Nolan V., Am. Nat. 140 Suppl 1(), 1992
PMID: 19426026
The effects of prenatal social stress on behaviour: mechanisms and function.
Kaiser S, Sachser N., Neurosci Biobehav Rev 29(2), 2005
PMID: 15811499
Maternal hormones as a tool to adjust offspring phenotype in avian species.
Groothuis TG, Muller W, von Engelhardt N, Carere C, Eising C., Neurosci Biobehav Rev 29(2), 2005
PMID: 15811503
The adaptive significance of maternal effects.
Mousseau TA, Fox CW., Trends Ecol. Evol. (Amst.) 13(10), 1998
PMID: 21238360
Maternal effects, paternal effects and sexual selection.
Qvarnstrom A, Price TD., Trends Ecol. Evol. (Amst.) 16(2), 2001
PMID: 11165708
The information value of non-genetic inheritance in plants and animals.
English S, Pen I, Shea N, Uller T., PLoS ONE 10(1), 2015
PMID: 25603120
Maternal effects as generators of evolutionary change: a reassessment.
Badyaev AV., Ann. N. Y. Acad. Sci. 1133(), 2008
PMID: 18559819
When is a maternal effect adaptive?
DJ, Oikos 116(), 2007
Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus)
J, Ecol Lett 6(), 2003
Testosterone and group size in cliff swallows: testing the "challenge hypothesis" in a colonial bird.
Smith LC, Raouf SA, Brown MB, Wingfield JC, Brown CR., Horm Behav 47(1), 2005
PMID: 15579268
Nest defence behaviour and testosterone levels in female pied flycatchers
A, Ethology 121(), 2015
Behavioral and physiological responses to experimentally elevated testosterone in female dark-eyed juncos (Junco hyemalis carolinensis).
Zysling DA, Greives TJ, Breuner CW, Casto JM, Demas GE, Ketterson ED., Horm Behav 50(2), 2006
PMID: 16678179
The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies
JC, Am Nat 136(), 1990
Competitive females are successful females; phenotype, mechanism and selection in a common songbird.
Cain KE, Ketterson ED., Behav. Ecol. Sociobiol. (Print) 66(2), 2012
PMID: 22345899
Testosterone in females: mediator of adaptive traits, constraint on sexual dimorphism, or both?
Ketterson ED, Nolan V Jr, Sandell M., Am. Nat. 166 Suppl 4(), 2005
PMID: 16224714
Females competing to reproduce: dominance matters but testosterone may not.
Jawor JM, Young R, Ketterson ED., Horm Behav 49(3), 2005
PMID: 16226754
Seasonality and hormonal control of territorial aggression in female song sparrows (Passeriformes: Emberizidae: Melospiza melodia)
MM, Ethology 106(), 2000
Social status, circulating levels of hormones, and competition for food in winter flocks of the white-throated sparrow
H, Behaviour 107(), 1988
Testosterone might not be necessary to support female aggression in incubating northern cardinals
MS, Anim Behav 107(), 2015
Social buffering of the stress response: diversity, mechanisms, and functions.
Hennessy MB, Kaiser S, Sachser N., Front Neuroendocrinol 30(4), 2009
PMID: 19545584
Glucocorticoid hormone levels increase with group size and parasite load in cliff swallows
SA, Anim Behav 71(), 2006
Dominance rank and cage density effects on performance traits, feeding activity and plasma corticosterone levels of laying hens (Gallus domesticus)
DL, Appl Anim Behav Sci 17(), 1987
Behavioural and physiological effects of population density on domesticated Zebra Finches (Taeniopygia guttata) held in aviaries.
Poot H, ter Maat A, Trost L, Schwabl I, Jansen RF, Gahr M., Physiol. Behav. 105(3), 2011
PMID: 22037197
Social instability in laying quail: consequences on yolk steroids and offspring's phenotype.
Guibert F, Richard-Yris MA, Lumineau S, Kotrschal K, Guemene D, Bertin A, Mostl E, Houdelier C., PLoS ONE 5(11), 2010
PMID: 21124926
Adrenocortical response to mating, social interaction and restraint in the female Japanese quail.
Rutkowska J, Place NJ, Vincent S, Adkins-Regan E., Physiol. Behav. 104(5), 2011
PMID: 21763334
Negative effects of elevated testosterone on female fecundity in zebra finches.
Rutkowska J, Cichon M, Puerta M, Gil D., Horm Behav 47(5), 2005
PMID: 15811361
Maternal testosterone affects the primary sex ratio and offspring survival in zebra finches
J, Anim Behav 71(), 2006
Effects of experimentally sustained elevated testosterone on incubation behaviour and reproductive success in female great tits (Parus major).
de Jong B, Lens L, Amininasab SM, van Oers K, Darras VM, Eens M, Pinxten R, Komdeur J, Groothuis TG., Gen. Comp. Endocrinol. 230-231(), 2016
PMID: 26996426
Do female red-winged blackbirds limit their own breeding densities?
WA, Ecology 69(), 1988
Exogenous testosterone increases female aggression in the European starling (Sturnus vulgaris)
MI, Behav Ecol Sociobiol 62(), 2007
Hormonal correlates of individual quality in a long-lived bird: a test of the 'corticosterone-fitness hypothesis'.
Angelier F, Wingfield JC, Weimerskirch H, Chastel O., Biol. Lett. 6(6), 2010
PMID: 20573614
Hormone levels predict individual differences in reproductive success in a passerine bird.
Ouyang JQ, Sharp PJ, Dawson A, Quetting M, Hau M., Proc. Biol. Sci. 278(1717), 2011
PMID: 21247953
Endocrine phenotype, reproductive success and survival in the great tit, Parus major.
Ouyang JQ, Sharp P, Quetting M, Hau M., J. Evol. Biol. 26(9), 2013
PMID: 23961922
The relationship between fitness and baseline glucocorticoids in a passerine bird.
Bonier F, Moore IT, Martin PR, Robertson RJ., Gen. Comp. Endocrinol. 163(1-2), 2008
PMID: 19135999
Baseline hormone levels are linked to reproductive success but not parental care behaviors.
Burtka JL, Lovern MB, Grindstaff JL., Gen. Comp. Endocrinol. 229(), 2016
PMID: 26972151
Do baseline glucocorticoids predict fitness?
Bonier F, Martin PR, Moore IT, Wingfield JC., Trends Ecol. Evol. (Amst.) 24(11), 2009
PMID: 19679371
Hormones in avian eggs: physiology, ecology and behavior
D, Adv Study Behav (), 2008
Hormones and reproduction of vertebrates
N, 2011
Maternal testosterone in tree swallow eggs varies with female aggression
LA, Anim Behav 63(), 2002
Egg yolk androgen levels increase with breeding density in the European starling, Sturnus vulgaris
KM, Funct Ecol 18(), 2004
Maternal yolk androgens in European starlings: affected by social environment or individual traits of the mother?
C, Behaviour 145(), 2008
Egg composition in relation to social environment and maternal physiological condition in the collared flycatcher
R, Behav Ecol Sociobiol 63(), 2009
Toward a dynamic model of deposition and utilization of yolk steroids.
Moore MC, Johnston GI., Integr. Comp. Biol. 48(3), 2008
PMID: 21669802
Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them?
Groothuis TG, Schwabl H., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 363(1497), 2008
PMID: 18048291
Testosterone response to GnRH in a female songbird varies with stage of reproduction: implications for adult behaviour and maternal effects
PMID: IND43931176
Golden eggs: maternal manipulation of offspring phenotype by egg androgen in birds
D, Ardeola 50(), 2003
The UFAW handbook on the care and management of laboratory and other research animals: eighth edition
KM, 2010

The behavior of the Japanese or domestic quail Coturnix japonica.
Mills AD, Crawford LL, Domjan M, Faure JM., Neurosci Biobehav Rev 21(3), 1997
PMID: 9168263
Behaviour of Japanese quail (Coturnix japonica) kept in semi-natural aviaries
I, Appl Anim Behav Sci 55(), 1997
Regulation of androgen action
AK, Vitam Horm (), 1998
Sexual differences in the Japanese quail: behavior, morphology, and intracellular metabolism of testosterone.
Balthazart J, Schumacher M, Ottinger MA., Gen. Comp. Endocrinol. 51(2), 1983
PMID: 6413294
Modulation of the adrenocortical responses to acute stress in arctic birds: a possible ecological basis
JC, Am Zool 35(), 1995
Seasonal and individual variation in response to GnRH challenge in male dark-eyed juncos (Junco hyemalis).
Jawor JM, McGlothlin JW, Casto JM, Greives TJ, Snajdr EA, Bentley GE, Ketterson ED., Gen. Comp. Endocrinol. 149(2), 2006
PMID: 16814785
The behaviour of Japanese quail: review of literature from a bioethological perspective
JK, Applied Animal Ethology (), 1974
Daily temporal organization of laying in Japanese quail: variability and heritability.
Houdelier C, Guyomarc'h C, Lumineau S., Chronobiol. Int. 19(2), 2002
PMID: 12025931
The timing of ovulation, movement of the ovum through the oviduct, pigmentation and shell deposition in Japanese quail (Coturnix coturnix japonica)
AE, Poult Sci 43(), 1964
Ovarian follicular growth and maturation in Coturnix quail.
Bacon WL, Koontz M., Poult. Sci. 50(1), 1971
PMID: 4101367
Variability of yolk testosterone concentrations during the reproductive cycle of Japanese quail.
Okuliarova M, Skrobanek P, Zeman M., Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 154(4), 2009
PMID: 19720153
Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material.
Walsh PS, Metzger DA, Higuchi R., BioTechniques 10(4), 1991
PMID: 1867860
Microsatellite loci in Japanese quail and cross-species amplification in chicken and guinea fowl.
Kayang BB, Inoue-Murayama M, Hoshi T, Matsuo K, Takahashi H, Minezawa M, Mizutani M, Ito S., Genet. Sel. Evol. 34(2), 2002
PMID: 12081810
Pre- and post-natal stress in context: effects on the stress physiology in a precocial bird.
Marasco V, Robinson J, Herzyk P, Spencer KA., J. Exp. Biol. 215(Pt 22), 2012
PMID: 22899536
Sex differences in the organizational effects of corticosterone in the egg yolk of quail.
Hayward LS, Richardson JB, Grogan MN, Wingfield JC., Gen. Comp. Endocrinol. 146(2), 2006
PMID: 16430891
The role of testosterone in social interaction.
Eisenegger C, Haushofer J, Fehr E., Trends Cogn. Sci. (Regul. Ed.) 15(6), 2011
PMID: 21616702
Male song quality affects circulating but not yolk steroid concentrations in female canaries (Serinus canaria).
Marshall RC, Leisler B, Catchpole CK, Schwabl H., J. Exp. Biol. 208(Pt 24), 2005
PMID: 16326941
Social influences on the mate choices of male and female Japanese quail
BG, Comp Cogn Behav Rev 3(), 2008
Predictors of fertilization in the Japanese quail, Coturnix japonica
E, Anim Behav 50(), 1995
Gonadal hormone specificity in the sexual behavior of ring doves
M-F, Psychoneuroendocrinology 1(), 1975
Individual variation and the endocrine regulation of behaviour and physiology in birds: a cellular/molecular perspective.
Ball GF, Balthazart J., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 363(1497), 2008
PMID: 18048288
Female Japanese quail aggregate to avoid sexual harassment by conspecific males: a possible cause of conspecific cueing
KN, Anim Behav 65(), 2003
Use of space in the domestic fowl: separating the effects of enclosure size, group size and density
EH, Anim Behav 76(), 2008
Stimulatory effects on the reproductive axis in female songbirds by conspecific and heterospecific male song.
Bentley GE, Wingfield JC, Morton ML, Ball GF., Horm Behav 37(3), 2000
PMID: 10868481
Within-pair testosterone covariation and reproductive output in greylag geese Anser anser
K, Ibis 141(), 1999
Female androgen patterns and within-pair testosterone compatibility in domestic geese (Anser domesticus).
Hirschenhauser K, Weiss BM, Haberl W, Mostl E, Kotrschal K., Gen. Comp. Endocrinol. 165(2), 2009
PMID: 19576216
Testosterone and partner compatibility: evidence and emerging questions
K, Ethology 118(), 2012

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

PMID: 28467428
PubMed | Europe PMC

Suchen in

Google Scholar