Quality of maternal and paternal care predicts later stress reactivity in the cooperatively-breeding marmoset (Callithrix geoffroyi)
Open accessAbstract
Variation in the early postnatal social environment can have lasting effects on hypothalamic–pituitary–adrenal (HPA) axis stress responses. Both rats and macaque monkeys subjected to low quality or abusive maternal care during the early postnatal period have more pronounced HPA responses to environmental stressors throughout development and into adulthood compared to animals reared in higher quality early maternal environments. However, little is known about the relative contributions to HPA stress response styles in developing offspring in species in which offspring care is routinely provided by group members other than the mother, such as in cooperatively breeding mammals. Marmoset monkeys exhibit cooperative offspring rearing, with fathers and older siblings providing care in addition to that provided by the mother. We evaluated the effects of early maternal, paternal, and older sibling care on HPA responses to social separation across development in captive white-faced marmoset offspring (Callithrix geoffroyi). We monitored offspring care by mothers, fathers, and older siblings in marmosets for the first 60 days of life. Later in development, each marmoset experienced three standardized social separation/novelty exposure stressors at 6, 12, and 18 months of age. During separation, we collected urine samples and analyzed them via enzyme immunoassay for cortisol levels. Infants that received higher rates of rejections from the entire family group showed higher cortisol responses to social separation. This relationship was found when mothers, fathers, and older siblings, were analyzed separately as well. No differences in cortisol responses were found between offspring that received high and low rates of carrying or high and low rates of licking and grooming by any group member. In the cooperatively breeding marmoset, early social cues from multiple classes of caregivers may influence HPA stress responses throughout the lifespan.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000) · Endocrine Reviews · doi:10.1210/edrv.21.1.0389 · Cited by 7,541 · see citing works
Effects of stress throughout the lifespan on the brain, behaviour and cognition
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2639 · Cited by 6,256 · see citing works
Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177 · see citing works
Stress, adaptation, and disease. Allostasis and allostatic load
McEWEN, B. S. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09546.x · Cited by 5,092 · see citing works
Nestler, E. J., Barrot, M., DiLeone, R. J., Eisch, A. J., Gold, S. J., & Monteggia, L. M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00653-0 · Cited by 3,217 · see citing works
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997) · Science · doi:10.1126/science.277.5332.1659 · Cited by 3,170 · see citing works
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638 · see citing works
Candelotti, E., De Vito, P., De Luca, R., Gionfra, F., Percario, Z., Farías, R., Luly, P., Affabris, E., Davis, P., Pedersen, J., et al. (2010) · Wiley eBooks · doi:10.1002/cphy · Cited by 1,501 · see citing works
The role of corticotropin-releasing factor in depression and anxiety disorders
Arborelius, L., Owens, M., Plotsky, P., & Nemeroff, C. (1999) · Journal of Endocrinology · doi:10.1677/joe.0.1600001 · Cited by 1,378 · see citing works
Sapolsky, R. M., & Meaney, M. J. (1986) · Brain Research Reviews · doi:10.1016/0165-0173(86)90010-x · Cited by 991 · see citing works
Cooperative Breeding in Mammals
(1996) · Cambridge University Press eBooks · doi:10.1017/cbo9780511574634 · Cited by 970 · see citing works
Meaney, M. J., & Szyf, M. (2005) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2005.7.2/mmeaney · Cited by 958 · see citing works
Meaney, M. J., Diorio, J., Francis, D., Widdowson, J., LaPlante, P., Caldji, C., Sharma, S., Seckl, J. R., & Plotsky, P. M. (2010) · Developmental Neuroscience · doi:10.1159/000111395 · Cited by 878 · see citing works
Extrapolating brain development from experimental species to humans
Clancy, B., Finlay, B. L., Darlington, R. B., & Anand, K. J. S. (2007) · NeuroToxicology · doi:10.1016/j.neuro.2007.01.014 · Cited by 812 · see citing works
Child maltreatment and the developing HPA axis
Tarullo, A. R., & Gunnar, M. R. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.010 · Cited by 737 · see citing works
Early programming of the hypothalamo–pituitary–adrenal axis
MATTHEWS, S. (2002) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(02)00690-2 · Cited by 513 · see citing works
Liu, Caldji, Sharma, Plotsky, & Meaney (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00422.x · Cited by 451 · see citing works
Barr, C. S., Newman, T. K., Shannon, C., Parker, C., Dvoskin, R. L., Becker, M. L., Schwandt, M., Champoux, M., Lesch, K. P., Goldman, D., et al. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.12.008 · Cited by 385 · see citing works
Macaque societies: a model for the study of social organization
(2005) · Choice Reviews Online · doi:10.5860/choice.42-5276 · Cited by 274 · see citing works
The impact of early adverse care on HPA axis development: Nonhuman primate models
Sánchez, M. M. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.012 · Cited by 247 · see citing works
Gunnar, M. R., & Quevedo, K. M. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)67010-1 · Cited by 246 · see citing works
Higley, J. D., Suomi, S. J., & Linnoila, M. (1992) · Biological Psychiatry · doi:10.1016/0006-3223(92)90016-s · Cited by 240 · see citing works
Parker, K. J., & Dario Maestripieri, A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.09.003 · Cited by 192 · see citing works
Viau, V., Sharma, S., Plotsky, P. M., & Meaney, M. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-03-01097.1993 · Cited by 181 · see citing works
McCormack, K., Newman, T. K., Higley, J. D., Maestripieri, D., & Sanchez, M. M. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.01.009 · Cited by 161 · cited 1× · see citing works
“, 2004) or monoaminergic (Barr et al., 2004b; McCormack et al., 2009) neurotransmitter system components.”
BackgroundMacaque Societies. A Model for the Study of Social Organization
Bernstein, I. S. (2005) · International Journal of Primatology · doi:10.1007/s10764-005-6467-z · Cited by 157 · see citing works
2006 Curt P. Richter award winner
DeVries, A. C., Craft, T. K. S., Glasper, E. R., Neigh, G. N., & Alexander, J. K. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.04.007 · Cited by 153 · see citing works
Nunes, S., Fite, J. E., Patera, K. J., & French, J. A. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2000.1631 · Cited by 149 · see citing works
Self-citationClarke, A. S. (1993) · Developmental Psychobiology · doi:10.1002/dev.420260802 · Cited by 145 · see citing works
Psychosocial Stress and Urinary Cortisol Excretion in Marmoset Monkeys
SMITH, T., & French, J. A. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00103-0 · Cited by 143 · see citing works
Self-citationFlinn, M. V., Nepomnaschy, P. A., Muehlenbein, M. P., & Ponzi, D. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.01.005 · Cited by 139 · see citing works
Social development during the first twenty weeks in the cotton-top tamarin (Saguinus o. oedipus)
Cleveland, J., & Snowdon, C. T. (1984) · Animal Behaviour · doi:10.1016/s0003-3472(84)80279-1 · Cited by 137 · see citing works
Johnson, E. O., Kamilaris, T. C., Carter, C. S., Calogero, A. E., Gold, P. W., & Chrousos, G. P. (1996) · Biological Psychiatry · doi:10.1016/0006-3223(95)00397-5 · Cited by 132 · see citing works
Hewlett, B. S. (2017) · Routledge eBooks · doi:10.4324/9780203792063 · Cited by 128 · see citing works
Bhatnagar, S., & Meaney, M. J. (1995) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1995.tb00672.x · Cited by 127 · see citing works
Nunes, S., Fite, J. E., & French, J. A. (2000) · Animal Behaviour · doi:10.1006/anbe.2000.1524 · Cited by 123 · see citing works
Self-citationRukstalis, M., & French, J. A. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.09.004 · Cited by 115 · see citing works
Self-citationInfantile Experience and the Maturation of the Pituitary Adrenal Axis
Levine, S., Alpert, M., & Lewis, G. W. (1957) · Science · doi:10.1126/science.126.3287.1347 · Cited by 114 · see citing works
Dettling, A. C., Feldon, J., & Pryce, C. R. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00785-2 · Cited by 113 · see citing works
GABRA6 gene polymorphism and an attenuated stress response
Uhart, M., McCaul, M. E., Oswald, L. M., Choi, L., & Wand, G. S. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001535 · Cited by 106 · see citing works
Stevens, H. E., Leckman, J. F., Coplan, J. D., & Suomi, S. J. (2009) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/chi.0b013e318193064c · Cited by 106 · see citing works
Marmosets and tamarins: systematics, behaviour, and ecology
Peres, C. A. (1994) · Trends in Ecology & Evolution · doi:10.1016/0169-5347(94)90303-4 · Cited by 101 · see citing works
From dependence to sexual maturity: the behavioural ontogeny of Callitrichidae
Yamamoto, M. E. (1993) · doi:10.1093/oso/9780198540229.003.0011 · Cited by 100 · see citing works
Schaffner, C. M., Shepherd, R. E., Santos, C. V., & French, J. A. (1995) · American Journal of Primatology · doi:10.1002/ajp.1350360303 · Cited by 67 · see citing works
Self-citationArabadzisz, D., Heijtz, R. D., Knuesel, I., Weber, E., Pilloud, S., Dettling, A. C., Feldon, J., Law, A. J., Harrison, P. J., & Pryce, C. R. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.12.016 · Cited by 60 · see citing works
Mineralocorticoid Receptor Gene Variants as Determinants of HPA Axis Regulation and Behavior
DeRijk, R. H., de Kloet, E. R., Zitman, F. G., & van Leeuwen, N. (2010) · Endocrine development · doi:10.1159/000321235 · Cited by 50 · see citing works
Smith, A. S., Birnie, A. K., & French, J. A. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.06.014 · Cited by 48 · see citing works
Self-citationEffects of Early Parenting on Growth and Development in a Small Primate
Johnson, E. O., Kamilaris, T. C., Calogero, A. E., Gold, P. W., & Chrousos, G. P. (1996) · Pediatric Research · doi:10.1203/00006450-199606000-00012 · Cited by 47 · see citing works
Barr, C. S., Newman, T. K., Lindell, S. G., Becker, M. L., Shannon, C., Champoux, M. C., Suomi, S. J., & Higley, J. D. (2004) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000130973.94350.8c · Cited by 43 · see citing works
Meaney, M. J., Diorio, J. C., Francis, D. D., Widdowson, J., LaPlante, P., Caldji, C., Sharma, S., Seckl, J. R., & Plotsky, P. M. (2007) · Developmental Neuroscience · doi:10.1159/000111396 · Cited by 43 · see citing works
Caldji, C., Liu, D., Sharma, S., Diorio, J. C., Francis, D. D., Meaney, M. J., & Plotsky, P. M. (2001) · Comprehensive physiology · doi:10.1002/cphy.cp070413 · Cited by 41 · see citing works
Tardif, S. D., Carson, R. L., & Gangaware, B. L. (1992) · Ethology · doi:10.1111/j.1439-0310.1992.tb00956.x · Cited by 40 · see citing works
Dettling, A. C., Pryce, C. R., Martin, R. D., & D�beli, M. (1998) · Developmental Psychobiology · doi:10.1002/(sici)1098-2302(199807)33:1 · Cited by 39 · see citing works
French, J. A., Fite, J. E., Jensen, H. A., Oparowski, K., Rukstalis, M., Fix, H., Jones, B., Maxwell, H., Pacer, M., Power, M. L., et al. (2007) · American Journal of Primatology · doi:10.1002/ajp.20385 · Cited by 35 · see citing works
Self-citationFamily Feuds: Severe Aggression among Cooperatively Breeding Cotton-Top Tamarins
Snowdon, C. T., & Pickhard, J. J. (1999) · International Journal of Primatology · doi:10.1023/a:1020796517550 · Cited by 34 · see citing works
French, J. A., Smith, A. S., Gleason, A., Birnie, A. K., Mustoe, A. C., & Korgan, A. C. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.006 · Cited by 17 · see citing works
Self-citationCavanaugh, J., & French, J. A. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.02.006 · Cited by 17 · see citing works
Self-citationDifferential infant carrying in captive and wild common marmosets (Callithrix jacchus)
Yamamoto, M. E., Albuquerque, F. S., Lopes, N. A., & Ferreira, E. S. (2008) · acta ethologica · doi:10.1007/s10211-008-0046-1 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Early-life experience, epigenetics, and the developing brain
Kundakovic, M., & Champagne, F. A. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.140 · Cited by 304 · see citing works
Paternal Influences on Offspring Development: Behavioural and Epigenetic Pathways
Braun, K., & Champagne, F. A. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12174 · Cited by 157 · see citing works
- Authors
- Birnie, A. K., Taylor, J. H., Cavanaugh, J., & French, J. A.
- Affiliations
- University of Nebraska at Omaha (US)
- Corresponding author
- Birnie, Andrew K.
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2013-12
- Volume
- 38
- Issue
- 12
- Pages
- 3003-3014
- ISSN
- 0306-4530 (ISSN-L)
- PMC
- PMC3877691
- OpenAlex
- W2120963974
- Cited by
- 43
- References
- 58
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2023: 1 · 2022: 3 · 2021: 4 · 2020: 3 · 2019: 2 · 2018: 6 · 2017: 2 · 2016: 2 · 2015: 12 · 2014: 4 · 2013: 1
- FWCI
- 2.51
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- University of Nebraska Medical Center
- University of Nebraska Omaha
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD 42882, R01HD042882, R56HD042882)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Keywords
- maternal care, paternal care, sibling caregiving, cooperative breeding, hypothalamic-pituitary-adrenal axis, stress reactivity, cortisol, social separation, Callithrix geoffroyi
- MeSH terms
- Animals, Anxiety, Separation, Behavior, Animal, Callithrix, Female, Grooming, Hydrocortisone, Hypothalamo-Hypophyseal System, Individuality, Male, Maternal Behavior, Paternal Behavior, Pituitary-Adrenal System, Rejection, Psychology, Sex Characteristics, Stress, Psychological, Parenting
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review