Sensory cues and the suppression of reproduction in subordinate female marmoset monkeys, Callithrix jacchus
Open accessAbstract
Subordinate female marmoset monkeys remain anovulatory and have low plasma concentrations of luteinizing hormone (LH) when maintained with their dominant females. Olfactory cues from the dominant female have been implicated in maintaining this reproductive suppression. Subordinate females that received either ablation of the vomeronasal organ (an accessory olfactory organ; n = 3), ablation of the main olfactory epithelium (n = 4), or both lesions (n = 5) did not ovulate in the following 7 weeks while housed with their dominant female. Plasma LH concentrations following either or both lesions were similar to pre-lesion concentrations. Olfactory lesions (verified by histological and behavioural trials) did not impair reproductive activity, as olfactory-lesioned dominant females underwent ovarian cycles of similar duration to intact dominant females. Lesioned subordinate females (n = 6), maintained in visual-only contact with their dominant female and group ovulated 29.1 ± 9.3 days (mean ± sem) after physical separation from their dominant females; this first onset of ovulation was significantly delayed (P < 0.05) compared with intact subordinate females completely isolated from their dominant females and group (10.8 ± 1.3 days, n = 8). Behavioural and visual cues together with olfaction all appear to play important roles in maintaining the suppression of ovulation in subordinate female marmoset monkeys.
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.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Reproductive suppression in subordinate females, as may occur in some primate species, may also involve a conservation of metabolic effort until more favorable circumstances arise.
“Reproductive suppression in subordinate females, as may occur in some primate species (Barrett et al., 1993), may also involve a conservation of metabolic effort until more favorable circumstances arise.”
From Human Vomeronasal Organ Function: A Critical Review of Best and Worst Cases (2001) · cites this paper as Barrett et al., 1993
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
Role of the brain and accessory olfactory system in the block to pregnancy in mice
Lloyd-Thomas, A., & Keverne, E. B. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90051-3 · Cited by 138 · see citing works
Flagged first, then by citations
Research works printed but not linked: 20
- Abbott DH (1984) Behavioral and physiological suppression of fertility in subordinate marmoset monkeys American Journal of Primatology 6 169-186
- Abbott DH (1988) Natural suppression of fertility Symposium of Zoological Society of Eondon 60 7-28
- Abbott DH (1989) Social suppression of reproduction in primates. In Comparative Socioecology. The Behavioural Ecology of Humans and Other Mammals, pp 285-304 (Symposium No. 8 of The British Ecological Society) Eds V Standen and RA Foley. Blackwell Scientific Publications, Oxford
- Abbott DH, McNeilly AS, tunn SF, Hulme MJ and Burden FJ (1981) Inhibition of ovarian function in subordinate female marmoset monkeys {Calliihrix jacchus Jacchus) Journal of Reproduction and Fertility 63, 335-345
- Abbott DH, Hodges JK and George LM (1988) Social status controls LH secretion and ovulation in female marmoset monkeys (Calliihrix Jacchus) Journal of Endocrinology 117 329-339
- Beattie J (1927) The anatomy of the common marmoset Proceedings of the Zoological Society of Eondon 97 (Part 3), 593-718
- Epple G and Katz Y (1984) Social influences on estrogen excretion of ovarian cyclicity in Saddle-back tamarins {Saguinus fuscicollis) American Journal of Primatology 6 215-227
- Harlow CR, Gems S, Hodges JK and Hearn JP (1983) The relationship between plasma progesterone and the timing of ovulation and early embryonic devel¬ opment in the marmoset monkey (Callithrix jacchus) Journal of Zoology 201 273-282
- Harlow CR, Hearn JP and Hodges JK (1984) Ovulation in the marmoset monkey: endocrinology, prediction and detection Journal of Endocrinology 103 17-24
- Hearn JP (1983) The common marmoset {Callithrix jacchus). In Reproduction in New World Primates, pp 161-215 Ed. JP Hearn. M.T.P. Press, Lancaster Hearn JP, Lunn SF, Burden FJ and Pilcher MM (1975) Management of animals for biomedicai research Laboratory Animals 9 125-134
- Hodges JK, Green DI, Cottingham PG, Sauer MJ, Edwards C and Lightman SL (1988) Induction of luteal regression in the marmoset monkey {Callithrix jacchus) by a gonadotrophin-releasing hormone antagonist and the effects on subsequent follicular development. Journal of Reproduction and Fertility 82 743-752
- Sauer MJ, Foulkes JA, Worsfold A and Morris BA (1986) Use of progesterone 11-glucuronide-alkaline phosphatase conjugate in a sensitive microtitre- plate enzymeimmunoassay of progesterone in milk and its application to pregnancy testing in dairy cattle Journal of Reproduction and Fertility 76 375-391
- Savage A, Ziegler TE and Snowdon CT (1988) Sociosexual development, pair bond formation, and mechanisms of fertility suppression in female Cotton- Top Tamarins {Saguinus oedipus oedipus) American Journal of Primaiology 14, 345-359
- Scalia F and Winans SS (1976) New perspectives on the morphology of the olfactory system: olfactory and vomeronasal pathways in mammals. In Mammalian Olfaction, Reproductive Processes and Behavior, pp 7-28 Ed. RL Doty. Academic Press, New York
- Schilling A, Perrett M and Predine J (1984) Sexual inhibition in a prosimian primate: a pheromone-like effect Journal of Endocrinology 102 143-151
- Schultz EW (I960) Repair of the olfactory mucosa American Journal of Pathology 37 1-19
- Siegel S (1956) Non-parametric Statistics for the Behavioral Sciences. McGraw-Hill Koger Kushe, Tokyo Sokal RR and Rohlf FJ (1981) Biometry: The Principles and Practice in Biological Research (2nd Edn) W. H. Freeman & Co., New York
- Stevenson MF (1978) The behaviour and ecology of the common marmoset {Callithrix jacchus jacchus) in its natural environment. In Biology and Behavior of Marmosets, 298 Eds Rothe, HJ Wolters and JP Hearn. Eigenverlag Hartmut Rothe, Gottingen Stevenson MF and Poole TB (1976) An ethogram of the common marmoset {Callithrix jacchus jacchus): general behavioural repertoire Animal Behaviour 24 428-451
- Stevenson MF and Rylands AB (1988) The marmosets, genus Callithrix. In Ecology of Behavior of Neotropical Primates, pp 131-122 Eds RA Mittermeier, AD Rylands, A Coimbra-Filho and GAB Fonseca. World Wildlife Fund, Washington Summers PM, Wennick CJ and Hodges JK (1985) Cloprostenol-induced luteolysis in marmoset monkeys {Callithrix jacchus) Journal of Reproduction and Fertility 73 133-138
- Webb R, Baxter G, McBride D, Norelblom GD and Shaw MPK (1985) The measurement of testosterone and oestradiol-17ß using iodinated tracers and incorporating an affinity chromatography extraction procedure Journal of Steroid Biochemistry 23 104-105
Cited by
Sorted by citations
Structure and function of the vomeronasal system: an update
Halpern, M. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(03)00103-5 · Cited by 639 · see citing works
“, 1993) , however neither main olfactory epithelium ablation nor VNX or both of these procedures is sufficient to overcome the suppression of ovulation in subordinate females when the dominant female is present (Barrett et al., 1993) .”
BackgroundFemale competition and its evolutionary consequences in mammals
Stockley, P., & Bro‐Jørgensen, J. (2010) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2010.00149.x · Cited by 444 · see citing works
Human Vomeronasal Organ Function: A Critical Review of Best and Worst Cases
Meredith, M. (2001) · Chemical Senses · doi:10.1093/chemse/26.4.433 · Cited by 280 · see citing works
“Reproductive suppression in subordinate females, as may occur in some primate species (Barrett et al., 1993), may also involve a conservation of metabolic effort until more favorable circumstances arise.”
BackgroundRelaxed selective pressure on an essential component of pheromone transduction in primate evolution
Liman, E. R., & Innan, H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0636123100 · Cited by 220 · see citing works
Thompson, M. E., Kahlenberg, S. M., Gilby, I. C., & Wrangham, R. W. (2007) · Animal Behaviour · doi:10.1016/j.anbehav.2006.09.007 · Cited by 233 · see citing works
“Resource competition among female primates frequently results in dominants outperforming subordinates (Gouzoules et al. 1982; Harcourt 1987; Bercovitch & Strum 1993; Ellis 1995; Altmann & Alberts 2003b; Creel 2005), sometimes due to reproductive suppression of subordinates (Abbott 1984; Epple & Katz 1984; Ziegler et a…”
Evolution of the nose and nasal skeleton in primates
Smith, T. D., Rossie, J. B., & Bhatnagar, K. P. (2007) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.20143 · Cited by 125 · see citing works
D'scent of man: A comparative survey of primate chemosignaling in relation to sex
Drea, C. M. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.08.001 · Cited by 114 · see citing works
“GC–MS analyses of platyrrhine secretions illustrate the chemical complexity from which one can detect individual scent signatures (Callithrix: T.E. Smith et al., 2001).”
InfluentialScent-marking behavior in wild groups of common marmosets (Callithrix jacchus)
Lázaro-Perea, C., Snowdon, C., & Arruda, M. D. F. (1999) · Behavioral Ecology and Sociobiology · doi:10.1007/s002650050625 · Cited by 109 · see citing works
“... Kleiman 1978; SutcliAe and Poole 1978; Smith 1994); dominant animals display higher rates of marking (common marmosets: Epple 1970; saddle-back tamarins, S. fuscicollis: Epple et al. 1979; and cotton-top tamarins: French and Cleveland 1984); scent marks from dominant females are involved in the suppression of ovul…”
Smith, T. E. (2001) · Chemical Senses · doi:10.1093/chemse/26.5.449 · Cited by 106 · see citing works
“In at least one species, the common marmoset, odor cues specific to certain individuals may regulate the reproductive physiology of conspecifics (Barrett et al., 1990, 1993; Smith and Abbott, 1995; Abbott et al., 1997).”
BackgroundSelf-citationStress and Behaviorally Induced Reproductive Dysfunction in Primates
Cameron, J. (1997) · Seminars in Reproductive Endocrinology · doi:10.1055/s-2008-1067966 · Cited by 102 · see citing works
Female chemical signalling underlying reproduction in mammals
Coombes, H. A., Stockley, P., & Hurst, J. L. (2018) · Journal of Chemical Ecology · doi:10.1007/s10886-018-0981-x · Cited by 98 · see citing works
“Further, female common marmosets that remained in visual, but not in olfactory, contact with their dominant female were still reproductively suppressed, again indicating that suppression is not directly caused by a chemical cue (Barrett et al. 1993).”
BackgroundSaltzman, W., Digby, L. J., & Abbott, D. H. (2009) · Proceedings of the Royal Society of London. Biological Sciences · doi:10.1098/rspb.2008.1374 · Cited by 96 · see citing works
“Finally, when subordinate females housed with their social groups were rendered anosmic, they did not begin to ovulate (Barrett et al. 1993).”
BackgroundInfluentialSelf-citationSmith, T. D., Siegel, M. I., & Bhatnagar, K. P. (2001) · The Anatomical Record · doi:10.1002/ar.1152 · Cited by 98 · see citing works
The evolution of pheromonal communication
Swaney, W. T., & Keverne, E. B. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.09.039 · Cited by 79 · see citing works
“Pheromones are thought to play a role in behavioural regulation n prosimians and new world monkeys [1,2], although the effects f pheromones on behaviour do not appear to be as significant in rimates as in small-brained mammals [3].”
BackgroundAbbott, D. H., Wendy Saltzman, A., SCHULTZ‐DARKEN, N. J., & Smith, T. E. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51923.x · Cited by 80 · see citing works
Self-citationSmith, T. E., & Abbott, D. H. (1998) · American Journal of Primatology · doi:10.1002/(sici)1098-2345(1998)46:4 · Cited by 88 · see citing works
Self-citationFaulkes, C. G., & Abbott, D. H. (1993) · Journal of Reproduction and Fertility · doi:10.1530/jrf.0.0990225 · Cited by 85 · see citing works
Self-citationReproductive suppression in female primates: A review
Beehner, J., & Lu, A. (2013) · Evolutionary Anthropology (print) · doi:10.1002/evan.21369 · Cited by 84
Adaptations to subordinate status in female marmoset monkeys.
Abbott, D. H., Saltzman, W., Schultz-Darken, N., & Tannenbaum, P. L. (1998) · Comparative biochemistry and physiology. Part C, Pharmacology, toxicology & endocrinology · doi:10.1016/s0742-8413(98)00015-2 · Cited by 78 · see citing works
“Olfactory, visual and behavioral cues from dominant female marmosets all play a role in maintaining inhibition of ovulation in subordinate females [14].”
BackgroundSelf-citationAujard, F. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00206-0 · Cited by 73 · see citing works
Lasley, B. L., Loskutoff, N. M., & Anderson, G. B. (1994) · Theriogenology · doi:10.1016/s0093-691x(05)80057-3 · Cited by 75 · see citing works
Atema, J., & Steinbach, M. (2007) · doi:10.1093/acprof:oso/9780195179927.003.0006 · Cited by 75
“Estrus synchrony (McClintock 1983) and reproductive suppression (e.g., Barrett et al. 1993) can also occur with exposure to female urine.”
BackgroundFaulkes, C., Arruda, M. F., & Cruz, M. D. D. (2003) · Molecular Ecology · doi:10.1046/j.1365-294x.2003.01809.x · Cited by 66 · see citing works
“In captivity, reproductive skew in peer groups of unrelated individuals is achieved by a combination of behavioural and pheromonal cues from the dominant female (Barrett et al. 1993; Abbott et al. 1998).”
BackgroundIndividual olfactory signatures in common marmosets (Callithrix jacchus)
Smith, T. E. (2006) · American Journal of Primatology · doi:10.1002/ajp.20254 · Cited by 64 · see citing works
“In the common marmoset, individual odors from the dominant female are one of the primary proximate cues that suppress female reproductive physiology [Barrett et al., 1990, 1993].”
Seasonality in squirrel monkeys (Saimiri sciureus): Social facilitation by females
Schiml, P. A., Mendoza, S. P., Wendy Saltzman, A., Lyons, D. M., & Mason, W. A. (1996) · Physiology & Behavior · doi:10.1016/0031-9384(96)00134-5 · Cited by 59 · see citing works
Scent-marking investment is determined by sex and breeding status in meerkats
Jordan, N. R. (2007) · Animal Behaviour · doi:10.1016/j.anbehav.2006.12.015 · Cited by 62 · see citing works
“cotton-top tamarins, Saguinus oedipus oedipus: Savage et al. 1988; common marmosets: Barrett et al. 1993 ) but whether this is also true for meerkats remains unknown.”
Spiering, P. A., Somers, M. J., Maldonado, J., Wildt, D., & Gunther, M. (2010) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-009-0875-6 · Cited by 61
“A combination of behavioral and hormonal cues is also well known to limit subordinate reproduction in the common marmoset (Callithrix jacchus, Barrett et al. 1993 ) and cotton-top tamarin (Saguinus oedipus, Savage et al. 1988).”
BackgroundNonhuman Primate Models of Atherosclerosis
Shelton, K. A., Clarkson, T. B., & Kaplan, J. R. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-381366-4.00008-0 · Cited by 65 · see citing works
Behavioural suppression of female pine voles after replacement of the breeding male
Brant, C. L., Schwab, T. M., Vandenbergh, J. G., Schaefer, R. L., & Solomon, N. G. (1998) · Animal Behaviour · doi:10.1006/anbe.1997.0639 · Cited by 60 · see citing works
Smith, T. E., Faulkes, C. G., & Abbott, D. H. (1997) · Hormones and Behavior · doi:10.1006/hbeh.1997.1384 · Cited by 58
Self-citationThe vomeronasal organ of Lemur catta
Smith, T. D., Muchlinski, M., Bhatnagar, K. P., Durham, E., Bonar, C., & Burrows, A. (2015) · American Journal of Primatology · doi:10.1002/ajp.22326 · Cited by 57
The Vomeronasal Organ of New World Monkeys (Platyrrhini)
Smith, T. D., Garrett, E. C., Bhatnagar, K. P., Bonar, C. J., Bruening, A. E., Dennis, J. C., Kinznger, J. H., Johnson, E. W., & Morrison, E. E. (2011) · The Anatomical Record · doi:10.1002/ar.21509 · Cited by 54 · see citing works
“Attempts to experimentally ablate the VNO have produced no evidence, as of yet, for VNS function in platyrrhines (Barrett et al., 1993).”
BackgroundExpression of neuron-specific markers by the vomeronasal neuroepithelium in six species of primates.
Dennis, J., Smith, T. D., Bhatnagar, K. P., Bonar, C., Burrows, A., & Morrison, E. (2004) · Anatomical Record Part A-discoveries in Molecular Cellular and Evolutionary Biology · doi:10.1002/ar.a.20124 · Cited by 48 · see citing works
“Likewise, several behaviors that in rodents are mediated by the VNO are not solely VNO-mediated in primates (Barrett et al., 1993; Aujard, 1997; Kraus et al., 1999).”
BackgroundMaternal care associates with play dominance rank among adult female rats
Parent, C. I., Corpo, A. D., Cameron, N. M., & Meaney, M. J. (2012) · Developmental Psychobiology · doi:10.1002/dev.21070 · Cited by 43 · see citing works
Manipulation of sex ratio at birth by urinary cues in a prosimian primate
Perret, M. (1996) · Behavioral Ecology and Sociobiology · doi:10.1007/s002650050241 · Cited by 45
“Impaired ovulation, inhibition of oestrus cycles, abortion and reduction in maternal investment have also been described in primates and attributed to social relationships (Fedigan 1983; Harcourt 1987; Keverne 1992) and the role of chemical cues in such e⁄ects has been stressed in callithrichids (Epple and Katz 1984;…”
BackgroundResolving social conflict among females without overt aggression
Cant, M., & Young, A. J. (2013) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2013.0076 · Cited by 43 · see citing works
“Indeed, such offspring competition costs could also account for reproductive abstention in response to the signals of dominants [80,87,106,107,127,128], without a need to invoke a role for threats per se.”
Jackson, L. M., & Harder, J. D. (1996) · Biology of Reproduction · doi:10.1095/biolreprod54.2.506 · Cited by 43 · see citing works
Smith, T. E., Schaffner, C., & French, J. (1997) · Hormones and Behavior · doi:10.1006/hbeh.1997.1380 · Cited by 40 · see citing works
“Familytory function (Epple and Katz, 1984; Savage et al., 1988; Barrett, Abbott, and George, 1990; 1993; Smith, 1994). groups ranged in size from four to eight individuals and always contained the breeding pair and their off-There is also evidence, however, that an absence of stimulatory cues from…”
BackgroundSexual motivation in relation to social rank in pair-housed sows.
Pedersen, L., Heiskanen, T., & Damm, B. (2003) · Animal Reproduction Science · doi:10.1016/s0378-4320(02)00208-7 · Cited by 37
“The results are in agreement with previous reports of negative effects of social subordination or social stress on sexual behaviour in other species (Abbott et al., 1988; Barrett et al., 1993; Wasser, 1996; Packer et al., 1995; Shively et al., 1997; Marchlewska-Koj, 1997; Molteno and Bennett, 2000), and in group-house…”
BackgroundResultSeasonal endocrine changes and breeding activity in mediterranean wild ruminants.
Santiago-Moreno, J., Gómez-Brunet, A., Toledano-Díaz, A., Picazo, R., González-Bulnes, A., & López-Sebastián, A. (2006) · Reproduction in domestic animals = Zuchthygiene · doi:10.1111/j.1439-0531.2006.00771.x · Cited by 36
Perret, M., Aujard, F., Séguy, M., & Schilling, A. (2003) · Journal of Biological Rhythms · doi:10.1177/0748730403254248 · Cited by 34 · see citing works
“Despite the wide use of olfactory communication in many species of primates including humans, the role of olfactory bulb removal or chemosignals has only been investigated for sociosexual behaviors or reproduction (Barret et al., 1993; Converse et al., 1995; Weller, 1998).”
BackgroundSmith, T. E., Abbott, D., Tomlinson, A., & Mlotkiewicz, J. (1997) · Journal of Chemical Ecology · doi:10.1023/b:joec.0000006664.38169.e5 · Cited by 32 · see citing works
Self-citationThe Accessory (Vomeronasal) Chemoreceptor System in Some Prosimians
Evans, C., & Schilling, A. (1995) · Springer eBooks · doi:10.1007/978-1-4757-2405-9_23 · Cited by 31 · see citing works
Dehnhard, M. (2011) · International Zoo Yearbook · doi:10.1111/j.1748-1090.2010.00131.x · Cited by 29 · see citing works
Santiago-Moreno, J., Gómez-Brunet, A., González-Bulnes, A., Malpaux, B., Chemineau, P., Pulido-Pastor, A., & López-Sebastián, A. (2003) · Reproduction, nutrition, development · doi:10.1051/rnd:2003023 · Cited by 27
Accessory chemosignaling mechanisms in primates
Evans, C. S. (2006) · American Journal of Primatology · doi:10.1002/ajp.20250 · Cited by 21 · see citing works
“The degree of AOS involvement in reproduction and the extent of VN semiochemical usage within the New World monkeys have not been fully established [Barrett et al., 1993; Belcher et al., 1990; Fuchs et al., 1991].”
Novel restraint system for neuroendocrine studies of socially living common marmoset monkeys
Schultz-Darken, N., Pape, R., Tannenbaum, P., Saltzman, W., & Abbott, D. H. (2004) · Laboratory Animals. Journal of the Laboratory Animal Science Association · doi:10.1258/0023677041958918 · Cited by 26
“At the same time, the ovulatory cycles of subordinate females in social groups are suppressed in response to a combination of behavioural, visual and olfactory cues from the dominant female, so that subordinate females are usually anovulatory and hypo-oestrogenemic (Abbott et al. 1988, 1993, 1997, Barrett et al. 1990,…”
BackgroundSelf-citationJohnston, R., & delBarco‐Trillo, J. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00011-5 · Cited by 28 · see citing works
Faulkes, C. G., Arruda, M. F., & da Cruz, M. A. O. M. (2009) · Springer eBooks · doi:10.1007/978-1-4419-0293-1_5 · Cited by 22 · see citing works
“In captivity, reproductive skew in peer groups of unrelated individuals is achieved by a combination of behavioral and pheromonal cues from the dominant female that brings about a hypogonadotrophic state resulting in anovulation in subordinate females (Abbott et al. 1998; Barrett et al. 1993 ).”
BackgroundSocial dominance and breeding activity in Spanish ibex (Capra pyrenaica) maintained in captivity
Santiago‐Moreno, J., Gómez-Brunet, A., Toledano‐Díaz, A., Pulido‐Pastor, A., & López-Sebastián, A. (2007) · Reproduction Fertility and Development · doi:10.1071/rd06122 · Cited by 18 · see citing works
Solomon-Lane, T. K., Willis, M. C., Pradhan, D. S., & Grober, M. (2014) · doi:10.1163/1568539x-00003188 · Cited by 21
“In extreme cases of reproductive skew, only dominants breed and subordinates are reproductively suppressed (Barrett et al., 1993; Clarke & Faulkes, 2001; White et al., 2002; Fitzpatrick et al., 2008).”
BackgroundMechanisms of reproductive suppression in female pine voles (Microtus pinetorum).
Solomon, N. G., Brant, C., Callahan, P., & Steinly, B. (2001) · Reproduction · doi:10.1530/rep.0.1220297 · Cited by 20
“In two species of mole-rat and in callitrichid monkeys, subordinate females have significantly lower concentrations of LH in the presence of a dominant female compared with subordinate females housed alone (Abbott, 1984; Savage et al., 1988; Faulkes et al., 1990a; Barrett et al., 1993; Bennett et al., 1993; Molteno an…”
BackgroundGenetic basis of olfactory communication in primates
Mundy, N. I. (2006) · American Journal of Primatology · doi:10.1002/ajp.20252 · Cited by 17 · see citing works
“The most direct evidence for pheromonal use in primates come from studies in marmosets (Callithrix jacchus) and mouse lemurs (Microcebus murinus) [Aujard, 1997; Barrett et al., 1993].”
BackgroundThe Vomeronasal Organ and Its Evolutionary Loss in Catarrhine Primates
Bhatnagar, K. P., & Smith, T. D. (2007) · doi:10.1016/b0-12-370878-8/00013-6 · Cited by 18
Mustoe, A. C. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105293 · Cited by 18 · see citing works
Smith, T. D., Bhatnagar, K. P., Bonar, C., Shimp, K. L., Mooney, M., & Siegel, M. (2003) · American Journal of Physical Anthropology · doi:10.1002/ajpa.10165 · Cited by 17
“Experiments on callitrichids have involved combined ablation of olfactory and vomeronasal pathways (Barret et al., 1993; Dixson, 1993), rendering it difficult to determine the relative importance of vomeronasal vs. olfactory systems to chemosensation.”
BackgroundOlfaction in Nonhuman Primates
Laska, M., & Salazar, L. T. H. (2015) · doi:10.1002/9781118971758.ch27 · Cited by 16 · see citing works
Pradhan, D. S., Solomon-Lane, T. K., & Grober, M. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00008 · Cited by 16 · see citing works
Rasoloharijaona, S., Randrianambinina, B., & Joly-Radko, M. (2010) · American Journal of Primatology · doi:10.1002/ajp.20865 · Cited by 16
“In fact, relatively little is known about pheromones in primates, but they seem to play a great role in strepsirrhines and platyrrhines [Aujard, 1997; Barrett et al., 1993].”
BackgroundPhysiological Constraints and Latitudinal Breeding Season in the Canidae
Valdespino, C. (2007) · Physiological and Biochemical Zoology · doi:10.1086/521802 · Cited by 14 · see citing works
“Individual differences in the threshold of the perception of stressful situations (such as being in captivity) could also have resulted in the reproductive suppression (Barrett et al. 1993; Wingfield et al. 1997; von Holst 1998; Durham 2002) of this female.”
BackgroundPutative chemical inhibition of development by conspecifics in mosquitofish, Gambusia affinis
Lutnesky, M. M. F., & Adkins, J. W. (2003) · Environmental Biology of Fishes · doi:10.1023/a:1023696609963 · Cited by 15
Mucignat-Caretta, C. (2014) · doi:10.1201/b16511-10 · Cited by 12
Séguy, M., & Perret, M. (2005) · Physiology and Behavior · doi:10.1016/j.physbeh.2004.10.019 · Cited by 12
Pradhan, D. S., Willis, M. C., Solomon-Lane, T. K., Thonkulpitak, K., & Grober, M. (2015) · doi:10.1163/1568539x-00003262 · Cited by 11
“Dominants may gain higher reproductive success by suppressing subordinate reproduction (Barrett et al., 1993; Fitzpatrick et al., 2008), monopolizing mating opportunities, producing more offspring, and experiencing lower rates of abortion, egg loss, and offspring mortality (Trunzer et al.”
BackgroundReproduction in Female Marmoset Monkeys, Callithrix jacchus
Abbott, D. (1992) · Springer eBooks · doi:10.1007/978-1-4612-2866-0_17 · Cited by 11 · see citing works
Self-citationFunctional Context of Scent-Marking in Callithrix penicillata
Oliveira, D. G., & Macedo, R. (2010) · Folia primatologica · doi:10.1159/000313011 · Cited by 9 · see citing works
“Although scentmarking in captive animals has been well studied in this family [Epple, 1973; Sutcliffe and Poole, 1978; Barrett et al., 1993; Washabaugh and Snowdon, 1998; Smith et al., 2001; Sousa et al., 2006], there are few systematic studies of this behaviour in the wild [Lazaro-Perea et al.,…”
The Humane Control of Captive Marmoset and Tamarin Populations
Sainsbury, A. (1997) · Animal Welfare · doi:10.1017/s0962728600019825 · Cited by 9
Smith, T. D., Dennis, J., Bhatnagar, K. P., Bonar, C., Burrows, A., & Morrison, E. (2004) · Anatomical Record Part A-discoveries in Molecular Cellular and Evolutionary Biology · doi:10.1002/ar.a.20035 · Cited by 8 · see citing works
“Existing experimental evidence is inconclusive (Barrett et al., 1993; Dixson, 1998).”
BackgroundFaulkes, C. G. (2001) · doi:10.1038/npg.els.0001847 · Cited by 6
Xu, X.-W., Sun, X., Bai, Q.-Q., Zhang, Y.-Y., Qin, J., & Zhang, X.-M. (2021) · Journal of Comparative Physiology · doi:10.1007/s00359-021-01480-8 · Cited by 4
Bercovitch, F., & Berry, P. S. (2018) · African Journal of Ecology · doi:10.1111/aje.12530 · Cited by 1
Basic Physiology of Callithrix jacchus
Mätz-Rensing, K., & Korte, S. (2015) · doi:10.1016/b978-0-12-417144-2.00007-x · Cited by 1
Female-Based Patterns and Social Function in Avian Chemical Communication
Whittaker, D. J., & Hagelin, J. C. (2020) · Journal of Chemical Ecology · doi:10.1007/s10886-020-01230-1 · Cited by 32 · see citing works
Condition-Dependent Traits in Arthropods and Mammals
Geary, D. C. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-801562-9.00004-1
- Authors
- Barrett, J., Abbott, D. H., & George, L. M.
- Affiliations
- Zoological Society of London (GB)
- Venue
- Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 1993-01-01
- Volume
- 97
- Issue
- 1
- Pages
- 301-310
- ISSN
- 1470-1626 (ISSN-L)
- 1741-7899
- OpenAlex
- W2045346978
- Cited by
- 77
- References
- 16
- Citations by year
- 2024: 1 · 2022: 2 · 2021: 1 · 2020: 1 · 2018: 2 · 2017: 1 · 2015: 8 · 2014: 3 · 2013: 2 · 2012: 2
- FWCI
- 2.63
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Reproduction (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust
- Topics
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- reproductive suppression, marmoset monkey, Callithrix jacchus, olfactory cues, vomeronasal organ, olfactory epithelium, luteinizing hormone, anovulation, social dominance, social isolation, visual cues, ovarian cycle
- MeSH terms
- Animals, Anovulation, Callithrix, Dominance-Subordination, Epithelium, Female, Luteinizing Hormone, Nasal Mucosa, Ovary, Progesterone, Reproduction, Smell, Social Environment, Vision, Ocular
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