American Journal of Primatology 75:197–201 (2013)
The Integrative Biology of Reproductive Functioning in Nonhuman Primates
AMANDA M. DETTMER*
Department of Psychiatry, University of Pittsburgh, Pittsburgh, Pennsylvania
At the 34th annual meeting of the American Society of Primatologists in 2011, the society organized an
interdisciplinary symposium entitled, “Reproductive Function & Dysfunction in Nonhuman Primates.”
The articles in this special section, excluding this introduction, represent the findings presented by
four of the five speakers in that symposium. The data presented highlight the myriad factors that
contribute to primate reproductive function and dysfunction, including hormones, genes, maternal
variance, environmental factors, social relationships, and strategic interactions. Collectively, these ar-
ticles emphasize the integrative nature of primate reproductive function, and highlight the importance
of the nonhuman primate as a model for human reproductive function and dysfunction in humans.
Am. J. Primatol. 75:197–201, 2013.
C ?2012 Wiley Periodicals, Inc.
Key words: reproduction; dysfunction; integrative; primate
The reproductive system represents a window
into the integrative biology of primates. Multiple fac-
tors simultaneously influence reproductive function-
ing as well as dysfunction, including maternal vari-
ance, environmental factors, social relationships and
interactions, genes, and hormones. Nonhuman pri-
of human reproductive processes owing to their high
degree of genetic, physiological, morphological, and
behavioral similarity. Though the majority of re-
search into NHP reproductive function and dysfunc-
tion has occurred with female models, the articles
in this special issue highlight this important model
while emphasizing that the study of male NHP re-
productive functioning is just as critical. Studying
the multiple factors that contribute to reproductive
success and failure in both sexes will yield valuable
information regarding similar processes in humans.
HISTORY OF NONHUMAN PRIMATE
As many as 70 years ago, researchers were look-
ing to the study of NHPs to gain insights into re-
productive function. These first studies were general
studies of anatomy and physiology [Matthews, 1946;
Young & Yerkes, 1943] and mating/breeding behav-
iors in captivity [Souri and Swani, 1962; van Wage-
relation of these variables to reproductive success.
The 1960s saw characterizations of the menstrual
cycle in a variety of female NHP species including
the chimpanzee [Erikson, 1963], loris [Ramaswami
rel monkey [Lang, 1967], baboon [Hendrickx, 1967],
lemur [Evans & Goy, 1968], and gibbon [Chaicumpa
et al., 1969]. In this decade researchers began recog-
nizing the importance of studying the content, collec-
tion, and storage, of semen in male monkeys [Krae-
mer and Cruz, 1969; Mastroianni & Manson, 1963],
though the emphasis was largely for the use of sam-
ples in artificial reproductive methods.
More in-depth characterization of female NHP
reproductive physiology was achieved in the 1970s,
when studies of reproductive hormones under natu-
ral and experimental conditions were conducted in
a variety of species at various stages of the repro-
ductive cycle [Boorman et al., 1974; Chandra et al.,
1971; Erikson & Wada, 1970; Kanagawa et al., 1973;
Parkin & Hendrickx, 1975], which ultimately led to
the development of techniques for pregnancy diag-
nosis in NHPs [Gribnau, 1975; Hobson et al., 1975].
This period also saw the first studies into environ-
mental influences (i.e., irradiated diet) on female re-
productive functions [Sialy et al., 1976]. In contrast,
in this decade the preponderance of research into
an article referenced herein was withdrawn, and the corrected
article was published online 6 December 2012.
*Correspondence to: Amanda M. Dettmer, Department of Psy-
chiatry, University of Pittsburgh, 3811 O’Hara Street, Pitts-
burgh, PA 15213. E-mail: email@example.com
Received 7 May 2012; revised 31 May 2012; revision accepted 6
Published online 23 July 2012 in Wiley Online Library
C ?2012 Wiley Periodicals, Inc.
198 / Dettmer
male NHP reproductive physiology remained pri-
marily limited to evaluating semen collection meth-
of spermatozoa development and chemical composi-
tion were beginning [Amann et al., 1976; Arora et al.,
1975], as were some studies into male contraceptives
[Laumas et al., 1978; Purandare et al., 1979].
The focus of NHP reproductive research shifted
in the 1980s, when we began to see studies directed
at understanding reproductive dysfunction (as op-
posed to normal function) in females. These studies
occurred primarily in the laboratory and included
environmental [Mohanty & Das, 1982] and drug
[Jaszczak, 1983; Mello et al., 1983; Smith & Asch,
1984; Mottet et al., 1985] effects on dysfunction, in-
cluding a greater understanding of the mechanisms
of the placenta [Berglund et al., 1989; Fazleabas
et al., 1989; Pepe & Albrect, 1984; Ramsey, 1981]
and uterus [Ducsay et al., 1983; Harbert & Spisso,
1980; Potgieter et al., 1985] during pregnancy.
We were also beginning to understand the neu-
ral underpinnings of female reproductive function
[Ferin, 1983; Hodges, 1985; Pohl & Hotchkiss,
1983], though detailed findings in this area of
research were forthcoming. Importantly, during this
decade, field researchers began the first studies of
wild NHP reproductive hormones owing to the de-
velopment of fecal hormone analysis (Risler et al.,
1987). This breakthrough opened the door for future
studies of wild primate reproductive endocrinology
ratory studies into male reproductive processes were
being extended to examine endocrine effects on tes-
ticular function [Mann et al., 1987; Shandilya et al.,
1982], though this area still lagged behind research
done in females.
In the 1990s, a more integrative approach
to studying female reproductive functioning was
emerging, with studies of social influences, includ-
ing dominance rank and pair-bond formation, on
reproductive endocrinology and reproductive suc-
cess being completed in both the field and labo-
ratory [Koenig, 1995; Silva & Sousa, 1997; Smith
et al., 1997; Ziegler & Bercovitch, 1990]. Re-
search in this decade also saw the emergence
of a focus of research by Cameron and col-
leagues [Cameron, 1997; Cameron et al., 1993;
Williams et al., 1997], whose research focuses on
the interaction between metabolic and psycholog-
ical stressors on reproductive function in female
macaques. Accordingly, we began to recognize NHPs
as models for reproductive health issues of con-
cern in humans such as stress-induced infertil-
ity and endometriosis [Schenken, 1997]. In this
decade, studies in male macaques were focused
on seasonal reproductive cyclicity [Chik et al.,
1992; Matsubayashi et al., 1991; Medhamurthy
et al., 1994], as well as on the effects of diet [Mattern
et al., 1993; Suhana et al., 1999], environmental pol-
lutants/toxins [Foster et al., 1998], and social rela-
tionships [Baker et al., 1999; Berard, 1999] on male
reproductive function, though again this realm of
research lagged behind what was known about fe-
The past 10–15 years have seen our understand-
ing of the truly integrative nature of primate repro-
ductive functioning strengthen, due in large part
to contributions from the authors in this special
issue. We now know the roles that the metabolic
et al., 2001a,b, 2007] play in female NHP fertility.
We also know more about the role of neuropeptides
and neurotransmitters in mediating the relation-
ships between various stressors and reproductive
function [Bethea et al., 2005, 2008; Centeno et al.,
2007; Cunningham et al., 2004]. During this time,
due in large part studied conducted in the field,
we have also seen a greater understanding of the
effects of kinship, social relationships, and group
dynamics in reproductive success for both male
and female NHPs [Altmann & Alberts, 2003; Fedi-
gan & Jack, 2011; Goossens et al., 2006; Klinkova
et al., 2005; Pope, 2000; Takahata et al., 2006]. This
understanding has led to a natural progression to-
ward the characterization of strategic interactions,
for example, postcopulatory mechanisms, postcopu-
latory, and extragroup mating, and even sexual co-
ercion by males, and their roles in reproductive suc-
cess [Doran-Sheehy et al., 2009; Emery Thompson
et al., 2008; Engelhardt et al., 2006; Knott et al.,
2010; Muller et al., 2007]. In the past 10–15 years,
we have also begun to learn about the heritabil-
ity of fitness in macaques [Blomquist, 2009, 2010]
while expanding our knowledge of female reproduc-
tive strategies to include behavioral and endocrine
reproductive suppression [Puffer et al., 2004; Saltz-
man et al., 2008] and selective investment in off-
spring [Fite et al., 2005]. In this decade, we also
learned more about male reproductive success with
respect to paternal care and associated neurobiol-
Duque et al., 2009; Nunes et al., 2001; Schradin
et al., 2003; Ziegler et al., 2009a,b], though not ex-
clusively; see Buchan et al. .
OVERVIEW OF THE SPECIAL SECTION
This special section is comprised of contributions
from four of the five presenters in the 2011 sympo-
sium (T.E. Ziegler, J.A. French, M. Emery Thomp-
son, and G.E. Blomquist). Like the symposium it-
self, this special issue is heterogeneous in nature in
that it comprises work performed in both New and
Old World primates, in both males and females, and
in both field and laboratory settings. Ziegler 
highlights research in her laboratory that has iden-
tified neural mechanisms underlying the social in-
fluences vis-` a-vis olfactory cues on reproductive
Am. J. Primatol.
Integrative Biology of Reproduction / 199
function and dysfunction in cotton-top tamarins
(Callithrix jacchus). French  adopts a “womb
to tomb” perspective to describe years of work in
his laboratory that has revealed the role of andro-
gens in male marmosets’ (Callithrix spp.) social phe-
notypes across the lifespan, which influence repro-
ductive function and dysfunction. Emery Thompson
 summarizes research describing the repro-
ductive ecology of wild female chimpanzees (Pan
troglodytes), with particular foci on energetics and
reproductive strategies. Finally, Blomquist 
presents an original study examining the roles of
infant genetics and maternal variance in infant sur-
vivorship in free-ranging rhesus macaques (Macaca
mulatta), using a novel quantitative genetics ap-
Together, these contributions highlight not only
the usefulness of the NHP as models for human
reproductive processes, but also the truly integra-
tive nature of the reproductive sciences. Further,
these studies underscore the notion that primatol-
multifaceted field of study. The studies presented
here yield exciting avenues for multidisciplinary
and collaborative research for future generations of
NOTE ADDED IN PROOF
manuscript by JL Cameron has been withdrawn,
and all references to it herein have been removed.
Altmann J, Alberts SC. 2003. Variability in reproductive suc-
cess viewed from a life-history perspective in baboons. Am
J Hum Biol 15:401–409.
Amann RP, Johnson L, Thompson DL, Jr., Pickett BW. 1976.
Daily spermatozoal production, epididymal spermatozoal
reserves and transit time of spermatozoa through the epi-
didymis of the rhesus monkey. Biol Reprod 15:586–592.
Arora R, Dinakar N, Prasad MRN. 1975. Biochemical changes
of the epididymis of the rhesus monkey, Macaca mulatta.
Baker JV, Abbott DH, Saltzman W. 1999. Social determinants
of reproductive failure in male common marmosets housed
with their natal family. Anim Behav 58:501–513.
Berard J. 1999. A four-year study of the association between
male dominance rank, residency status, and reproductive
activity in rhesus macaques (Macaca mulatta). Primates
Berglund L, Gebremedhin M, Lindberg B, Lilja A, Langstrom
B, Lundqvist H. 1989. Placental transfer of methionine dur-
ing protein restriction in the rhesus monkey studied by
positron emission tomography. Placent 10:387–397.
Bethea CL, Centeno ML, Cameron JL. 2008. Neurobiol-
ogy of stress-induced reproductive dysfunction in female
macaques. Mol Neurobiol 38:199–230.
Bethea CL, Pau KYF, Fox S, Hess DL, Berga SL, Cameron
JL. 2005. Sensitivity to stress-induced reproductive dys-
function linked to activity of the serotonin system. Fertil
Blomquist GE. 2009. Fitness-related patterns of genetic vari-
ation in rhesus macaques. Genetica 135:209–219.
Blomquist GE. 2010. Heritability of individual fitness in fe-
male macaques. Evol Ecol 24:657–669.
rhesus macaques (Macaca mulatta). Am J Primatol 75:238–
Boorman GA, Speltie TM, Fitzgerald GH. 1974. Urinary chori-
onic gonadotrophin excretion during pregnancy in the chim-
panzee. J Med Primatol 3:269–275.
Buchan JC, Alberts SC, Silk JB, Altmann J. 2003. True pater-
nal care in a multi-male primate society. Nature 425:179–
Bush DE, Russell LH, Jr., Flowers AI, Sorensen AM, Jr. 1975.
Semen evaluation in capuchin monkeys (Cebus apella). Lab
Anim Sci 25:588–593.
Butler H. 1966. Observations on the menstrual cycle of the
grivet monkey (Cercopithecus aethiops aethiops) in the
Sudan. Folia Primatol 4:194–205.
Cameron JL. 1997. Stress and behaviorally induced repro-
ductive dysfunction in primates. Semin Reprod Endocrinol
Cameron JL. 2003. Hormonal mediation of physiological and
behavioral processes that influence fertility. In: Wachter
KW, Bulatao RA, editors. Washington, DC: Nat Academies
Press. p 104–139.
Cameron JL, Helmreich DL, Schreihofer DA. 1993. Modula-
tion of reproductive hormone secretion by nutritional in-
take: stress signals versus metabolic signals. Hum Reprod
Centeno ML, Sanchez RL, Reddy AP, Cameron JL, Bethea
opiomelanocortin gene expression in female monkeys with
differences in sensitivity to stress. Neuroendocrinology
Chaicumpa V, Johnsen DO, Pulliam JD. 1969. Gibbon men-
strual cycle and breeding. Annual Progress Report of
Seato Medical Research Laboratories, 1968/1969. p 200–
Chandra H, Dasgupta PR, Kamboj VP, Setty BS, Chowdhury
SR, Kar AB. 1971. The nature and kinetics of biochemi-
cal response of the genital organs of ovariectomized female
rhesus monkeys to sex hormones. Contraception 4:253–
Chik CL, Almeida OFX, Libre EA, Booth JD, Renquist D, Mer-
riam GR. 1992. Photoperiod-driven changes in reproductive
function in male rhesus monkeys. J Clin Endocrinol Metab
Cunningham MJ, Shahab M, Grove KL, Scarlett JM, Plant
TM, Cameron JL, Smith MS, Clifton DK, Steiner RA. 2004.
Galanin-like peptide as a possible link between metabolism
and reproduction in the macaque. J Clin Endocrinol Metab
Doran-Sheehy DM, Fernandez D, Borries C. 2009. The strate-
gic use of sex in wild female western gorillas. Am J Primatol
Ducsay CA, Cook MJ, Walsh SW, Novy MJ. 1983. Circadian
tivity in pregnant rhesus monkeys. Am J Obstet Gynecol
Emery Thompson M. 2013. Reproductive ecology of female
chimpanzees. Am J Primatol 75:222–237.
Emery Thompson M, Stumpf RM, Pusey AE. 2008. Female
reproductive strategies and competition in apes: an intro-
duction. Int J Primatol 29:815–821.
Engelhardt A, Heistermann M, Hodges JK, Nuernberg P,
Niemitz C. 2006. Determinants of male reproductive suc-
cess in wild long-tailed macaques (Macaca fascicularis)—
male monopolisation, female mate choice or post-copulatory
mechanisms? Behav Ecol Sociobiol 59:740–752.
Am. J. Primatol.
200 / Dettmer
Erikson LB. 1963. Sex skin turgescence, vaginal smear
changes and determination of the period of ovulation in the
chimpanzee. Fertil Steril 14:273–283.
Erikson LB, Wada JA. 1970. Effect of lesions in the temporal
lobe and rhinencephalon on reproductive function in adult
female rhesus monkeys. Fertil Steril 21:434–454.
Evans CS, Goy RW. 1968. Social behaviour and reproductive
cycles in captive ring-tailed lemurs (Lemur catta). J Zool
Fazleabas AT, Verhage HG, Waites G, Bell SC. 1989. Char-
acterization of an insulin-like growth factor binding pro-
tein,analogousto humanpregnancy-associated secreteden-
dometrial alpha-1-globulin, in decidua of the baboon (Papio
anubis) placenta. Biol Reprod 40:873–885.
Fedigan LM, Jack KM. 2011. Two girls for every boy: the ef-
fects of group size and composition on the reproductive suc-
cess of male and female white-faced capuchins. Am J Phys
Ferin M. 1983. Neuroendocrine control of ovarian function in
the primate. J Reprod Fertil 69:369–381.
Fernandez-Duque E, Valeggia CR, Mendoza SP. 2009. The
biology of paternal care in human and nonhuman primates.
Annu Rev Anthropol 38:115–130.
CN. 2005. Opportunistic mothers: female marmosets (Cal-
lithrix kuhlii) reduce their investment in offspring when
they have to, and when they can. J Hum Evol 49:122–142.
Foster WG, Singh A, McMahon A, Rice DC. 1998. Chronic
lead exposure effects in the cynomologus monkey (Macaca
fascicularis) testis. Ultrastruct Pathol 22:63–71.
French JA. 2013. The role of androgenic steroids in shaping
social phenotypes across the lifespan in male marmosets
(Callithrix spp.). Am J Primatol 75:212–221.
Goossens B, Setchell JM, James SS, Funk SM, Chikhi L,
Abulani A, Ancrenaz M, Lackman-Ancrenaz I, Bruford
MW. 2006. Philopatry and reproductive success in Bornean
orangutans (Pongo pygmaeus). Mol Ecol 15:2577–2588.
Gribnau AAM. 1975. Immunologic pregnancy test in the rhe-
sus monkey (Macaca mulatta). J Med Primatol 4:65–69.
Harbert GM, Jr., Spisso KR. 1980. Biorhythms of the primate
uterus (Macaca mulatta) during labor and delivery. Am J
Obstet Gynecol 138:686–696.
Hendrickx AG. 1967. The menstrual cycle of the baboon as
determined by the vaginal smear, vaginal biopsy, and per-
ineal swelling. In: Vagtborg H, editor. The baboon in medi-
cal research. vol. 2. Austin, TX: University of Texas Press.
Hobson W, Faiman C, Dougherty WJ, Reyes JI, Winter JSD.
1975. Radioimmunoassay of rhesus monkey chorionic go-
nadotrophin. Fertil Steril 26:93–97.
Hodges JK. 1985. The endocrine control of reproduction. Symp
Zool Soc Lond 54:149–168.
Kanagawa H, Hafez ESE, Mori J, Kurosawa T, Kothari L.
1973. Cyclic changes in cervical mucus and LH levels in the
bonnet macaque (Macaca radiata). Folia Primatol 19:208–
Klinkova E, Hodges JK, Fuhrmann K, de Jong T, Heister-
mann M. 2005. Male dominance rank, female mate choice,
and male mating and reproductive success in captive chim-
panzees. Int J Primatol 26:357–384.
Knott CD, Emery Thompson M, Stumpf RM, McIntyre MH.
2010. Female reproductive strategies in orangutans, evi-
dence for female choice and counterstrategies to infanticide
in a species with frequent sexual coercion. Proc Biol Sci
Koenig A. 1995. Group size, composition, and reproductive
success in wild common marmosets (Callithrix jacchus). Am
J Primatol 35:311–317.
Kraemer DC, Cruz NCV. 1969. Collection, gross characteris-
tics and freezing of baboon semen. J Reprod Fertil 20:345–
Lang CM. 1967. The estrous cycle of the squirrel monkey
(Samiri sciureus). Lab Anim Care 17:442–451.
Laumas KR, Ahsan RK, Farooq A, Kapur MM. 1978. An ap-
proach to the control of male fertility using intravasal cop-
per implant in rhesus monkey. In: Chivers DJ, Ford HR,
editors. Recent advances in primatology. vol. 4: Medicine.
New York: Academic Press. p 193–199.
Mann DR, Gould KG, Smith MM, Duffey T, Collins DC. 1987.
Influence of simultaneous gonadotropin-releasing hormone
agonist and testosterone treatment on spermatogenesis and
potential fertilizing capacity in male monkeys. J Clin En-
docrinol Metab 65:1215–1224.
Mastroianni L, Manson WA, Jr. 1963. Collection of monkey se-
men by electroejaculation. Proc Soc Exp Biol Med 112:1025–
Matsubayashi K, Nozaki M, Suzuki J, Watanabe G, Taya K,
Katakai Y, Sasamoto S. 1991. Seasonal changes in concen-
trations of immunoreactive inhibin and testosteron in the
peripheral blood of male Japanese monkey (Macaca fuscata
fuscata). In: Ehara A, Kimura T, Takenaka O, Iwamoto M,
editors. Primatology today. Amsterdam: Elsevier Science
Publishers. p 417–418.
Mattern LG, Helmreich DL, Cameron JL. 1993. Diurnal pat-
tern of pulsatile luteinizing hormone and testosterone se-
cretion in adult male rhesus monkeys (Macaca mulatta):
influence of the timing of daily meal intake. Endocrinology
Matthews LH. 1946. Notes on the genital anatomy and physi-
ology of the gibbon (Hylobates). Proc Zool Soc Lond 116:339–
Medhamurthy R, Suresh R, Paul SS, Moudgal NR. 1994.
Correlation of seasonal changes in sperm output with en-
docrinological changes in the adult male bonnet monkey,
Macaca radiata. J Biosci 19:67–74.
Mello NK, Bree MP, Mendelson JH, Ellingboe J, King NW, Se-
hgal P. 1983. Alcohol self-administration disrupts reproduc-
tive function in female macaque monkeys. Science 221:677–
Mohanty D, Das KC. 1982. Effect of folate deficiency on the
reproductive organs of female rhesus monkeys: a cytomor-
phological and cytokinetic study. J Nutr 112:1565–1576.
Mottet NK, Shaw CM, Burbacher TM. 1985. Health risks from
increases in methylmercury exposure. Environ Health Per-
Muller MN, Kahlenberg SM, Emery Thompson M, Wrangham
RW. 2007. Male coercion and the costs of promiscuous mat-
ing for female chimpanzees. Proc Biol Sci 274:1009–1014.
Nunes S, Fite JE, Patera KJ, French JA. 2001. Interactions
among paternal behavior, steroid hormones, and parental
experience in male marmosets (Callithrix kuhlii). Horm Be-
Parkin RF, Hendrickx AG. 1975. The temporal relationship
between the preovulatory estrogen peak and the optimal
mating period in rhesus and bonnet monkeys. Biol Reprod
Pepe GJ, Albrect ED. 1984. Comparison of cortisol-cortisone
interconversion in vitro by the human and baboon placenta.
Pohl CR, Hotchkiss J. 1983. Neural control of reproductive
function in primates. Int Rev Physiol 27:147–175.
Pope TR. 2000. Reproductive success increases with degree
of kinship in cooperative coalitions of female red howler
monkeys (Alouatta seniculus). Behav Ecol Sociobiol 48:253–
Potgieter HC, Spies JH, Klein T, Thierry M, van der Watt JJ.
1985. Estrogen and progesterone receptors in the uterus of
the vervet monkey. J Recept Res 5:193–218.
Puffer AM, Fite JE, French JA, Rukstalis M, Hopkins EC, Pat-
Am. J. Primatol.
Integrative Biology of Reproduction / 201 Download full-text
the hormonal status of daughters in marmosets (Callithrix
kuhlii). Am J Primatol 64:29–37.
Purandare TV, Kholkute SD, Gurjar A, Joshi UM, Dat-
tatreyamurty B, Sheth AR, Swamy XR, Jayaraman S,
Munshi SR. 1979. Semen analysis & hormonal levels in
bonnetmacaquesadministeredEmbelia ribes berries,an in-
digenous plant having contraceptive activity. Indian J Exp
Biol 17: 935–936.
Ramaswami LS, Kumar TCA. 1965. Some aspects of reproduc-
tion of the female slender loris, Loris tardigradus lydekke-
rianus Cabr. Acta Zool 46:257–273.
Ramsey EM. 1981. Functional anatomy of the primate pla-
centa. Placenta S1:29–42.
Risler L, Wasser SK, Sackett GP. 1987. Measurement of ex-
Saltzman W, Liedl KJ, Salper OJ, Pick RR, Abbott DH. 2008.
Post-conception reproductive competition in cooperatively
breeding common marmosets. Horm Behav 53:274–286.
Schenken RS. 1997. Endometriosis in the nonhuman primate.
In: Diamond MP, Osteen KG, editors. Endometrium and
endometriosis. Oxford: Blackwell Science. p 114–120.
Schradin C, Reeder DM, Mendoza SP, Anzenberger G. 2003.
Prolactin and paternal care: comparison of three species
of monogamous New World monkeys (Callicebus cupreus,
Callithrix jacchus, and Callimico goeldii). J Comp Psychol
Shandilya L, Clarson TB, Adams MR, Lewis JC. 1982. Ef-
fects of gossypol on reproductive and endocrine functions of
male cynomolgus monkeys (Macaca fascicularis). Biol Re-
Sialy R, Chakravarti RN, Nair CR, Gupta BD. 1976. Effect
on the reproductive functions of female rhesus monkeys of
feeding irradiated wheat flour and potato diet. Int J Radiat
Biol Relat Stud Phys Chem Med 29:555–564.
Silva HPA, Sousa MBC. 1997. The pair-bond formation and
its role in the stimulation of reproductive function in fe-
male common marmosets (Callithrix jacchus). Int J Prima-
Smith CG, Asch RH. 1984. Acute, short-term, and chronic ef-
fects of marijuana on the female primate reproductive func-
tion. Natl Inst Drug Abuse Res Monogr Ser 44:82–96.
mental influences on reproductive function in female Wied’s
black tufted-ear marmosets (Callithrix kuhlii). Horm Behav
Souri SJ, Swani V. 1962. Breeding of Macaca radiata radiata
in the animal house. A preliminary report. J Anatom Soc
Suhana N, Sutyarso, Moeloek N, Soeradi O, Sri Sukmaniah
S, Supriatna J. 1999. The effects of feeding an Asian or
Western diet on sperm numbers, sperm quality and serum
hormone levels in cynomolgus monkeys (Macaca fascicu-
laris) injected with testosterone enanthate (TE) plus depot
medroxyprogesteroneacetate(DMPA). IntJAndrol 22:102–
Takahata Y, Koyama N, Ichino S, Miyamoto N, Nakamichi
M. 2006. Influence of group size on reproductive suc-
cess of female ring-tailed lemurs: distinguishing be-
tween IGFC and PFC hypotheses. Primates 47:383–
van Wagenen G. 1944/1945. Mating in relation to pregnancy
in the monkey. Yale J Biol Med 17:745–760.
Williams NI, Berga SL, Cameron JL. 1997. Mild metabolic
stress potentiates the suppressive effect of psychological
stress on reproductive function in female cynomolgus mon-
keys [Abstract]. Endocr Soc 79:226.
Williams NI, Berga SL, Cameron JL. 2007. Synergism be-
tween psychosocial and metabolic stressors: impact on re-
productive function in cynomolgus monkeys. Am J Physiol
Williams NI, Caston-Balderrama AL, Helmreich DL, Parfitt
DB, Nosbisch C, Cameron JL. 2001a. Longitudinal changes
in reproductive hormones and menstrual cyclicity in
cynomolgus monkeys during strenuous exercise training:
abrupt transition to exercise-induced amenorrhea. En-
Williams NI, Helmreich DL, Parfitt DB, Caston-Balderrama
A, Cameron JL. 2001b. Evidence for a causal role of low
energy availability in the induction of menstrual cycle dis-
turbances during strenuous exercise training. J Clin En-
docrinol Metab 86:5184–5193.
Young WC, Yerkes RM. 1943. Factors influencing the re-
productive cycle in the chimpanzee: the period of adoles-
cent sterility and related problems. Endocrinology 33:121–
Ziegler TE. 2013. Social effects via olfactory sensory stimuli on
reproductive function and dysfunction in cooperative breed-
ing marmosets and tamarins. Am J Primatol 75:202–211.
Ziegler TE, Bercovitch FB. 1990. Socioendocrinology of pri-
mate reproduction. New York: Wiley-Liss, Inc. 217 p.
Ziegler TE, Prudom SL, Zahed SR. 2009a. Variations in male
parenting behavior and physiology in the common mar-
moset. Am J Hum Biol 21:739–744.
Ziegler TE, Prudom SL, Zahed SR, Parlow AF, Wegner
F. 2009b. Prolactin’s meditative role in male parenting
in parentally experienced marmosets (Callithrix jacchus).
Horm Behav 56:436–443.
Am. J. Primatol.