Hormones and Behavior 59 (2011) 265–270

Contents lists available at ScienceDirect

Hormones and Behavior
j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / y h b e h

Differential endocrine responses to infant odors in common marmoset(Callithrix jacchus) fathers
Toni E. Ziegler ⁎, Laura J. Peterson, Megan E. Sosa, Allison M. Barnard
Wisconsin National Primate Research Center, University of Wisconsin - Madison, 1220 Capitol Court, Madison, WI 53715, USAa r t i c l e

i n f oArticle history:
Received 29 June 2010
Revised 28 November 2010
Accepted 1 December 2010
Available online 9 December 2010
Keywords:
Olfactory communication
Chemosensory
Infant odors
Testosterone
Androgens
Estrogens
Marmoset
Parentinga b s t r a c t
Olfactory cues can exert priming effects on many mammalian species. Paternally experienced marmosets,
Callithrix jacchus, exposed to direct isolated olfactory contact with their own infant's scent show rapid
decreases in testosterone levels within 20 min, whereas paternally inexperienced males do not. The
following study tests whether there is a differential steroid response to exposure of infant scent fromdependent infants (own and novel) and independent infants (own and novel). We examined the serum
levels of estradiol, estrone, testosterone, dihydrotestosterone (DHT), and combined estrogens andandrogens in eight male marmosets 20 min after exposure to isolated infant scent. Testosterone andandrogen levels combined were signiﬁcantly lower with exposure to own infant scent than a novel infant
scent when the infants were at a dependent age but not at an independent age. Estrogen levels elevatedsigniﬁcantly in response to own infant scent when the infants were at a dependent age but not at an
independent age. These results suggest that marmoset fathers are more responsive to priming cues from
related infants and hormonal responses from fathers are greatest when the infant is at a dependent age.
Published by Elsevier Inc.

Introduction
Olfactory stimuli play an important role in optimizing sex andreproductive outcome in many species. Odor cues can produce
signaling effects, such as signaling the estrous state of females(Vandenbergh, 1994), or primer effects on reproduction, such aschanges in the physiological condition of the recipient due to odor
cues (Koyama, 2004). Many primer effects have been found,including stimuli that can disrupt pregnancy [as in the Bruce affect(Bruce, 1959)], extend female estrous cycles (Lee and van der Boot,
1955), and induce estrus (Whitten, 1956), accelerate the onset ofpuberty (Vandenbergh, 1969) and increase LH levels in males(Maruniak and Bronson, 1976). However, olfactory cues may play alesser role in social relationships in primates.
Odor recognition is an important component in the maternal–
infant bond. In species such as rats, mice, sheep, goats, and rabbits,
as well as in humans, olfaction is involved in the regulation ofmaternal care of the offspring (Fleming et al., 1993; Levy et al.,
2004; Gonzalez-Mariscal and Poindron, 2002; Numan and Insel,
2003; Stern, 1989). The neonate chemosensory signal is processed
differently relative to the hormonal priming that occurs during⁎ Corresponding author. Fax: +1 608 263 3524.
E-mail address: ziegler@primate.wisc.edu (T.E. Ziegler).
0018-506X/$ – see front matter. Published by Elsevier Inc.
doi:10.1016/j.yhbeh.2010.12.001

pregnancy and parturition. The valence of the chemosensory signal
from rat neonates can cause an averse or avoidance response invirgin, non-mothers while this signal is a motivational cue formaternal behaviors in mothers (Rosenblatt and Mayer, 1995). At
parturition mothers of many mammalian species develop immediate responsiveness to olfactory cues by exhibiting maternal caretaking behaviors (Levy et al., 2004). However, large brained
primates can form maternal–infant bonds without relying primarily
on odor cues.
Parental recognition of offspring odors plays a role in determining the difference between offspring and non-offspring. Offspring
recognition by mothers to their kin has been well characterized andis a function of the MHC odor type (Yamazaki et al., 2000). Kin
recognition is an assessment of genetic relatedness, and can inferdifferential treatment of conspeciﬁcs based on cues that correlatewith relatedness (Gamboa et al., 1991). Recognition of odor signals
from offspring requires the production of the speciﬁc label and therecognition of the labels through parent learning of the odor
signature (Mateo, 2002). Less is understood about paternal offspring
recognition in biparental mammalian species. Males do not undergo
pregnancy and parturition where hormonal facilitation of brain
plasticity is produced, with neurogenesis occurring to promote
olfactory involvement in offspring recognition and facilitation of
infant care. However, neuroendocrine changes are recorded frommales of biparental species during the gestational phase of theirmate or in response to infants (Berg and Wynne-Edwards, 2002;

266

T.E. Ziegler et al. / Hormones and Behavior 59 (2011) 265–270

Brown et al., 1995; Fleming et al., 2002; Reburn and WynneEdwards, 1999; Ziegler, 2000).
The New World primates, marmosets and tamarins, areespecially reactive to olfactory scents as both stimulating effects
on behavior and priming effects on hormones. They have highly
developed circumgenital scent glands, which are under hormonal
control (Epple, 1986; Savage et al., 1988). Scent secretions canidentify individuals and determine sex and dominance status(Belcher et al., 1990) as well as activate neural pathways for sexual
arousal and increase testosterone levels in response to isolated
ovulatory scents (Ferris et al., 2004; Ziegler et al., 2005). Marmosets
and tamarins have well-deﬁned main and accessory olfactory
systems with an intact vomeronasal organ and mature sensory
neurons in their vomeronasal organ with marker proteins thatindicate their functional state (Dennis et al., 2004).
Marmoset infant odor cues may work as signaling odors in theform of recognition of offspring and as primer odors by affecting
paternal hormones. We have shown paternal recognition of infant
scent cues where father marmosets show reduced serum testosterone levels within 20 min of contact with an isolated scentstimuli (Prudom et al., 2008). Parentally inexperienced males show
no changes in testosterone levels. Testosterone responsiveness toinfant odor may indicate kin recognition and its role in the
promotion of paternal behaviors and/or the regulation of testosterone production to reduce testosterone-dependent behaviors thatare not conducive to paternal care. Testosterone responsiveness infathers has not been tested with novel infant scents where thecontrast between related and novel infants can provide information
on kin recognition and whether the priming effect on fathers is
speciﬁc to related infants.
The perception of the infant odor signal may change depending
upon the hormonal priming, as occurs in mothers for whom the signal
is a motivational cue for maternal behaviors (Rosenblatt and Mayer,1995). Older infants who are no longer dependent upon the father tocare for them may be recognized as kin but do not exert a priming
effect on the father. Chemical signals found in the scent secretions may
only be relevant when the infant is totally dependent upon being
carried.
Estrogen levels are elevated in expectant marmoset and tamarinfathers, especially during the last month of their mate's pregnancy(Ziegler et al., 2004a, 2009). Male cotton-top tamarins have highlevels of estrogens at times and these are derived from gonadal
testosterone (Ziegler et al., 2000). Our infant scent tests indicate that
testosterone levels decline within 20 min of exposure in marmoset
fathers. The mechanism is unknown but could be due to a rapid
conversion. Estrogens could act to reduce the behavioral effects ofelevated testosterone at a time when males need to be parental. In the
California mouse testosterone is aromatized to estradiol in the brain
to facilitate parental behaviors (Trainor and Marler, 2002). Aromataseactivity can increase with singing in songbirds within 30 min of thesinging onset (Remage-Healey et al., 2009). Rapid changes incirculating testosterone levels have been observed in males of various
species following social encounters (see Cornil et al., 2009 for review).
These short-acting effects are thought to be due to the non-genomic
effects of estrogens on behavior in the brain. Yet, the rapid changes incirculating testosterone might also implicate peripheral aromatasechanges of testosterone to estrogens.
The following study was designed to examine the changes inpaternal gonadal steroids due to olfactory stimuli from isolated infant
scent cues. Levels of the major estrogens, estradiol and estrone, as
well as the major androgens, testosterone and dihydrotestosterone,
were examined in parentally-experienced male marmosets to address
the following questions: 1) does relatedness inﬂuence the priming
effect of infant odors on fathers 2) does age of the infant inﬂuence themale testosterone levels and, 3) does relatedness or age affectestrogen levels in fathers?

Methods
Animals
Eight paternally experienced male common marmosets were used
for this study. They were socially housed with their mate andoffspring in the marmoset colony at the Wisconsin National Primate
Research Center. The males were between the ages of 4 and 12 years.
These males are part of the breeding colony and had sired one to eightprevious offspring prior to their current infants. Only one of thefathers had been used in our previous study on scent discrimination.
Details of male age, the family composition, and mate's pregnancy
state at the times of the studies are shown in Table 1.
Marmoset families were housed in cages that measured either
122 × 61 × 183 or 61 × 91 × 183 cm. Diet and husbandry have beenreported previously for this colony (Saltzman et al., 1994). Marmosets
were fed twice daily, between 07:00 and 08:30 am, and between
12:30 and 14:00. Water was provided ad libitum. Lighting wasregulated on a 12:12 h light/dark cycle and the humidity wasmaintained at approximately 40%. Housing conditions and olfactory
testing met the guidelines for nonhuman primates and were approvedby the Animal Care and Use Committee (IAC UC) at the University of
Wisconsin.
Scent collection
To collect a scent from an infant, the infant was removed from its
family and isolated for the short time it takes to collect the sample. As
reported in Prudom et al. (2008), a ground glass laboratory stopper
was gently rubbed in the anogenital area of the infant to remove thescent secretions that were usually mixed with urine. The stopper waswashed with 300 μl of a mixture of deoxygenated ethanol/distilledwater (50:50) to remove the scent. Scent samples were pipetted off
the glass stopper and into a micro centrifuge tube and stored at−80 °C until testing.
Infant scent was collected several days prior to testing the malewith the scent. More than one scent sample was collected from each of
the infant marmosets so that each infant could provide a scentstimulus for its own father (own) and for an unknown father (novel).
Experimental design
Eight father marmosets were tested with 3 different scentstimuli at two different ages of their offspring in a randomized
design. For the ﬁrst test, infant scent was collected at infant age 5–
10 days. Males were presented with the vehicle, own infant scent,or novel infant scent. The vehicle odor was ethanol/water presented
at the same volume as the infant scents. Males were removed fromtheir home cages in a metal nest box and then once in the testing

Table 1Age of marmoset fathers, number of offspring present and pregnancy state of his mateat the time of infant scent presentation.
Father age at
ﬁrst presentation(years)

Offspringpresent at ﬁrst
presentation

Offspringpresent at second
presentation

Female pregnancy
condition

7.3 years
12.6 years
4.4 years

3, inc. 1 infant
4, inc. 2 infants
4, inc. 1 infant

3, inc. 1 infant
4, inc. 2 infants
3, inc. 1 infant

6.0 years
4.4 years
4.2 years

7, inc. 2 infants
5, inc. 2 infants
1 infant

6, inc. 2 infants
4, inc. 1 infant
1 infant

7.5 years
5.2 years

8, inc. 2 infants
3, inc. 1 infant

8, inc. 2 infants
3, inc. 1 infant

Pregnant ~ 2 months
Pregnant ~ 3 months
Pregnant ~ 10 days
aborted 3 weeks earlier
Pregnant ~ 3 months
Pregnant ~ 3 months
Nonpregnant
aborted 3 weeks earlier
Pregnant ~ 3 months
Pregnant ~ 3 months

T.E. Ziegler et al. / Hormones and Behavior 59 (2011) 265–270

room were transferred to an identical but clean nest box without
the odors associated with his family. The testing room was isolated
from the marmoset housing rooms so males would be separated
from olfactory and auditory cues from other marmosets. Males
would sit in the nest box for 10 min to allow their olfactory system
to clear of the family's odors and then testing would begin. Testing
consisted of applying the scent onto a small wooden dowel, 3 cm indiameter, placing the dowel into the male's nest box and allowing
him to sit with the dowel for 20 min. Males were allowed to touch,lick, and smell the disc. Twenty minutes after initial presentation ofscent stimuli males were bled within 3 min to obtain 0.6 ml ofblood, received a liquid treat, and were taken back to their families.
Odor testing and blood sample collection occurred between 11:00
and 13:00. Males were tested with the three odors within a week'stime. Three to four months later males were tested again for all
three scents in a randomized design where the scents werecollected from the same infants after the infants were weaned
and independent of constant care.
Hormonal assays
All samples were centrifuged and collected as serum samples
and then stored at −80 °C until assay. Samples were analyzed in
two batches over a year's time and analyzed for testosterone (T),dihydrotestosterone (DHT), estradiol (E2) and estrone (E1) by themethod reported in Ziegler et al. (2000). An aliquot of 200 μl wasused for each sample. They were extracted by adding 300 μl waterand 5 ml diethyl ether. Samples were reconstituted in 1 ml 96:4 isooctane:ethyl acetate and the individual steroids were separated bycelite chromatography using system I (Abraham et al., 1972). Using
this system DHT is eluted in 4 ml of 10% ethyl acetate, E1 and T are
eluted in 4 ml 20% ethyl acetate and E2 is eluted in 4 ml of 40%
ethyl acetate. The eluted samples were dried and reconstituted backto 200 μl in ethanol and the individual fractions were assayed for T,
DHT, E2 and E1.
The method for measuring marmoset serum T as assayed by EIA isdescribed in Ziegler et al. (2005) at a volume of 15 μl and a 90%
recovery. The method for DHT is the same assay as for T except with
DHT standards and the sample size was 200 μl. Marmoset serum wasvalidated for DHT: serial dilutions of pooled marmoset serum wereparallel to the DHT standards (no difference in the slopes of the lines,t = −1.50, p N 0.05) and accuracy was 98.65 ± 0.42%, n = 8. The
recovery of DHT through the procedures was 86%. Coefﬁcient ofvariation (CV) was 6.24 for intra CV for two assays. Since all samples
for T, DHT, E1 and E2 were assayed in three or less assays, we report
the lab values for marmoset serum pools: Intra and inter-assay CVs for
the T EIA were 3.2 and 12.0%, n = 11.
E2 and E1 were validated and assayed with a radioimmunoassay
as described in Saltzman et al. (1998) using 200 μl amounts.
Recoveries for E2 were 97% and for E1 were 86.5%. Intra and interassay CVs for the E2 were 3.8 and 15.7% and for E1 were 6.0 and
17%, n = 11.

267

to own infant scent at dependent and independent ages, 2-tailed,
p b 0.05.
Results
Dependent age
Androgens: Testosterone levels were signiﬁcantly different between condition at the dependent age (F2,7 = 4.2, p = 0.04) whereown infant scent was signiﬁcantly lower than the vehicle and thecontrol scent (p b 0.05). DHT levels were not different by condition.
Combined androgens were signiﬁcantly different by condition(F2,7 = 4.02, p = 0.04) and levels with own infant scent weresigniﬁcantly lower than the vehicle and the novel infant scent(p b 0.05) (Fig. 1A). Estrogens: Estradiol levels were not different bycondition at the dependent age but estrone levels were nearsigniﬁcance (F2,7 = 2.99, p = 0.07) and own infant was signiﬁcantly
different from both the vehicle and the novel infant (p b 0.05). Total
estrogens were signiﬁcantly different by conditions (F2,7 = 3.41,
p = 0.05) and levels with own infant scent were signiﬁcantly higher
than the vehicle and the novel infant (Fig. 1B, p b 0.05).
Independent age
No signiﬁcant differences were found for any of the hormones orfor estrogens or androgens when the infants were of an independentage (Fig. 2). Planned comparisons of each infant scent collected fromthe infant when dependent and when independent showed signiﬁcant differences for androgen levels where androgens were signiﬁcantly lower for the dependent infant condition (Fig. 3A, t = 2.19,
p = 0.03). Estrogen levels were near signiﬁcance (Fig. 3B, t = 1.76,
p = 0.06).
Estrogen response
Estrogen levels were signiﬁcantly higher for own infants independent-aged infants. Estrogen levels were similar in fathers
during this time for both estrone and estradiol ranging between

Statistical analysis
Steroid results were recorded for each steroid per male pertreatment. Tests for normality were performed and the data had anormal distribution. There were no order effects on the randomized
steroid data. Repeated measures ANOVA with post hoc comparisons(least squares differences, LSD) was used to determine differences
between hormonal response to own, novel and vehicle fordependent infants and independent infants. Planned comparisonswere used to determine the steroid response to infant scent fromthe same infant with scents taken at different ages. Pair-wise t-tests
were used to determine signiﬁcant differences between responses

Fig. 1. The effect of infant scent exposure on mean hormone levels in marmoset fathers.
A. Androgen (testosterone + DHT) levels in fathers were signiﬁcantly lower from scentcollected from own infant aged 5–10 days. B. Estrogen (estradiol + estrone) levels in
fathers were signiﬁcantly higher from own infant scent.

268

T.E. Ziegler et al. / Hormones and Behavior 59 (2011) 265–270

Fig. 2. The effect of infant scent exposure on hormone levels in fathers exposed to infant
scents collected at an independent age (3–4 months). No signiﬁcant differences arefound in (A) androgen levels or (B) estrogen levels.

0.04 and 0.35 ng/ml and these levels are in the same range as reported
for estradiol and estrone in female marmosets during the follicularand periovulatory period (Saltzman et al., 1998).
Discussion
Marmoset fathers showed relatively quick changes in circulating
hormone levels following exposure to anogenitally-derived scents of
their infant offspring. Olfactory cues clearly distinguished between
dependent, pre-weaned related infants and unrelated, novel infants.
Dependent aged infant scent lowered testosterone and elevatedestrogens while scent from the infant when it was older was lesseffective. This ability to alter the male hormones appears to be related
to the dependence of the infant. Scent from older related offspring

Fig. 3. A comparison of marmoset father's hormonal response to his own infant scentcollected at a dependent age and again at an independent age. Androgen levels weresigniﬁcantly higher after exposure to own infant scent at the dependent age. Estrogenlevels are higher for the dependent own infant versus the independent own infant but
not signiﬁcantly.

was more variable in inducing hormonal changes in the fathers. Thissuggests that males actually perceive the scent as more relevant when
the infants are young. Hormonally primed fathers may be more
receptive to the odors of their own young infants. Alternatively, there
may be a change in the odor signature of older infants. The olfactoryhormonal system in parents may be highly tuned or highly ﬂexible toshow hormonal responses to the odor of dependent offspring but lessto the odors of independent or non-related offspring.
This study provides a powerful indicator of the olfactory/chemicalcommunication that occurs in this species. As we have seen whenmales respond to isolated scents of ovulating females (Ziegler et al.,2005), males have a rapid response of altering testosterone
production. The chemical/olfactory communication in marmosets
provides an important mechanism for maintaining the bonds
between individuals with their family groups. Olfactory cues play a
primary role in social bonding in small-brained mammals such as
rodents but are thought to play a lesser role in large-brained primates(Broad et al., 2006). Odor recognition of offspring in rodents and othersmall-brained mammals that are regulated by odor cues is short lived
compared to essential long-lasting cues in a primate with a long birth
to weaning period and continued parental care up to offspring
reproduction or longer. While primate species may use all sensory
cues to form and maintain parent–infant bonds, odor cues may still beessential for many aspects of parental care. Human mothers have beenshown to recognize their newborn infants by olfactory cues (Kaitz
et al., 1987). Human fathers are more affectionate toward children
whose smell they can identify than towards children smells that they
do not recognize (Dubas et al., 2009). As our data indicate, marmoset
fathers are highly responsive to infant scent cues and hormonal
responses are strongest when the infants are related, pre-weaned anddependent upon parental care for survival.
Marmoset fathers are very responsive to their social environment.
They are also hormonally primed for paternal care. Marmoset andtamarin fathers have hormonal and physical changes that occur prior
to and following birth of their infants (Ziegler et al., 2004a, 2009).
Males increase their weight prior to infant birth and have hormonalchanges. Following birth, prolactin increases and testosterone
decreases during weight loss. The prolactin/testosterone inverse
relationship has been well documented in biparental birds during
the breeding season versus the parenting season (Buntin, 1996;
Wingﬁeld and Goldsmith, 1990). Prolactin regulates neurogenesis in
the olfactory bulb and hippocampus in recognition of offspring inmice (Mak and Weiss, 2010). Marmoset fathers should be especially
receptive to infant cues.
Socially relevant infant scents can alter the levels of testosterone
and estradiol within 20 min of exposure. This mechanism of increased
estrogens and lowered androgens would favor more “maternal” type
behaviors from the males. It is highly likely that males need to be
responsive to many stimuli during this period since their matesusually ovulate within 10 days following birth (McNeilly et al., 1981)
and fathers are also responsible for guarding their territory from otherunrelated males (Lazaro-Perea, 2001). In fact, cotton-top tamarin(Saguinus oedipus) parentally experienced fathers show lower
testosterone levels during the infant dependence period but also
increased testosterone during their mate's periovulatory period while
the infants are still being carried (Ziegler et al., 2004b).
Estrogen levels were elevated following infant scent exposure in
our fathers. Males in this study have comparable levels to fertile
female marmosets during follicular and periovulatory periods for both
estradiol and estrone (Saltzman et al., 1998). Since males have suchhigh levels of circulating estrogens, the gonads are the most likely
source. In the cotton-top tamarin we have found that high levels ofurinary estrogens are from the gonads since treatment with agonadotropin-releasing hormone antagonist, Antide, which blocks
LH stimulation of gonadal steroidogenesis, signiﬁcantly lowers
estradiol levels and intramuscular injection of testosterone increases

T.E. Ziegler et al. / Hormones and Behavior 59 (2011) 265–270

urinary estrogens (Ziegler et al., 2000). This would most likely be thesituation for the common marmoset.
The mechanism of olfactory stimulation causing decreased androgens and increased estrogens in response to infant scent is unknown.
In rodents an increase in testosterone occurs through chemosensory
input from the main olfactory and vomeronasal systems (VNO) where
the pathways contain gonadotropin-releasing hormone (GnRH)
neurons (Blake and Meredith, 2010). Male marmoset increased
testosterone response to an ovulatory scent works through themedial preoptic area (MPOA)/anterior hypothalamus (AH) as shownby functional magnetic resonance imaging (Ferris et al., 2004). These
hypothalamic areas are the location of the GnRH neurons that activate
the LH induced increase in testosterone. GnRH neuronal activity iscontrolled by VNO-mediated chemosensory input in rodents via themedial and posteromedial cortical nuclei of the amygdala where
information is relayed to the MPOA/AH inﬂuencing behavioral andendocrine responses (Choi and Anderson, 2005; Touhara andVosshall, 2009; for review). Since scent from related dependent
infants does the opposite and lowers testosterone, it is unlikely thatthe chemosensory activation originates from this route unless there isa negative input to GnRH neurons.
It would be useful to determine aromatase activity in the gonads ofparentally experienced compared to inexperienced males. The rapid
regulation of aromatase activity is known to work in the brain to cause
estrogen actions on behaviors (Charlier et al., in press). Aromatasecatalyzes estrogen biosynthesis and is expressed in many tissues suchas the gonads, brain and adipose tissue (Boon et al., 2010). Since
estrogens are so high in circulation they may be derived more from aperipheral source than from brain aromatase. Brain and circulating
estrogens may work to promote both acute and more long-termchanges in the male's behavior.
Acknowledgments
We would like to acknowledge the expertise of the animal carestaff for their special care of the marmosets. We thank Dan Wittwer
for his consultation with steroid assays. This work was funded by the
NIH grant: HD057684 to T.E.Z. Support was also provided by
Wisconsin National Primate Research Center, RR000167 and the
University of Wisconsin's Institute of Clinical and Translational
Research, 1UL1RR025011, both from the NIH National Center for
Research Resources.
References
Abraham, G.E., Buster, J.E., Lucas, L.A., Corrales, P.C., Teller, R.C., 1972. Chromatographic
separation of steroid hormones for use in radioimmunoassay. Anal. Lett. 5,
509–517.
Belcher, A.M., Epple, G., Greenﬁeld, K.L., Richards, L.E., Kuderling, I., Smith III, A.B., 1990.
Proteins: biologically relevant components of the scent marks of a primate(Saguinus fuscicollis). Chem. Senses 15, 431–446.
Berg, S.J., Wynne-Edwards, K.E., 2002. Salivary hormone concentrations in mothers andfathers becoming parents are not correlated. Horm. Behav. 42, 424–436.
Blake, C.B., Meredith, M. 2010. Selective enhancement of main olfactory input to themedial amygdala. Brain Res. 1317, 46–59.
Boon, W.C., Chow, J.D., Simpson, E.R., 2010. The multiple roles of estrogens and the
enzyme aromatase. Prog. Brain Res. 181, 209–232.
Broad, K.D., Curley, J.P., Keverne, E.B., 2006. Mother–infant bonding and the evolution of
mammalian social relationships. R. Soc. B 361, 2199–2214.
Brown, R.E., Murdoch, T., Murphy, P.R., Moger, W.H., 1995. Hormonal responses of malegerbils to stimuli from their mate and pups. Horm. Behav. 29, 474–491.
Bruce, H.M., 1959. An exteroceptive block to pregnancy in the mouse. Nature 184, 105.
Buntin, J.D., 1996. Neural and hormonal control of parental behavior in birds. In:
Rosenblatt, J.S., Snowdon, C.T. (Eds.), Parental Care: Evolution, Mechanisms, andAdaptive Signiﬁcance. : Advances in the Study of Behavior, Vol. 25. Academic Press,
San Diego, CA, pp. 161–213.
Charlier, T.D., Cornil, C.A., Ball, G.F, Balthazart, J., 2010. Diversity of mechanisms
involved in aromatase regulation and estrogen action in the brain. Biochim.
Biophys. Acta 1800, 1094–1105.
Choi, G.B., Anderson, D.J., 2005. A nose by any other name (should smell as sweetly).
Cell 11, 550–553.

269

Cornil, C.A., Stevenson, T.J., Ball, G.F., 2009. Are rapid changes in gonadal testosterone
release involved in the fast modulation of brain estrogen effects? Gen. Comp.
Endocrinol. 163, 298–305.
Dennis, J.C., Smith, T.D., Bhatnagar, K.P., Bonar, C.J., Burrows, A.M., Morrison, E.E., 2004.
Expression of neuron-speciﬁc markers by the vomeronasal neuroepithelium in six
species of primates. Anat. Rec. A 281A, 1190–1200.
Dubas, J.S., Heijkoop, M., van Aken, M.A.G., 2009. A preliminary investigation of parentprogeny olfactory recognition and parental investment. Hum. Nat. 20, 80–92.
Epple, G., 1986. Communication by chemical signals. In: Mitchell, G., Erwin, J. (Eds.),
Part A: Behavior, Conservation and Ecology. : Comparative Primate Biology, Vol. 2.
Alan R. Liss, New York, New York, pp. 531–580.
Ferris, C.F., Snowdon, C.T., King, J.A., Sullivan Jr., J.M., Ziegler, T.E., Olson, D.P., SchultzDarken, N.J., Tannenbaum, P.L., Ludwig, T., Wu, Z., Einspanier, A., Vaughan, J.T.,
Duong, T.Q., 2004. Imaging neural pathways associated with stimuli for sexual
arousal in non-human primates. J. Neuroimaging 19, 168–175.
Fleming, A.S., Corter, C., Franks, P., Surbey, M., Schneider, B., Steiner, M., 1993.
Postpartum factors related to mother's attraction to newborn infant odors. Dev.
Psychobiol. 26, 115–132.
Fleming, A.S., Corter, C., Stallings, J., Steiner, M., 2002. Testosterone and prolactin areassociated with emotional response to infant cries in new fathers. Horm. Behav. 42,
399–413.
Gamboa, G.J., Reeve, H.K., Holmes, W.G., 1991. Conceptual issues and methodology in
kin-recognition research: a critical discussion. Ethology 88, 109–127.
Gonzalez-Mariscal, G., Poindron, P., 2002. Parental care in mammals: immediate
internal and sensory factors of control. Hormones, Brain and Behavior, vol. 1.
Elsevier, San Diego, pp. 215–298.
Kaitz, M., Good, A., Rokem, A.M., Eidelman, A.I., 1987. Mothers' recognition of theirnewborns by olfactory cues. Dev. Psych. 20, 587–591.
Koyama, S., 2004. Primer effects by conspeciﬁc odors in house mice: a newperspective in the study of primer effects on reproductive activities. Horm.
Behav. 46, 303–310.
Lazaro-Perea, C., 2001. Intergroup interactions in wild common marmosets, Callithrix
jacchus: territorial defense and assessment of neighbors. Anim. Behav. 62, 11–21.
Lee, S., van der Boot, L.M., 1955. Spontaneous pseudopregnancy in mice. Acta Physiol.
Pharmacol. Neerl. 4, 442–443.
Levy, F., Keller, M., Poindron, P., 2004. Olfactory regulation of maternal behavior inmammals. Horm. Behav. 46, 284–302.
Mak, G.K., Weiss, S., 2010. Paternal recognition of adult offspring mediated by newly
generated CNS neurons. Nat. Neurosci. 13, 753–758.
Maruniak, J.A., Bronson, F.H., 1976. Gonadotropic responses of male mice to female
urine. Endocrinology 99, 963–969.
Mateo, J.M., 2002. Kin-recognition abilities and nepotism as a function of sociality. Proc.
R. Soc. Lond. B 269, 721–727.
McNeilly, A.S., Abbott, D.H., Lunn, S.F., Chambers, P.C., Hearn, J.P., 1981. Plasma
prolactin concentrations during the ovarian cycle and lactation and theirrelationship to return of fertility post partum in the common marmoset(Callithrix jacchus). J. Reprod. Fertil. 62, 353–360.
Numan, M., Insel, T.R., 2003. The Neurobiology of Parental Behavior. Springer, NewYork.
Prudom, S.L., Broz, C.A., Schultz-Darken, N.J., Ferris, C.T., Snowdon, C.T., Ziegler, T.E.,
2008. Exposure to infant scent lowers serum testosterone in father common
marmosets (Callithrix jacchus). Biol. Lett. 6, 603–605.
Reburn, C.J., Wynne-Edwards, K.E., 1999. Hormonal changes in males of a naturallyparental and a uniparental mammal. Horm. Behav. 35, 163–176.
Remage-Healey, L., Oyama, R.K., Schlinger, B.A., 2009. Elevated aromatase activity inforebrain synaptic terminals during song. J. Neuroendocrinol. 21, 191–199.
Rosenblatt, J.S., Mayer, A.D., 1995. An analysis of approach/withdrawal processes in theinitiation of maternal behavior in the laboratory rat. In: Hood, K.E., Greenberg, G.,
Tobach, E. (Eds.), Handbook of Behavioral Neurobiology, vol. 7. Plenum Press, New
York, pp. 229–298.
Saltzman, W., Schultz-Darken, N., Schefﬂer, G., Wegner, F., Abbott, D., 1994. Social andreproductive inﬂuences on plasma cortisol in female marmoset monkeys. Physiol.
Behav. 56, 801–810.
Saltzman, W., Schultz-Darken, N.J., Wegner, F.H., Wittwer, D.J., Abbott, D.H., 1998.
Suppression of cortisol levels in subordinate female marmosets: reproductive andsocial contributions. Horm. Behav. 33, 58–74.
Savage, A., Ziegler, T.E., Snowdon, C.T., 1988. Sociosexual development, pair bondformation, and mechanisms of fertility suppression in female cotton-top tamarins(Saguinus oedipus oedipus). Am. J. Primatol. 14, 345–359.
Stern, J.M., 1989. Maternal behavior: sensory, hormonal, and neural determinants.
In: Levine, S., Brush, F.R. (Eds.), Psychoendocrinology. Academic Press, New York,
pp. 104–225.
Touhara, K., Vosshall, L.B., 2009. Sensing odorants and pheromones with chemosensory
receptors. Annu. Rev. Physiol. 71, 307–332.
Trainor, B.C., Marler, C.A., 2002. Testosterone promotes paternal behaviour in amonogamous mammal via conversion to estrogen. Proc. R. Soc. B 269, 823–829.
Vandenbergh, J.G., 1969. Male odor accelerates female sexual maturation in mice.
Endocrinology 84, 658–660.
Vandenbergh, J., 1994. Pheromones and mammalian reproduction, In: Knobil, E.,
Neill, J.D. (Eds.), The Physiology of Reproduction, second ed. Raven Press, New
York, pp. 343–359.
Whitten, W.K., 1956. Modiﬁcation of the oestrus cycle of the mouse by external stimuli
associated with the male. J. Endocrinol. 13, 399–404.
Wingﬁeld, J.C., Goldsmith, A.R., 1990. Plasma levels of prolactin and gonadal steroids inrelation to multiple-brooding and re-nesting in free-living populations of the songsparrow, Melospiza melodia. Horm. Behav. 24, 89–103.

270

T.E. Ziegler et al. / Hormones and Behavior 59 (2011) 265–270

Yamazaki, K., Beauchamp, G.K., Curran, M., Bard, J., Boyse, E.A., 2000. Parent-progeny
recognition as a function of MHC odor type identity. Proc. Natl. Acad. Sci. 97,
10500–10502.
Ziegler, T.E., 2000. Hormones associated with non-maternal infant care: a review ofmammalian and avian studies. Folia Primatol. 71, 6–21.
Ziegler, T.E., Carlson, A.A., Ginther, A.J., Snowdon, C.T., 2000. Gonadal source of
testosterone metabolites in urine of male cotton-top tamarin monkeys (Saguinus
Oedipus). Gen. Comp. Endocrinol. 118, 332–343.
Ziegler, T.E., Washabaugh, K.F., Snowdon, C.T., 2004a. Responsiveness of expectant malecotton-top tamarins, Saguinus Oedipus, to mate's pregnancy. Horm. Behav. 45, 84–92.

Ziegler, T.E., Jacoris, S., Snowdon, C.T., 2004b. Sexual communication between breeding
male and female cotton-top tamarins (Sagunius oedipus) and its relationship to
infant care. Am. J. Primatol. 61, 57–69.
Ziegler, T.E., Schultz-Darken, N.J., Scott, J.J., Snowdon, C.T., Ferris, C.F., 2005.
Neuroendocrine response to female ovulatory odors depends upon social
condition in male common marmosets, Callithrix jacchus. Horm. Behav. 47,
56–64.
Ziegler, T.E., Prudom, S.L., Zahed, S.R., Parlow, A.F., Wegner, F.W., 2009. Prolactin's
mediative role in male parenting in parentally experienced marmosets(Callithrix jaccus). Horm. Behav. 56, 436–443.