Opportunistic Mothers: Female Marmosets (Callithrix Kuhlii) Reduce Their Investment in Offspring When They Have To, and When

Journal of Human Evolution 49 (2005) 122e142

Opportunistic mothers: female marmosets (Callithrix kuhlii) reduce their investment in oﬀspring when they have to, and when they can

Jeﬀrey E. Fite a,b,*, Kimberly J. Patera b,c, Jeﬀrey A. French a,b,c, Michael Rukstalis b,c, Elizabeth C. Hopkins a,b, Corinna N. Ross b,d

a Department of Psychology, University of Nebraska at Omaha, NE 68182-0274, USA b Callitrichid Research Center, University of Nebraska at Omaha, USA c Department of Biology, University of Nebraska at Omaha, USA d School of Biological Sciences, University of Nebraska, USA

Received 17 May 2004; accepted 5 April 2005

Abstract

All female primates incur energetic costs associated with producing and caring for offspring, but females belonging to the New World primate family Callitrichidae, the marmosets and tamarins, appear to face even further demands. In fact, the energetic demands of rearing callitrichid infants are thought to have led to the evolution of cooperative infant care in these species. If this explanation is true, then one might expect that natural selection should also have shaped patterns of maternal behavior to be sensitive to the costs of reproduction and equipped females to reduce their investment in offspring under certain conditions. Therefore, we examined the maternal effort and postpartum endocrine profiles of individual female marmosets (Callithrix kuhlii) across conditions that represented two hallmarks of callitrichid reproductiondconception during the early postpartum period and alloparental assistance. When females conceived during the early postpartum period and faced the upcoming demands of caring for their newly conceived litters (Study 1), they significantly reduced their caregiving effort and had significantly higher postpartum levels of estradiol relative to breeding attempts in which conception occurred later in the postpartum period. Postpartum estradiol was negatively correlated with maternal carrying effort. When experienced alloparents were present (Study 2), females again reduced their caregiving effort relative to breeding attempts in which experienced alloparents were not present. Postpartum cortisol, however, did not vary as a function of experienced alloparental assistance. The results of these studies suggest that female marmosets have been subjected to similar selection pressures as females of other primate taxadto maximize their reproductive success by reducing their investment in offspring under the worst and best

* Corresponding author. Tel.: C1 402 5543094; fax: C1 402 5542556. E-mail addresses: jﬁ[email protected] (J.E. Fite), [email protected] (K.J. Patera), [email protected] (J.A. French), [email protected] (M. Rukstalis), [email protected] (E.C. Hopkins), [email protected] (C.N. Ross).

0047-2484/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2005.04.003 J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142 123 of conditionsdand suggest that hormones may mediate within-female variation in maternal care. These studies also provide support for the notion that mothers are ‘‘ﬂexible opportunists’’ when it comes to providing care to their young. Ó 2005 Elsevier Ltd. All rights reserved.

Keywords: Wied’s black tufted-ear marmoset; Callitrichidae; Maternal care; Postpartum conception; Lactation; Alloparental care

Introduction If the energetic demands of rearing callitrichid infants did lead to the evolution of cooperative All female primates incur energetic costs breeding in these species, then one might expect associated with producing and caring for offspring that natural selection should also have shaped (Altmann, 1983), but females belonging to the patterns of maternal behavior to be sensitive to the New World primate family Callitrichidae, the costs of caring for offspring, and equipped females marmosets and tamarins, appear to face even to reduce their investment in offspring under further energetic demands. Callitrichid primates certain conditions. Decades of research on the are the smallest (100e750 g; Fleagle, 1999)and reproductive ecology of maternal care have most fecund (Tardif, 1996) of the anthropoid revealed that female mammals, including primates, primates. Females typically produce dizygotic- are neither selfless nor indiscriminate about the twin litters, which at birth can weigh as much care they provide their young (see reviews in as 15e25% of the female’s own body weight Trivers, 1972, 1974; Clutton-Brock, 1991; Hrdy, (Kleiman, 1977). Moreover, marmosets and tam- 1999). Instead, they appear to have been shaped by arins do not exhibit lactational suppression of natural selection to be ‘‘flexible opportunists’’ ovulation (e.g., Lunn and McNeilly, 1982; French, (Hrdy, 1999), whose motivation to produce and 1983; Sousa et al., 1999). Instead, a postpartum care for their offspring appears to be contingent on ovulation occurs two to four weeks following birth complex interactions, or trade-offs, between their (e.g., Ziegler et al., 1990; French et al., 1996a), so ability to invest in current offspring and the that females can conceive while still nursing and probability of producing offspring in the future. carrying their current litter of large, twin infants. When their physical condition is poor and when These energetic demands have often been cited they have difficulty meeting their own subsistence as factors necessitating some form of assistance needs, females may sacrifice their current off- for callitrichid females (e.g., Leutenegger, 1980; spring’s fitness, and possibly survival, in favor of Garber, et al., 1984; Goldizen, 1987; Dunbar, maternal survival and the possibility of producing 1988; Wright, 1990; Price 1992c), and, indeed, offspring in the future (Clutton-Brock, 1991; cooperative rearing of offspring is a hallmark of Hrdy, 1999). There is also good reason to believe callitrichid reproduction (see review in Tardif, that females in the best physical condition, and 1996). In every species studied to date, females those with abundant resources, might also reduce share the responsibility of infant care with members their overall investment in offspring relative to of their family or social group (e.g., Cleveland and females in lesser condition and/or with fewer Snowdon, 1984; Goldizen, 1987). Breeding males resources available to them (Lee et al., 1991; and alloparents (i.e., older offspring and/or non- Fairbanks and McGuire, 1995; Hrdy, 1999). related individuals living in the family group) play Without jeopardizing offspring survival, these an active role in every aspect of infant care, except females can improve their own physical condition for nursing (e.g., Cleveland and Snowdon, 1984; and prepare for future breeding attempts by Goldizen, 1987), and the timing and/or extent of providing offspring with the necessary resources their involvement appears to be controlled by in less time and with less effort than other mothers. females (Schradin and Anzenberger, 2003). Thus, one might expect that callitrichid primates 124 J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142 have been subjected to similar selection pressures parturient and/or sibling-rearing experience, ma- as other mammalian taxa, albeit within the context ternal carrying effort is not correlated with the of their unique reproductive system, to maximize number of previous litters females had produced their reproductive success by reducing their in- (Fite and French, 2000). Washabaugh et al. (2002) vestment in offspring under the worst and best of examined the parental effort of cotton-top tamar- conditions. If this is true, it seems likely that ins with sibling-rearing experience and found that natural selection should have favored callitrichid maternal carrying effort did not vary with female females equipped to relinquish infant care to other parity. In fact, the carrying effort of females that caregivers within their family group, and thereby had produced at least three sets of surviving litters reduce their behavioral investment in their current did not differ significantly from less experienced litters, under two conditions: 1) when conception females that had produced one or fewer surviving occurred during lactation and infant carrying, and litters. Among golden lion tamarins with sibling- 2) when alloparental assistance for rearing off- rearing experience, neither parity nor age ac- spring was available. To the best of our knowl- counted for a significant portion of variance in edge, however, within-female shifts in callitrichid maternal carrying effort (Bales et al., 2002). caregiving effort in response to these conditions During the first postpartum week, primiparous have not been previously explored. females exhibited a carrying rate (71.7 G 17%) What proximate mechanisms might have been that was only slightly less than that of multiparous shaped by natural selection to regulate within- females (73.1 G 6.5%). Experiential factors, there- female variation in callitrichid maternal behavior? fore, appear to be unlikely candidates for mech- One possibility is that experiential factorsdwhich anisms regulating within-female variation in include the experiences of pregnancy, parturition, callitrichid maternal care. and rearing one’s own offspring, as well as the A second possibility is that physiological experience of providing care to siblingsdmight factorsdwhich include the hormonal changes that facilitate within-female changes in maternal moti- accompany pregnancy, parturition, and lacta- vation to care for offspring. Experiential factors tiondmight facilitate within-female variation in are known to exert long-lasting, if not permanent, callitrichid maternal behavior and responsiveness. enhancement effects on female primates’ motiva- Primate maternal care was long thought to be tion to care for offspring (see review in Coe, 1990), relatively independent of endocrine processes (e.g., and callitrichid females are no exception. Parturi- Coe, 1990; Pryce, 1992, 1996; Maestripieri, 1999). ent and sibling-rearing experience have been However, recent correlational and experimental shown to positively impact the expression of studies have implicated hormonal factors in the competent and nurturing maternal care and regulation of maternal competency and caregiving greatly improve infant survivorship in a variety motivation in a number of primate species (e.g., of callitrichid species (e.g., black lion tamarins, humans, Homo sapiens: Fleming et al., 1997a; Leontopithecus chrysopygus: French et al., 1996b; Japanese macaques, Macaca fuscata: Bardi et al., common marmosets, Callithrix jacchus: Tardif 2003b; pigtail macaques, M. nemestrina: Maestri- et al., 1984; cotton-top tamarins, Saguinus oedipus: pieri and Zehr, 1998; rhesus macaques, Kirkwood et al., 1983; Tardif et al., 1984; Bardi M. mulatta: Holman and Goy, 1995; savannah et al., 2001; golden lion tamarins, L. rosalia: baboons, Papio hamadryas: Bardi et al., 2004; Hoage, 1978; French et al., 1996b; golden-headed western lowland gorillas, Gorilla gorilla gorilla: lion tamarins, L. chrysomelas: French et al., 1996b; Bahr, 1995), including marmosets and tamarins saddleback tamarins, S. fuscicollis: Epple, 1975). (e.g., common marmosets: Pryce, 1993; Pryce Once the prerequisite experience is gained, how- et al., 1993, 1995; red-bellied tamarins, S. labiatus: ever, experiential factors appear to exert little Pryce et al., 1988; Pryce, 1993; Wied’s black impact on future variability in the expression of tufted-ear marmosets: Fite and French, 2000). infant caregiving behavior. For example, among There is also good reason to believe that within- Wied’s black tufted-ear marmosets (C. kuhlii)with female variation in callitrichid maternal caregiving J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142 125 effort corresponds to within-female variation in administer veterinary care. We also limited their endocrine status. Utilizing a within-subjects de- exposure to unfamiliar humans. For further details sign, Fite and French (2000) compared the of animal housing and husbandry, see Schaffner endocrine profiles and caregiving effort of female et al. (1995). Wied’s black tufted-ear marmosets when their infants did, and did not, survive a minimum of two Behavioral measures weeks postpartum. Females exhibited significantly higher prepartum levels of the sex steroid hormone Observations of parental caregiving behavior estradiol (E2), and significantly less infant-carrying were conducted from August 1996 through August effort, when their infants did not survive relative to 2001. Our observational protocol employed the when the same females’ infants did survive. ‘‘all-occurrences’’ recording technique (Martin and Additionally, prepartum E2 levels were signifi- Bateson, 1993) using the Observer 3.0 (Noldus cantly, and negatively, correlated with postpartum Information Technology, Leesburg, VA, USA) carrying effort. To date, however, potential computerized behavioral recording program. relationships between peripartum hormones and Family groups were observed for 20 min five times opportunistic, within-female shifts in maternal per week for the first nine weeks of infant life (total caregiving effort have not been assessed. For that observation time per litter, across nine reason, in this investigation we assessed within- weeks Z 15 hr; total observation time for Studies female changes in the caregiving behavior and 1 and 2 Z 360 hr). Observations were conducted at endocrinological profiles of female marmosets randomly selected times between 0800 and across conditions that represented conception 1600 hr, but never less than 1 hr preceding, or during the early postpartum period (Study 1), subsequent to, the morning feeding. All behavioral and the opportunity to relinquish infant care to observations were conducted by one individual experienced alloparents (Study 2). (J.E.F.), with whom the animals were familiar. The observer sat approximately 2 m from each cage, and began conducting a behavioral observation General methods after a 10 min habituation period. Four forms of infant caregiving behavior were recorded: 1) Infant Subjects and housing carrying: when one or more infants clung to the body or pelage of a parent; 2) Infant acquisition: The subjects of these studies consisted of adult when a parent actively transferred an infant from female C. kuhlii, and their families, housed at the another carrier to itself with no resistance from the University of Nebraska at Omaha’s Callitrichid current carrier; 3) Infant rejection: when a parent Research Center. Marmosets were housed in wire removed an infant onto enclosure-wire or some mesh enclosures with wooden frames other substrate (other than another animal) by (1.6 ! 0.9 ! 2.4 m). Each enclosure contained biting, pulling, or rubbing; and 4) Infant grooming: a removable transport cage, natural branches, when a parent licked an infant’s body, and when a feeding platform, a nest box, and a variety of a parent manipulated an infant’s pelage by parting enrichment devices. A 12 hr:12 hr light:dark cycle its hair with its hands and removed particles with was controlled by automatic timers, with light the hands or mouth. onset occurring at 0800 hr. Enclosures containing Given that infant carrying is likely the most neighboring groups were at least 1 m apart. costly form of investment that mothers can Adjoining groups were denied visual, but not relinquish to others, we hypothesized that mater- auditory or olfactory contact. Our routine hus- nal carrying effort would be the form of maternal bandry practices were designed to minimize, as investment most sensitive to maternal energetics much as possible, any disturbance to the normal and resource availability (i.e., alloparents). No day-to-day activities of the animals. The marmo- distinction was made as to whether females and sets were handled only when it was necessary to males carried one versus two infants, because 126 J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142 infants born into large social groups are not resources are low and/or body condition is generally carried by the same individual (cotton- challenged (Clutton-Brock, 1991; Lee et al., top tamarins: Price, 1992c), and because there is 1991), then we predicted that marmoset females evidence that there are few additional energetic would invest less in their current litters when they costs associated with carrying more than one conceived during the period of critical infant infant at a time (e.g., Saddle-back tamarins, dependence (DPCID) than when they conceived S. fuscicollis: Goldizen, 1987; cotton-top tamarins: after the period of critical infant dependence Price, 1992c). We should note, however, that (APCID). More specifically, we expected that Schradin and Anzenberger (2001) reported a neg- conception DPCID, the time of maximal maternal ative correlation between carrying weight and the involvement in infant care, represents a cue for distance marmosets could leap, such that an upcoming energetic demands, as well as an animal carrying two infants might have greater opportunity for females to make a behavioral difficulty foraging and avoiding predators than an trade-off between investment in current versus animal carrying one infant. We recorded rates of future offspring. By investing less time and/or infant acquisition and infant rejection because we energy in their current litters, females might be expected that these behaviors would be good better prepared to nurse and carry their newly indicators of maternal tolerance and motivation conceived litters. Furthermore, it seems likely that to spend time in contact with infants. We recorded the cooperative breeding system that is a trade- rates of infant grooming because grooming is mark of callitrichid reproduction and sociality (see likely to be much less costly than infant carrying. review in Tardif, 1996) should allow females to We did not record nursing time, due to the make such trade-offs without any loss of fitness to difficulty in distinguishing between ‘‘time on the the current litters, because breeding males and nipple’’ and suckling. alloparents are clearly equipped to assist them in every form of infant care, except nursing (e.g., Urine collection Cleveland and Snowdon, 1984; Goldizen, 1987; Tardif, 1996). We collected urine samples two to five times per To assess the possibility that the endocrine week from all of the breeding female and male changes accompanying pregnancy might serve as marmosets in this study. A noninvasive, stress-free cues for the upcoming costs of rearing newly collection procedure previously described (French conceived litters, we evaluated the postpartum et al., 1996a) was utilized. Urine samples were excretion of urinary E2. Given previously de- collected between 0600 and 0800 hr, centrifuged at scribed increases in levels of urinary E2 that are 7000 rpm for 2 min to remove detritus, and the expected to follow conception (Wied’s black supernatant was then transferred to a clean mini- tufted-ear marmosets: Fite and French, 2000), we vial for storage. All of the samples collected were predicted that females would exhibit higher levels catalogued and stored at ÿ20 C until assayed. of postpartum urinary E2 when they conceived DPCID relative to breeding attempts in which they conceived APCID. Moreover, we predicted Study 1: Postpartum conception and maternal care that elevated levels of E2 would be associated with decreased maternal effort. In Study 1, we evaluated the sensitivity of patterns of maternal care to impending costs Methods associated with the rearing of offspring, and tested the prediction that females would opportunistically Subjects reduce their investment in offspring when energetic The selection criterion for individuals to include constraints required them to do so. If females in this study was the timing of females’ postpartum reduce their investment in current offspring in conception. We identified adult females (n Z 6) favor of future reproductive attempts when who gave birth to surviving litters followed by J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142 127 conception DPCID and APCID. All APCID intensive during this time period. Weeks 4e6 conceptions were preceded by normal ovulatory postpartum are a transitional period for infants functioning, as assessed by urinary PdG levels (see in which locomotion and feeding becomes in- ‘‘Identification of Conception’’ below). All DPCID creasingly independent (common marmosets: and APCID conceptions resulted in surviving, full- Tardif et al., 1998). By weeks 7e10 postpartum, term litters. When more than one DPCID or marmoset infants exhibit locomotion that is APCID conception occurred for a female, we completely independent, as well as independent randomly selected one conception per female. feeding, although some nursing can still occur. To distinguish between DPCID and APCID Therefore, we presumed females to be maximally conditions, we relied on Tardif et al.’s (1998) involved in the rearing of their current litters when identification of three distinct phases of early conception occurred DPCID, and less involved infant development, which emphasizes infants’ when conception occurred APCID. reliance on caregivers for nutrition and transport. Demographic data for the females in Study 1 For this study, conception DPCID was operation- are presented in Table 1. We used paired t-tests ally defined as conception during the first three and a chi-square test to compare these variables weeks postpartum because infants exhibit very across conditions. Individual females did not differ little, if any, independent feeding or locomotion significantly in age between DPCID and APCID during this time (common marmosets, C. jacchus: conditions (t(5) Z 0.57, NS), nor did their litter Tardif et al., 1998). During this phase of infant sizes (X2(1) Z 0.00, NS). Neither the number of development, marmoset females nurse their infants potential alloparents nor the number of experi- every few hours (common marmosets: Missler enced alloparents present to assist each female in et al., 1992), and infants are carried more than the rearing of offspring differed significantly 90% of the time by the adult female and other between conditions (number of potential allopar- caregivers (common marmosets; cotton-top tam- ents: t(5) Z ÿ0.42, NS; number of experienced arins; golden lion tamarins, Leontopithecus rosalia; alloparents: t(5) Z 0.76, NS). Further, the age of saddle-back tamarins; silvery marmosets, C. ar- females’ male partners did not vary significantly gentata; see review in Tardif et al., 1993). This care between DPCID and APCID conditions is energetically costly for females. Lactation is the (t(5) Z 0.56, NS). most energetically expensive component of re- Each of the parents examined had experience production for female mammals (see review in caring for infants prior to the commencement of Gittleman and Thompson, 1988), and callitrichid this study. All six females and their male partners females have been observed to lose weight (cotton- had extensive sibling-rearing experience as allo- top tamarins: Sańchez et al., 1999) and signifi- parents. Three females (Bas, Jin, Pix) and their cantly increase their energetic intake (cotton-top male partners had experience rearing their own tamarins: Kirkwood and Underwood, 1984; sad- offspring. dle-back tamarins: Goldizen, 1987) during lactation. Carrying callitrichid infants comes at a 21% Hormone assays. Concentrations of E2 and PdG in increase in the caloric cost (per minute) of postpartum urine samples were determined using traveling (Tardif, 1996). Infant transport is also enzyme immunoassays described and validated for associated with other costs, such as decreased use with C. kuhlii in prior work (E2: Fite and foraging and feeding time (e.g., saddle-back French, 2000; PdG: French et al., 1996a). E2 was tamarins: Goldizen, 1987; cotton-top tamarins: extracted from samples with diethyl ether before Price, 1992c; also see review in Tardif, 1994)and performing assays (Fite and French, 2000). We increased risk of predation (cotton-top tamarins: measured hormone concentrations in 12 E2 assays Price, 1992c; see review in Tardif, 1994). Concep- and 12 PdG assays. Intra-assay coefficients of tion APCID was operationally defined as concep- variation, determined from duplicate evaluations tion four weeks following birth, and later, as of pooled marmoset urine run between assays, maternal caregiving effort is not expected to be as were 2.03% and 6.91% for high concentration 128 J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142

pools and 7.34% and 11.15% for low concentra- 0.33 tion pools in E2 and PdG assays, respectively. G Interassay coeﬃcients of variation, also determined from evaluations of pooled marmoset urine APCID Concept. 0.40/0.67 run within assays, were 5.50% and 6.48% for high

G concentration pools and 9.64% and 17.87% for low concentration pools in E2 and PdG assays, respectively. All hormone concentrations were

0.61 1.83 corrected for the creatinine concentration of each G sample. Creatinine concentrations were measured by a modified Jaffeénd-point assay (Tietz, 1976), of experienced alloparents C. kuhlii

DPCID previously described and validated for Concept. 0.21/1.33

G (French et al., 1996a).

14 days postpartum). Identiﬁcation of conception. We monitored moth- e

0.21 1.67 ers’ urinary PdG concentrations across the ﬁrst

G nine weeks of infant life. French et al. (1996a) APCID Concept. previously described the pattern of urinary PdG excretion throughout the reproductive cycle in C.

0.21 1.67 kuhlii, and these parameters were used to G determine the postpartum week during which DPCID Concept. conception occurred. Although there were inter- individual diﬀerences in urinary PdG concentra- 1.42 1.67 tions, qualitative changes in PdG proﬁles across G

APCID the postpartum period were similar among females Concept. in each condition. Elevated urinary PdG excretion, above early postpartum levels, was indicative of 1.49 6.61

G postpartum ovulation. For nonconceptive cycles, DPCID Concept. PdG levels returned to preovulatory follicular levels within 25 days (mean duration in days from

0.61 6.76 successive luteinizing hormone (LH) peaks:

G 24.9 G 0.60 days; French et al., 1996a). For APCID Concept. conceptive cycles, there was a rapid elevation in urinary PdG excretion during the first 30 days of 0.77 4.47 pregnancy, and PdG levels remained high for the G Female age (yr) Male age (yr) Litter size Number of alloparents/number first two trimesters of pregnancy (mean first DPCID Concept. trimester urinary PdG levels: 33.7 G 8.4 mg/mg

a Cr; mean second trimester urinary PdG levels: 0.67 4.63 G m

G 39.0 10.9 g/mg Cr; mean gestation length:

APCID G

Concept. 143.1 1.6 days; French et al., 1996a). The timing of each female’s conceptions is presented in

0.00 6.50 Table 1. conception G (postpartum week) DPCID Concept. Statistics. To compare levels of investment in offspring when females conceived DPCID versus SE 2.00 APCID, 3-way mixed ANOVAs (sex ! condi- G ! Postpartum week during which conception occurred (e.g., conception during week two postpartum occurred 8 tion weeks) were conducted on infant carrying a Female ID Timing of Table 1 Demographic data for mothers when they conceived DPCID and APCID BasBonJinLucPixXux 2 2Mean 2 2 9 2 2 4 7 6 3.00effort, 7 7.33 6 5.05 4.48 3.42 infant 6.91 5.78 2.11 4.63 3.56 2.39 acquisition, 12.97 5.36 2.96 8.43 4.58 2.82 12.55 6.42 5.74 8.01 infant 3.66 2 2 6.01 6.58 1 rejection, 1 2 1 2 2 2 2 and 2 1 2/0 2/1 1/2 1/4 2/1 2/0 3/1 1/1 1/0 2/0 1/0 3/2 J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142 129 infant grooming. As breeding males are not faced Conception DPCID (n = 6) with the same energetic demands as mothers, 40 Conception APCID (n = 6) males were included in these analyses as a control 30 Females for factors other than female reproductive ener- 20 getics that may be influenced by the timing of the 10 postpartum conception. To compare concentra- 0 tions of urinary E2 when females conceived DPCID and APCID, a 2-way repeated measures 40 ANOVA (condition ! week postpartum) was con- 30 Males

ducted. We used Pearson correlation coefficients to Infant Carrying (min/hr) 20 examine the relationship between postpartum 10 hormone levels and maternal behavior. Post hoc 0 analyses were conducted using the Tukey test 123456789 (Keppel, 1991), and an a level of 0.05 was adopted Weeks Postpartum for all statistical tests. All data are presented as Fig. 1. Mean (GSE) infant carrying effort for females and X G SE. males across the first nine weeks of infant life, when females conceived DPCID and APCID. Results transport. Rates of infant acquisition differed Postpartum conception and maternal caregiving significantly among weeks (F(8, 80) Z 9.47, behavior. Maternal carrying effort was influenced p ! 0.001), such that parents were significantly by the timing of the postpartum conception. In more likely to acquire infants from other family fact, a significant interaction between sex, concep- members during the first four weeks postpartum. tion, and weeks (F(8, 80) Z 2.16, p ! 0.05) in- Rates of acquisition during weeks 1e4 postpartum dicated that the carrying effort of females and (week 1: 0.87 G 0.18 /hr; week 2: 0.71 G 0.20 /hr; males was differentially influenced by conception week 3: 0.88 G 0.12 /hr; week 4: 0.96 G 0.17 /hr) DPCID versus APCID. When females conceived were significantly higher than during weeks 7e9 DPCID, their carrying effort at week two post- postpartum (week 7: 0.11 G 0.06 /hr; week 8: partum was significantly less than their carrying 0.00 G 0.00 /hr; week 9: 0.00 G 0.00 /hr; p ! 0.05). effort when they conceived APCID (Fig. 1; Rates of acquisition did not, however, vary as p ! 0.05). Further, when females conceived a function of the timing of the postpartum DPCID, their carrying effort at every time-point conception (F(1, 80) Z 0.53, NS). was significantly less than their effort at week one Parents rejected infants with the greatest fre- postpartum (p ! 0.05). In contrast, female carry- quency during the period of infant transition to ing effort slowly declined across the postpartum independent feeding and locomotion. Rates of period when females conceived APCID, with the infant rejection differed significantly between weeks only statistical difference occurring between weeks (F(8, 80) Z 9.47, p ! 0.001), such that rates of six and seven postpartum (p ! 0.05). Male carry- rejection increased across weeks 1e5 postpartum ing effort did not vary as a function of the timing of and decreased across weeks 6e9 postpartum. The conception (Fig. 1). Because the significant in- rate of infant rejection at week five postpartum teraction between sex, conception, and weeks (1.42 G 0.27 /hr) was significantly higher than at indicated that these variables did not act alone to weeks 1e4 (week 1: 0.04 G 0.04 /hr; week influence carrying effort, significant main effects 2: 0.00 G 0.00 /hr; week 3: 0.43 G 0.21 /hr; week will not be addressed. 4: 0.43 G 0.21 /hr) and 7e9 postpartum (week 7: Parental motivation to be in contact with 0.86 G 0.26 /hr; week 8: 0.34 G 0.13 /hr; week 9: infants was most pronounced during the first few 0.17 G 0.08 /hr; p ! 0.05). Rates of rejection did weeks of infant life, when infants were most not vary as a function of the timing of the dependent on their caregivers for nutrition and postpartum conception (F(1, 80) Z 0.43, NS). 130 J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142

Variation in infant grooming was independent Conception DPCID (n = 6) of weeks and female reproductive status. Groom- Conception APCID (n = 6) ing effort did not differ significantly among weeks 60 (F(8, 80) Z 1.80, NS). Furthermore, it did not differ as a function of the timing of the postpartum 40 conception (F(1, 80) Z 1.37, NS). (µg/mg Cr) 2 Postpartum conception and urinary E2 E 20 excretion. Urinary E2 excretion, which varied across the postpartum period, was related to the 0 timing of conception and the expression of 123456789 maternal caregiving behavior. Urinary E2 concen- Weeks Postpartum trations varied significantly among weeks (F(8, G Z ! Fig. 2. Mean ( SE) weekly concentrations of E2 in the urine of 40) 6.65, p 0.001). At week one postpartum, females across the first nine weeks of infant life, when they urinary E2 was significantly lower than at any conceived DPCID and APCID. other postpartum time point (10.24 G 1.527 mg/mg Cr; p ! 0.05); E steadily increased across the 2 Z postpartum period, reaching its highest level at (p 0.07). When conception occurred APCID, week nine postpartum (46.01 G 5.56 mg/mg Cr). maternal caregiving effort was not found to be When females conceived DPCID, their overall significantly related to urinary E2 levels for any female. urinary E2 concentrations were significantly higher (32.00 G 3.03 mg/mg Cr) than at breeding attempts in which these same females conceived APCID (19.50 G 3.23 mg/mg Cr; F(1, 5) Z 9.07, p Z 0.03). Study 2: Alloparental assistance and Although the main effect of the timing of maternal care conception was significant and the interaction between weeks and conception was not, different In Study 2, we evaluated the sensitivity of E levels for females in each condition can be patterns of maternal care to the opportunity to 2 relinquish infant care to other family members. We accounted for by postpartum changes in E2 excretion that occurred after week one postpartum also tested the prediction that females would (Fig. 2). opportunistically reduce their investment in their current litters, perhaps in favor of future offspring, Urinary E2 excretion during the postpartum period was related to concurrent maternal behavior when they can. Previous investigations of the when conception occurred DPCID. Overall, fe- impact of alloparental assistance on callitrichid males’ weekly postpartum urinary E2 concentrations were negatively and significantly correlated Table 2 with their concurrent carrying effort (r(108) Z Correlations between weekly postpartum urinary E2 excretion ÿ0.30, p ! 0.003). However, examination of in- and concurrent maternal carrying effort for females, when dividual Pearson correlation coefficients (Table 2), conception occurred DPCID and APCID by female and condition, reveals that the relation- Female ID Conception DPCID Conception APCID ship between E2 and maternal effort varied by nr pnr p condition. When conception occurred DPCID, the Bas 9 ÿ0.34 0.38 9 ÿ0.27 0.49 maternal caregiving effort of all six females de- Bon 9 ÿ0.87 0.003 9 ÿ0.50 0.17 creased as urinary E2 levels increased. For four Jin 9 ÿ0.75 0.02 9 ÿ0.50 0.18 females (Bon, Jin, Luc, Xux), the relationship Luc 9 ÿ0.72 0.03 9 0.20 0.61 between urinary E levels and carrying effort was Pix 9 ÿ0.63 0.07 9 ÿ0.51 0.16 2 Xux 9 ÿ0.77 0.02 9 0.53 0.14 significant (p ! 0.05). For one female (Pix), this relationship approached statistical significance Mean r ÿ0.68 ÿ0.17 J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142 131 maternal care have produced mixed results (see postpartum CORT has been positively associated review in Bales et al., 2000). Although studies have with affectionate contact with infants (Fleming indicated that females reduce their caregiving et al., 1997b), as well as maternal responsiveness to effort when alloparental assistance is available infant cues (Stallings et al., 2001). (e.g., cotton-top tamarins: Cleveland and Snow- don, 1984; Ziegler et al., 1990; golden lion tamarins: Bales et al., 2002), there are also reports Methods that females are unaffected by the presence of alloparents (e.g., black lion tamarins, L. chrys- Subjects. The selection criterion for individuals to opygus: Santos et al., 1997; cotton-top tamarins: include in this study was the presence or absence of Tardif et al., 1990; golden lion tamarins and experienced alloparents within females’ family golden-headed lion tamarins, L. chrysomelas: groups. We identified adult female C. kuhlii, Santos et al., 1997). Moreover, contradictory to housed with their male partners, to which surviv- what one might expect, some females might even ing, full-weight twin-litters were born. We then spend more time carrying infants as group size identified females (n Z 6) who gave birth to one increases and more alloparents are present (e.g., litter when no experienced alloparents were Wied’s black tufted-ear marmosets and Geoffroy’s present in the family group, and one litter when marmosets, C. geoffroyi: Santos et al., 1997). We experienced alloparents were present. When more predicted that, if females do, in fact, reduce than one ‘‘with experienced alloparents’’ or investment in current offspring in favor of future ‘‘without experienced alloparents’’ reproductive reproductive attempts when resources allow them attempt occurred for a female, we randomly to do so (Lee et al., 1991), then marmoset females selected one reproductive event per female. Five would invest less in their current litters when reproductive attempts from four females in Study experienced alloparents were present. 1 were included in this study. To assess the possibility that endocrine changes In light of numerous reports that competent associated with the presence of experienced helpers caregiving behavior increases with age (e.g., might be associated with predicted decreases in common marmosets: Ingram, 1977; Tardif et al., maternal behavior, we also examined patterns of 1986; cotton-top tamarins: Tardif et al., 1986, postpartum urinary cortisol (CORT) excretion in 1992; Price, 1991, 1992b; but also see Achenbach individual females when they did and did not have and Snowdon, 1998; saddle-back tamarins: Epple, experienced alloparental assistance. Previous re- 1975) and experience (e.g., common marmosets: ports have indicated that marmoset family mem- Tardif et al., 1984; cotton-top tamarins: Tardif bers can be a source of comfort or stress, which is et al., 1984; Johnson et al., 1991; Washabaugh reliably reflected in urinary CORT excretion et al., 2002; but also see Achenbach and Snowdon, (Smith and French, 1997a,b; Smith et al., 1998). 1998; golden lion tamarins: Hoage, 1978; saddle- Therefore, we expected that females’ CORT levels back tamarins: Epple, 1975), alloparents must would be affected by the presence of experienced have been present for the birth of at least one litter alloparents, although we made no specific pre- of younger siblings, and at least one year of age, to diction regarding the direction of change. Such be considered experienced. The mean number of socially mediated changes in CORT excretion previous litters to which alloparents had been might impact the expression of maternal caregiv- exposed was 2.50 G 0.56 litters. The mean age of ing behavior. In western lowland gorillas (Gorilla experienced helpers was 1.26 G 0.07 yr. gorilla gorilla), postpartum CORT has been Table 3 presents demographic data for the associated with reduced maternal responsiveness females in Study 2. As in Study 1, we used paired (Bahr et al., 1998), and in Japanese macaques t-tests and a chi-square test to compare these (Macaca fuscata) postpartum CORT is associated variables across conditions. The age of individual with more rejecting mothering styles (Bardi females differed significantly between our ‘‘with’’ et al., 2003a). Among human females, however, and ‘‘without’’ experienced alloparents conditions 132 J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142

Table 3 Demographic data for mothers with and without experienced alloparental assistance Female ID Female age (yr) Male age (yr) Litter size Number of Timing of experienced conception alloparents (postpartum week)a Without With Without With Without With Without With exp. exp. exp. exp. exp. exp. exp. exp. alloparents alloparents alloparents alloparents alloparents alloparents alloparents alloparents Bas 3.00 3.42 2.39 2.82 2 2 1 8 2 Ind 3.55 5.14 3.62 5.21 2 2 4 8 2 Jin 4.63 5.05 8.01 8.43 2 1 2 2 7 Luc 3.15 4.48 3.25 4.58 2 1 4 2 7 Pix 5.36 5.78 6.01 6.42 2 2 1 2 7 Xux 2.11 3.44 5.74 7.07 2 2 3 6 2 Mean G SE 3.63 G 0.48 4.55 G 0.39 4.84 G 0.86 5.75 G 0.81 2.00 G 0.00 1.67 G 0.21 2.50 G 0.56 4.67 G 1.23 4.50 G 1.12 a Postpartum week during which conception occurred (e.g., conception during week two postpartum occurred 8e14 days postpartum).

(t(5) Z 4.06, p ! 0.01). Females were older when Pix) and their male partners had experience they had experienced alloparents living in their rearing their own offspring. family groups than when they did not have experienced alloparents living in their family Hormone assays. Concentrations of CORT in groups (mean age with experienced alloparents: postpartum urine samples were determined using 4.55 G 0.39; mean age without experienced allo- enzyme immunoassays described and validated for parents: 3.63 G 0.48). The age of females’ male use with C. kuhlii in prior work (Smith and partners also varied significantly between condi- French, 1997a). We measured hormone concen- tions (t(5) Z 4.06, p ! 0.01). Males were older trations in 12 assays. Intra-assay coefficients of when they had experienced alloparents living in variation, determined from duplicate evaluations their family groups than when they did not have of pooled marmoset urine run within assays, were experienced alloparents living in their family 3.59% for high concentration pools and 6.99% for groups (mean age with experienced alloparents: low concentration pools. Interassay coefficients of 5.75 G 0.81; mean age without experienced allo- variation, also determined from evaluations of parents: 4.84 G 0.86). These differences in age pooled marmoset urine run between assays, were were not entirely unexpected, because, in our 3.46% for high concentration pools and 9.69% for colony, alloparents were always older offspring low concentration pools. All hormone concentra- residing within their natal groups. As breeding tions were corrected for the creatinine concentra- males and females aged, and their families tion of each sample. Creatinine concentrations naturally grew in size, the number of alloparents were measured by a modified Jaffeénd-point assay present increased. Neither litter sizes nor the (Tietz, 1976), which was previously described and timing of females’ postpartum conceptions varied validated for C. kuhlii (French et al., 1996a). significantly between conditions (litter size: X2(1) Z 2.40, NS; timing of conception: Statistics. To compare levels of investment in t(5) Z 0.07, NS). offspring when experienced alloparental assistance Each of the parents in this study had experience was and was not available to females, 3-way mixed caring for infants, even in the ‘‘without experi- ANOVAs (sex ! condition ! weeks) were con- enced alloparents’’ condition. All six females, and ducted on infant carrying effort, infant acquisition, their male partners, had extensive sibling-rearing infant rejection, and infant grooming. The care- experience as alloparents. Three females (Bas, Jin, giving behavior of breeding males was again J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142 133 included in these analyses as a control for factors we illustrate the impact of experienced alloparental other than female reproductive energetics that may assistance on carrying effort of females and males be influenced by the presence of alloparents. To separately to show how female carrying effort was compare concentrations of urinary CORT when influenced by experienced helpers. At weeks two, females did and did not have experienced allopar- three, and four postpartum, females spent less time ental assistance, a 2-way repeated measures carrying infants when experienced alloparents ANOVA (condition ! week postpartum) was con- were present relative to when experienced allopar- ducted. When significant endocrine differences ents were not present. At weeks 1e7 postpartum, were indicated, we used Pearson correlation and at week nine postpartum, males spent less time coefficients to examine the relationship between carrying infants when experienced alloparents postpartum hormone levels and maternal behav- were present relative to when experienced allopar- ior. Post hoc analyses were conducted using the ents were not present. Because the significant Tukey test (Keppel, 1991), and an a level of 0.05 interactions between sex and weeks and between was adopted for all statistical tests. All data are alloparental assistance and weeks indicated that presented as X G SE. these variables did not act alone to influence carrying effort, significant main effects will not be Results addressed. Parental motivation to be in contact with Alloparental assistance and maternal caregiving infants was most evident during the first few weeks behavior. Females and males exhibited reciprocal of infant life. Rates of infant acquisition varied decreases and increases, respectively, in carrying significantly among postpartum weeks (F(8, effort across the postpartum period. A significant 80) Z 11.19, p ! 0.001), such that rates of acqui- interaction between sex and weeks (F(8, sition at weeks 1e4 postpartum (week 1: 80) Z 5.57, p ! 0.001) indicated that female and 0.76 G 0.14 /hr; week 2: 0.74 G 0.18 /hr; week 3: male carrying effort varied among postpartum 1.13 G 0.22 /hr; week 4: 1.01 G 0.19 /hr) were all weeks, such that females were the primary carriers significantly higher than at weeks 6e9 postpartum of infants during the first week of infant life (week 6: 0.30 G 0.09 /hr; week 7: 0.05 G 0.03 /hr; (Fig. 3; p ! 0.05). By weeks three and four week 8: 0.02 G 0.03 /hr; week 9: 0.00 G 0.00 /hr; postpartum, however, females reduced their car- p ! 0.05). While both parents exhibited distinct rying effort to such a degree that they carried their changes in their motivation to be in contact with infants at significantly lower rates than fathers infants across the postpartum period, rates of (p ! 0.05). Except for the first week of infant life, females carried their infants less than males did at every time-point. The carrying effort of both 50 Females (n = 12) females and males, however, was influenced by Males (n = 12) the presence of experienced alloparents. A signif- 40 icant interaction between alloparental assistance and weeks [Fig. 4A; F(8, 80) Z 2.34, p ! 0.03] 30 indicated that the effect of alloparental assistance on parental carrying effort varied across the 20 postpartum period. When experienced alloparents were present to share in the carrying effort, both 10 females and males carried infants significantly less Infant Carrying (min/hr) at week two postpartum than when experienced 0 alloparents were not present (p ! 0.05). Although 123456789 the interaction between alloparental assistance and Weeks Postpartum weeks was significant, and the interaction between Fig. 3. Mean (GSE) parental carrying effort across the first alloparental assistance and sex was not, in Fig. 4B nine weeks of infant life. 134 J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142

A Both females and males exhibited a pattern of 50 increasing intolerance for oﬀspring as infants Without experienced alloparental assistance (n = 12) With experienced alloparental assistance (n = 12) gained their independence; the timing of this 40 change in parental responsiveness was related to the presence of experienced alloparents. A signif- 30 icant interaction between alloparental assistance and weeks (F(8, 80) Z 2.56, p ! 0.03) indicated 20 that the impact of alloparental assistance on infant rejection varied among weeks (Fig. 6A). At weeks 10

Infant Carrying (min/hr) six, seven, and nine postpartum, parents exhibited higher rates of rejection when experienced allo- 0 parents were present (week 6: 1.63 G 0.42 /hr; 123456789 G G Weeks Postpartum week 7: 1.50 0.37 /hr; week 9: 0.48 0.19 /hr) than when experienced alloparents were not B present (week 6: 0.79 G 0.39 /hr; week 7: 0.41 G Without experienced alloparental assistance (n = 6) G ! 50 With experienced alloparental assistance (n = 6) 0.12 /hr; week 9: 0.06 0.06 /hr; p 0.05). 40 Although the interaction between alloparental 30 assistance and weeks was significant, and the Females 20 interaction between alloparental assistance and 10 sex was not, in Fig. 6B we illustrate the impact of 0 experienced alloparental assistance on the rejec- 50 tion rates of females and males separately to show 40 more clearly how female intolerance of infants was 30 Males Infant Carrying (min/hr) 20 influenced by experienced helpers. At weeks five, 10 six, seven, and nine postpartum, females rejected 0 infants at higher rates when experienced allopar- 123456789 ents were present relative to when experienced Weeks Postpartum alloparents were not present. At week six post- Fig. 4. A) Mean (GSE) parental carrying effort, across the first partum, males rejected infants at higher rates nine weeks of infant life, when experienced alloparents were and were not present; B) mean (GSE) infant carrying effort for when experienced alloparents were present relative females and males across the first nine weeks of infant life, when to when experienced alloparents were not present. experienced alloparents were and were not present.

1.2 Without experienced alloparental assistance (n = 6) infant acquisition for females and males were With experienced alloparental assistance (n = 6) diﬀerentially impacted by the presence of experi- 1.0 enced alloparental assistance (Fig. 5). A signiﬁcant interaction between sex and alloparental assistance 0.8 indicated that rates of infant acquisition by 0.6 females and males were dependent on whether or not experienced alloparents were present (F(8, 0.4 Z !

80) 5.11, p 0.05). Females exhibited signiﬁ- Infant Acquisitions / hr cantly higher rates of acquisition when experienced 0.2 alloparents were present relative to breeding 0.0 attempts in which experienced alloparents were Males Females ! not present (p 0.05). Male rates of acquisition Fig. 5. Mean (GSE) rates of infant acquisition for females and did not vary as a function of the presence of males, with and without experienced alloparental assistance, experienced alloparental assistance. during the ﬁrst nine weeks of infant life. J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142 135

Parental grooming of infants was most likely to Alloparental assistance and urinary CORT excre- occur during early infant life. Rates of infant tion. Patterns of postpartum urinary CORT ex- grooming differed significantly among weeks (F(8, cretion did not differ as a function of experienced 80) Z 2.59, p ! 0.02). Rates of infant grooming at alloparental assistance (F(1, 5) Z 0.15, NS). weeks 1e5 postpartum (week 1: 0.97 G 0.21 /hr; week 2: 1.07 G 0.56 /hr; week 3: 1.44 G 0.51 /hr; week 4: 0.95 G 0.31 /hr; week 5: 1.20 G 0.39 /hr) Discussion were all significantly higher than at weeks 6e9 postpartum (week 6: 0.65 G 0.15 /hr; week 7: When female marmosets conceived in the early 0.34 G 0.18 /hr; week 8: 0.31 G 0.12 /hr; week 9: postpartum period and were faced with the 0.21 G 0.11 /hr; p ! 0.05). Rates of infant groom- forthcoming energetic demands of lactation and ing did not differ significantly as a function of infant carrying, they exhibited swift and dramatic alloparental assistance (F(1, 80) Z 4.79, NS). reductions in levels of investment in their current litters relative to breeding attempts in which conception occurred later in the postpartum period. These behavioral changes might have endocrino- A logical underpinnings. The hormonal profiles of 2.5 Without experienced alloparental assistance (n= 12) With experienced alloparental assistance (n = 12) females when they conceived during the period of

2.0 critical infant dependence were characterized by elevated postpartum E2 levels, and postpartum E2 1.5 was significantly and negatively correlated with females’ carrying effort during the period of critical 1.0 infant dependence. When experienced alloparents were present to assist in the rearing of offspring, Infant Rejections / hr 0.5 thereby providing females with the opportunity to reduce the energetic costs associated with infant 0.0 care and transport, females reduced their carrying 123456789 effort and rejected their infants more frequently Weeks Postpartum relative to breeding attempts in which there were no B other experienced caregivers, other than the breed- 4 Without experienced alloparental assistance (n = 6) With experienced alloparental assistance (n = 6) ing male. However, postpartum urinary CORT 3 excretion, when females had experienced allopar-

2 Females ental assistance, did not differ from breeding attempts in which these same females did not have 1 experienced helpers. Thus, even in a captive setting, 0 in which marmosets are unlikely to incur the types 4 or magnitude of energetic burdens faced in the wild 3 (i.e., foraging for food and traveling 0.74e1.50 km Infant Rejections / hr 2 Males per day; Tardif, 1994), individual patterns of 1 maternal investment varied from litter to litter, 0 apparently in response to the competing demands 123456789 of caring for current and future litters. Weeks Postpartum Why might female marmosets spend less time Fig. 6. A) Mean (GSE) rates of infant rejection by parents, and energy caring for infants when facing upcom- across the first nine weeks of infant life, when experienced ing energetic demands and when they have an alloparents were and were not present; B) mean (GSE) rates of infant rejection for females and males, across the first nine opportunity to reduce their investment in off- weeks of infant life, when experienced alloparents were and spring? These seemingly conflicting findings are were not present. well explained by Lee et al.’s (1991) comparative 136 J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142 model of maternal investment. Generated with access to resources of moderate quality. Thus, by life-history data from 32 primate species represent- rearing offspring more efficiently and investing less ing both catarrhine and platyrrhine taxa (but no time and energy in the care of offspring, these species from the family Callitrichidae), this model females can improve their own physical condition states that weaning age, or the time and energy and prepare for future reproductive attempts. females devote to the care of offspring, is an Finally, a pattern of late weaning was predicted inverted U-shaped function of maternal condition to be associated with moderate food or resource and resource availability. limitations, relatively slow infant growth, and the Lee et al.’s (1991) model revealed three distinct least rejecting mothering styles. Fairbanks and patterns of weaning, which appear to exist within McGuire (1995) compared the caregiving behavior primate species under different conditions and of vervet monkeys, whose reproductive condition between species in different habitats. One pattern was defined as marginal, prime, or average, and of early weaning, or reduced maternal investment found that females in average reproductive condi- in offspring, was associated with maternal inability tion were less rejecting and spent more time in to maintain offspring growth or lactation due to ventral-ventral contact with their infants than low resource availability or poor physical condi- females in prime or marginal condition. It appears, tion. Indeed, early weaning (e.g., vervet monkeys, then, that natural selection has shaped patterns of Cercopithecus aethiops: Lee, 1984, 1987; Hauser primate maternal care to be sensitive to the costs and Fairbanks, 1988), unresponsive and neglectful of reproduction and equipped females with the parenting (e.g., vervet monkeys, Hauser, 1993; ability to reduce their investment in offspring when human: Belsky et al., 1991; also see review in attempting to reproduce under the worst and best Maestripieri and Carroll, 2000), infant abuse and of conditions. abandonment (e.g., humans: Daly and Wilson, The results of our studies suggest that patterns 1984; Hrdy, 1999), and infant mortality (e.g., of marmoset maternal behavior are also sensitive barbary macaques, Macaca sylvanus: Meńard and to the costs of caring for offspring, and that female Vallet, 1993; humans: Daly and Wilson, 1984; marmosets vary their caregiving effort in response Hrdy, 1999) have all been associated with poor to these costs. In Study 1, female marmosets faced maternal condition and/or poor resource avail- with the impending demands of nursing and ability. In such cases, females may sacrifice their carrying newly conceived litters during early infant current offspring’s fitness in favor of maternal care significantly reduced their investment in their survival and the possibility of producing offspring current littersdperhaps shifting investment away in the future. A second pattern of early weaning from their current litters to ensure sufficient was associated with high resource availability and resources for upcoming litters. Although studies good maternal condition. Comparisons of pro- have indicated that callitrichid caregivers some- visioned and non-provisioned populations have times reduce the energetic burden of infant care by revealed that provisioned females exhibit shorter spending less time foraging and traveling while interbirth intervals and lactational periods, live transporting infants (e.g., saddle-back tamarins: longer, and exhibit higher infant survival rates Goldizen, 1987; cotton-top tamarins: Price, 1992c; than non-provisioned conspecifics (see reviews in see review in Tardif, 1994), and that some may be Paul and Kuester, 1988; Asquith, 1989; Hendrickx physically limited in their ability to travel while and Dukelow, 1995). Additionally, there are carrying infants (common marmosets: Schradin reports that females with access to higher quality and Anzenberger, 2001), our results are consistent (but non-provisioned) diets (e.g., vervet monkeys: with recent reports that energetically challenged Hauser and Fairbanks, 1988) and those with high callitrichid females may actually provide less care dominance rank (e.g., yellow baboons, Papio to their offspring than females that are in better hamadryas cynocephalus: Altmann and Samuels, condition and/or have access to higher quality 1992) invest less time and energy in offspring than resources. Tardif et al. (2001) reported that, among females in relatively moderate condition and/or common marmosets, smaller females engaged in J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142 137 fewer nursing bouts than larger females, and Bales interesting in light of reports that female common et al. (2002) found that females with the lowest marmosets compensate for the care normally body weights also exhibited the lowest levels of provided by their mates when males were exper- carrying effort. Our results are also consistent with imentally removed from their family groups evidence that physiological components of calli- (Arruda et al., 1986; Yamamoto et al., 1987) and trichid maternal investment vary with maternal when normal patterns of paternal care were condition. In common marmosets, for example, disrupted by housing changes (Rothe et al., there was more within- than between-female 1993). Even though the females in Study 2 variation in the number of ova females ovulated decreased their carrying effort when experienced per cycle, and individual females ovulated signif- alloparents were present, they also exhibited icantly fewer ova at lower body weights than they increased motivation to acquire infants from other did at higher body weights (Tardif and Jaquish, carriers in this condition. It seems likely that the 1997). Similarly, Bales et al. (2001) reported that increase in rates of infant acquisition observed female golden lion tamarins at lower body weights among females, but not males, when experienced gave birth to smaller litters than females at higher alloparents were present might reflect the fact that body weights. In a study of the relationship only females are obligated to obtain infants from between nursing effort and ovulatory functioning other caregivers for the purpose of nursing. In fact, in cotton-top tamarins, Ziegler et al. (1990) found there is evidence that alloparental assistance may that females nursing twin infants exhibited their benefit breeding males more than females. Among first postpartum ovulation later in the postpartum golden lion tamarins, for example, male caregiving period than females nursing singletons and those effort decreased with increasing group size, and not nursing infants. Lactational performance also male reproductive tenure, but not female repro- appears to be sensitive to maternal condition and ductive tenure, increased with group size (Bales resource availability (Tardif et al., 2001). Small et al., 2000). Additionally, Achenbach and common marmoset females rearing twins had Snowdon (2002) reported that, among cotton-top lower milk fat percentages, lower gross milk energy tamarins, male weight loss associated with infant output, and lower nursing bout frequencies than care was negatively correlated with the number of larger mothers nursing twins. The results of our alloparents present to assist males. studies, therefore, complement a growing body of The results of Study 2 were not surprising given research indicating that a broad array of callitrichid reports indicating that female carrying effort is reproductive processes, both behavioral and phys- negatively correlated with group size (common iological, are sensitive to the costs of reproduction. marmosets: Box, 1977; cotton-top tamarins: Consequently, our findings also suggest that, even Cleveland and Snowdon, 1984; Ziegler et al., in the context of their unique reproductive system, 1990; golden lion tamarins: Bales et al., 2002). female marmosets have been subjected to similar However, an investigation into caregiving behav- selection pressures as females of other primate taxa ior in two taxa of callitrichid primates (Callithrix (Lee et al., 1991) to partition their reproductive and Leontopithecus) demonstrated that Callithrix effort between current and future offspring when females living in large groups (i.e., with more energetically challenged, because the investment of alloparental assistance) spent more time carrying time, energy, or resources to the production of their infants during the first month of infant life current offspring may diminish their ability to than females living in smaller groups (Santos et al., invest in future offspring (Trivers, 1972, 1974). 1997). Further, other studies have found females Female marmosets with an opportunity to to be unaffected by the presence of alloparents reduce the costs of rearing their current lit- (e.g., black lion tamarins: Santos et al., 1997: tersdthose with experienced alloparental assis- cotton-top tamarins: Tardif et al., 1990; Geoffroy’s tancedalso reduced their investment in offspring, marmosets: Santos et al., 1997; golden-headed lion possibly in favor of future reproductive opportu- tamarins: Santos et al., 1997; golden lion tamarins: nities. We found this result to be particularly Santos et al., 1997; Bales et al., 2000; Wied’s black 138 J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142 tufted-ear marmosets: Santos et al., 1997). One nal responsiveness and behavior. In Study 1, female likely explanation for these different findings marmosets had significantly higher postpartum regarding the impact of alloparents on maternal levels of E2 when they conceived DPCID than effort may be the difficulty of disentangling the when they conceived APCID, and these differences effects of alloparental assistance from the effects of did not occur until the second postpartum week, alloparental age and experience. Several studies when females had conceived in the DPCID have indicated that young alloparents (e.g., condition. Furthermore, postpartum E2 was signif- common marmosets: Ingram, 1977; Tardif et al., icantly and negatively correlated with maternal 1986; cotton-top tamarins: Tardif et al., 1986, carrying effort when conception occurred DPCID. 1992; Price, 1991, 1992c; saddle-back tamarins: Clearly, experimental studies will be required to Epple, 1975), and those without prior experience determine whether postpartum hormones are di- with infant siblings (e.g., common marmosets: rectly responsible for litter-to-litter variation in Tardif et al., 1984; cotton-top tamarins: Tardif marmoset maternal behavior. et al., 1984; Washabaugh et al., 2002; golden lion Unfortunately, the design of our study did not tamarins: Hoage, 1978; Johnson et al., 1991; allow us to identify the source(s) of the E2 excreted saddle-back tamarins: Epple, 1975), are less in- by females when conception occurred DPCID volved in infant care or provide less competent versus APCID. It may be, however, that the earliest care to infants. In our study, alloparents must have differences (i.e., weeks two and three postpartum) in been present for the birth of at least one litter of urinary E2 excretion were indicative of implantation younger siblings, and at least one year of age, to having occurred when females conceived DPCID; have been considered experienced, presumably Heger and Neubert (1983) described a characteristic resulting in their being old enough, large enough, increase in urinary E2 excretion in common and with enough infant-rearing experience to marmosets that occurs with conceptive, but not competently assist their mothers. nonconceptive, cycles and coincides with the timing It was also the case that in Study 2 there were of implantation. Future investigations into the two singleton litters born to females in our ‘‘with sources of E2 in early pregnancy and the timing of experienced alloparents’’ condition, while only implantation in Wied’s black tufted-ear marmosets twin litters were born to females in our ‘‘without may help to shed light on this issue. To date, there experienced alloparents’’ group. Nonetheless, we are no published reports on the timing of implan- do not expect that litter size influenced the changes tation in this species. in maternal behavior that we observed between Ours is not the first study to indicate a link conditions. Price (1991, 1992a), for example, between E2 and the expression of primate maternal reported that, in cotton-top tamarins, singletons behavior. Among red bellied tamarins (S. labi- were carried more than twins and, although atus), for example, prepartum urinary E2 levels individuals are known to compete to care for were found to be significantly higher in ‘‘good’’- infants (Pryce, 1988; Price, 1991), adult males and inexperienced mothers than in ‘‘poor’’-inexperi- alloparents were unlikely to resist the attempts of enced mothers who lost their infants within the adult females to take infants from another carrier first week of infant life due to neglect (Pryce et al., for the purposes of transport or nursing (Price, 1988). In an operant setting, nulliparous common 1991). In our study, females and males spent less marmosets treated with exogenous E2 and pro- time carrying infants when experienced alloparents gesterone in concentrations designed to mimic were present relative to when experienced allopar- those of late-pregnancy exhibited greater motiva- ents were not present. These results are not tion to bar-press for infant stimuli than they did consistent with what one would expect if litter when they received a control vehicle (Pryce et al., size had influenced our results. 1993). Similarly, group-living ovariectomized The studies presented in this paper suggest that rhesus macaques treated with early- to mid- hormonal factors may play a role in the regulation pregnancy levels of E2 handled infants at higher of some litter-to-litter changes in marmoset mater- rates than untreated ovariectomized females and J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142 139 untreated intact (nonpregnant) females (Maestri- Although we were unable to identify a hormonal pieri and Zehr, 1998). There is also reason to correlate to the changes in maternal behavior that believe that prepartum E2 might interfere with the occurred in the presence of experienced helpers, the expression of competent, responsive maternal results of our study did indicate that the presence caregiving behavior and the development of socio- of experienced helpers was not reliably associated emotional attachments to offspring. Among Wied’s with an increase or decrease in HPA activity. black tufted-ear marmosets, for instance, females had higher prepartum urinary E concentrations 2 Conclusions when their infants did not survive a minimum of two weeks postpartum relative to when their The energetic demands of producing and rearing infants did survive, and females with higher urinary callitrichid infants are often cited as factors E levels spent less time carrying their infants than 2 necessitating some form of assistance for callitrichid females with lower E levels (Fite and French, 2 females (e.g., Leutenegger, 1980; Garber, et al., 2000). Additionally, Fleming et al. (1997a) re- 1984; Goldizen, 1987; Dunbar, 1988; Wright, 1990; ported that human mothers with low feelings of Price 1992c), yet the response of individual females attachment toward their infants during the early to two of the hallmarks of callitrichid reproduc- postpartum period had higher plasma E levels and 2 tiondconception during lactation, and alloparental higher plasma E :PdG ratios during early preg- 2 assistancedhave not been previously investigated. nancy than mothers with high attachment. While The results of the studies presented here suggest that the majority of these studies have specifically female marmosets are equipped with the ability to focused on the involvement of prepartum E in 2 relinquish infant care to other caregivers when the priming of females for the postpartum care of conception occurs during the early postpartum offspring, the results of Study 1 suggest an period and when experienced alloparental assis- important role for postpartum E in the mainte- 2 tance is available. Our results also provide further nance of maternal motivation following birth. support for the notion that mothers are ‘‘flexible The postpartum CORT profiles of marmoset opportunists’’ (Hrdy, 1999) when it comes to females, when they did and did not have experi- providing care to their offspring. Indeed, the enced alloparental assistance, did not differ signif- females in our studies reduced their investment in icantly. Postpartum CORT has been associated offspring under two distinct conditionsdwhen they with reduced maternal responsiveness in western had to and when they could. lowland gorillas (Bahr et al., 1998). Females with elevated postpartum urinary CORT spent less time in ventro-ventral contact with their infants and Acknowledgments spent less time carrying and supporting their infants in a ventral position. In a study of the This study was a portion of the dissertation hormonal correlates of maternal behavior in research of J.E. Fite in the Department of Japanese macaques, Bardi et al. (2003a) reported Psychology at the University of Nebraska at that females with high CORT levels were more Omaha. The research presented here was described likely to reject their infants than females with low in Animal Research Protocol No. 95-103-07, and CORT levels. Also, females with high CORT/E2 was approved by the Institutional Animal Care ratios were more rejecting and responded to their and Use Committee of the University of Nebraska distress calls more slowly, and they were less Medical Center/University of Nebraska at Omaha. responsive to infants, than females with low Financial support for this project was provided by CORT/E2 ratios. Postpartum CORT has also been grants from the National Science Foundation associated with elevated maternal responsiveness (IBN 97-23842 and 00-91030), the National In- to newborn infant odors (Fleming et al., 1997b), as stitute of Child Health and Development (HD well as increased maternal sympathy toward infant 42882), and from the University of Nebraska at cries (Stallings et al., 2001), among human females. Omaha’s Animal Care Fund. 140 J.E. Fite et al. / Journal of Human Evolution 49 (2005) 122e142

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