International Journal of Primatology, Vol. 19, No. 3, 1998

Infant-Nonmother Interactions of Free-Ranging Mantled Howlers (Alouatta palliata) in

Margaret R. Clarke,1,4 Kenneth E. Glander,2 and Evan L. Zucker3 Received November 1, 1996; revised April 1 and August 8, 1997; accepted September 12, 1997

Proximate and ultimate explanations of interactions between infants and nonmothers vary depending upon the relatedness of the interactors. We investigated interactions of infants and nonmothers from a 22-month continuous study and from the long-term monitoring of the population of La Pacifica, Guanacaste Province, Costa Rica. Relatedness is low or absent in these mantled howler groups. Juvenile females appeared to practice care skills with older infants, but as most first infants died, they failed to benefit. Infant positive interactions with adults occurred with the mother and probable father. Other adult females behaved aggressively toward the youngest infants. Mothers were retentive of infants and responded negatively to these interactions, suggesting that they perceived them as threatening. Interactions with infants appear to reflect competition in groups of unrelated adults. A review of other populations of Alouatta palliata and other of howlers indicate variability in social group size and suggest variability in intragroup relatedness. We suggest that further study will confirm that social behavior (including interactions with infants) will vary by resource availability (group size) and associated demographic patterns (male and female migration) that affect relatedness in howler social groups. KEY WORDS: Alouatta palliata; howler; infant behavior; female-female competition; female dominance; alloparental interactions.

1Department of Anthropology, Tulane University, New Orleans, Louisiana 70118. 2Duke Center, Duke University, Durham, North Carolina 27705. 3Department of Psychology, Loyola University, New Orleans, Louisiana 70118. 4To whom correspondence should be addressed, e-mail: [email protected].

451

0164-0291/98/0600-0451S15.00/0 © 1998 Plenum Publishing Corporation 452 Clarke, Glander, and Zucker

INTRODUCTION

In the wake of sociobiological analyses of behavior based on inclusive fitness and kin helping kin (Alexander, 1975; Altmann, 1980; Hrdy, 1977; Hamilton, 1964a,b; Kurland, 1977; Trivers, 1972, 1974; Eberhard, 1975; Wilson, 1975), the behavior patterns observed for Alouatta palliata at La Pacifica presented an enigma (Clarke, 1981, 1983, 1985, 1986, 1990; Clarke and Glander, 1994; Glander, 1980, 1992). Like hanuman langurs or red- tailed guenons, male immigrations were accompanied by changes in adult dominance hierarchies and infant-killing (Hrdy, 1974, 1976, 1977, 1979; Struhsaker, 1977), but the howlers of La Pacifica appeared more competi- tive and less socially bonded than the Old World species are. While many species of nonhuman typically exhibit male migration, man- tled howlers exhibit male and female emigration at the juvenile stage and subsequent immigration as adults, resulting in multimale, multifemale social groups consisting of unrelated adults and their most recent offspring (Clarke, 1990; Clarke et al, 1986, 1994; Clarke and Zucker, 1994; Clarke and Glander, 1984; Glander, 1980, 1992; Jones, 1980a). Thus, evolutionary interpretations of mantled howler behavior should consider that howler groups probably consist of nonrelated competitors, a dramatic shift from the view that social behavior is driven by kinship and inclusive fitness. Other studies of interactions of nonmothers with infants were focused on kinship (Lancaster, 1971; Taub, 1979), but in a species with low intra- group relatedness, why should individuals bother to interact with infants? From an evolutionary perspective, infant-nonmother interactions could benefit the infant, the mother, or the interactor (Hrdy, 1976). Hypotheses about behaviors that benefit the interactor include learning to mother, agonistic buffering, or improved reproductive success. Hypotheses about be- haviors that benefit the infant include improved socialization or protection, while improved foraging efficiency, with a presumed decrease in interbirth interval, would benefit the mother, as well as the inclusive fitness of the infant. The benefit to a nulliparous interactor would be to practice mothering skills, i.e., learn to mother, on an unrelated infant, even if it harmed the infant, so that the nulliparous interactor could successfully raise her own subsequent first offspring (Lancaster, 1971; Wilson, 1975). While in groups of relatives mothers might encourage related nulliparous females to prac- tice mothering, in unrelated groups a mother should resist interactions, both to protect her own infant and to reduce the reproductive success of the nonrelated interactor. If agonistic buffering and the associated tempo- rary increase in access to resources were the impetus for interactions with infants, primary interactors would be low-ranking that use an infant Infant-Nonmother Interactions 453 to behave uncharacteristically, i.e., feed out of rank order, sleep in a pre- ferred site, or be near normally agonistic group members (Deag, 1980; Deag and Crook, 1971). Interactions improving adult reproductive success would include directing help toward relatives and directing harm toward nonrelatives (Hamilton, 1964a,b). While help directed toward relatives should increase inclusive fitness, it also increases competition for resources among animals living in the same social group. Harming and eliminating immature nonrelatives reduce both social and ecological competition, elimi- nate the nonrelated immature's reproductive potential, and reduce the lifetime reproductive potential of the nonrelated mother (Hrdy, 1976; Clarke, 1983; Clarke et al, 1994; Silk, 1980; Wasser, 1983; Wasser and Barash, 1981; Wilson, 1975). This harm to nonrelatives would be predicted in groups of unrelated adults to improve individual adult reproductive suc- cess. Benefits to infants would include interactions that improve socializa- tion, i.e., learning how to be adult (Altmann, 1980; Burton, 1972; Neville, 1972), and would be expected when older siblings or relatives are interac- tors, since helping a relative reproduce sooner would be beneficial to the related interactor, as well as to the developing individual. It would not be expected in a group of unrelated individuals since helping a nonrelative improve reproductive success should be selected against. If interactions with nonmothers improve an infant's chance of being rescued or adopted by that interactor (Busse and Hamilton, 1981; Rhine et al., 1980; Taub, 1979, 1980), it would be beneficial to the infant but could be costly to the nonmother. While costly care might be expected from an older, postreproductive re- lated interactor, such costly care would not be expected in groups of nonrelated animals. If infant interactions with nonmothers allowed the mothers to improve foraging efficiency (Hrdy, 1976; Smith, 1977), mothers should encourage in- fants to interact with nonmothers before feeding bouts regardless of relatedness. This increased efficiency should hasten weaning and increase reproductive success by decreasing interbirth intervals. In order to determine whether these hypotheses are supported, we analyzed data from Clarke's 22-month of study (1978-1980) of infant-non- mother interactions and our long-term demographic records on the howlers of La Pacifica. To assess whether the behaviors of Alouatta palliata are unusual, we compared our results to studies of A. seniculus, A. caraya, A. pigra, and A. fusca, specifically those parameters concerned with population dynamics, emigration patterns, infant-killing, and interactions of adult fe- males with infants. We did not include Alouatta belzebul because reports on this species lack appropriate comparative data (Almeida et al, 1995; Coimbra-Filho et al, 1995). 454 Clarke, Glander, and Zucker

METHOD

Study Site

The study site is Hacienda La Pacifica, a privately owned cattle ranch in Guanacaste Province, Costa Rica. It falls within the deciduous dry topical forest zone (Holdridge, 1967). Clarke and Zucker (1994) described the site and history of the La Pacifica population of Alouatta palliata.

Study Subjects

During Clarke's study, the main study group ranged in size between 15 and 23 individuals, with 2 or 3 adult males, 8-11 adult females, and 4-9 immatures.

Group History

As the relatedness of individuals is crucial to determine which hypothe- ses and explanations are most appropriate, we describe the group changes over time. At the beginning of the study (1978), 4 of 8 adult females and 2 of 3 adult males were known to have joined this group since 1972, when the animals were originally captured and marked (Glander, 1975). During the study, 15 infants were born, 7 infants died, 8 juveniles emigrated, and 1 adult male and 3 adult females joined the group. Between the end of 1980, when Clarke's study ended, and 1997, 21 adult females and 3 adult males have joined. Over this 25-year period (1972–1997), a total of 34 adults immigrated into the group, 93 infants were born to females in the group, and only 2 females and 2 males failed to emigrate and remained with the group as adults. Both natal females had mothers that died of old age after the daughters had become adults, so they had no relatives in the group. Both natal males met untimely deaths, and their genetic repre- sentation is minimal. Given that 36 of 38 adults were known to be immigrants or without relatives as adults (the other two died as young adults), it is reasonable to assume that the 4 adult females and 1 adult male in the study group in 1972 had previously immigrated into it. In addition, the combination of an interbirth interval of 22.5 mo fol- lowing surviving infants (Glander, 1980), or 19.9 mo for all pregnancies (Fedigan and Rose, 1995), and the juvenile emigration pattern already de- scribed means that there is little or no overlap between siblings in the natal group (Clarke and Glander, 1984), though a few female older siblings de- layed emigration until they were 3 years old. During the 22-month study, Infant-Nonmother Interactions 455 one focal subject had a juvenile female half-sibling present for 7 mo, and one focal subject had an adult female half-sibling present for 8 mo until the mother died of old age (bones and collar found) and the focal subject disappeared. The documented 25-yr demographic history of this group strongly suggests that the adults were unrelated or, alternatively, were equally related to all other adults in the population.

Interaction Data

Clarke recorded data on interactions of 12 infants via focal (703-hr) and ad libitum (753-hr) sampling (Altmann, 1974) from November 1978 through September 1980. In this context nonmothers are all group members other than the mother. An interaction began when a nonmother was <1 m of the focal infant. Interactions include care/affiliation: bridge, cuddle, carry; interest: watch, sit close, stare intently; and harm/aggression: chase, bat, bite, hit. Clarke (1990) also recorded the duration of interaction and response to the interaction by the infant, mother, and nonmother. Focal subjects >1 year old are juveniles. Clarke adjusted focal interaction data for the number of months a particular infant was observed, the number of months potential interactors were in the group, and the number of indi- viduals that were in each age-sex class at the time of the interaction.

Demographic Data

Clarke et al. (1986) and Clarke and Zucker (1994) collected demo- graphic information of the La Pacifica howlers—group size, group composition, and mortality—during the population surveys in July and Au- gust of 1984 and 1991. Additional information is available from capture and mark sessions conducted in conjunction with Earthwatch Expeditions in July and August of 1985, 1986, 1987, and 1989 (Glander and Clarke). Information on adult dominance hierarchies, reproductive states, and mi- gration patterns are from ad libitum observations during the 22-month study and from yearly monitoring and focal observations (2674 hr) on 6 different social groups in June and July or August of 1984-1996 by Clarke and Zucker. Subjects have been captured at semiregular intervals (1-2 times a year) and are individually identifiable by colored collars, tags, or leg chains (Glander et al., 1991; Scott et al., 1976). 456 Clarke, Glander, and Zucker

RESULTS

All adult and juvenile females interacted with focal subjects, though the pattern of interaction differed by age of the focal subject (Fig. 1). Adult females, regardless of their parity, were the primary nonmother interactors with infants <4 weeks old and both mothers and infants reacted negatively to these interactions at this early age (Clarke, 1990) (Fig. 2).

Learning to Mother

Juvenile females were primary nonmother interactors with focal infants >4 weeks old. Juvenile females repeatedly attempted to get infants to transfer by utilizing the stereotyped present-neck posture (Glander, 1975), but mothers were watchful. Mothers retrieved protesting infants immedi- ately, and frequently pushed juveniles away from them. Juvenile females with a history of interacting and a patient approach were tolerated (Clarke, 1990). While these interactions appear to be learning to mother in a proxi- mate sense, most infants of primiparous females died before 1 year of age (Clarke et al, 1994; Clarke and Glander, 1984; Glander, 1980, 1992), in- dicating they had not adequately learned to mother in the ultimate sense. An alternative explanation is that they have learned to mother but that additional factors are responsible for the failure of the first infants to sur- vive to 1 year of age. Data for females captured as nulliparous females with later documented infant outcome from 3 groups are in Table I. In the two larger groups, only 3 of 16 first-born infants survived, while in the smaller group (formed in 1980 and having only 1 adult male and 1-3 adult females at any time), almost all firstborn infants survived. Thus a lack of adult interactors is associated with the survival of firstborn infants, regard- less of mothering skills.

Agonistic Buffering—Social Status

No instance of behavior resembling agonistic buffering—a low-ranking howler carrying an infant as a buffer against high-ranking howlers in order to improve access to resources—has been observed by us at La Pacifica. If it does occur, because of low frequency it would have little or no effect on social status or reproductive success. Infant-Nonmother Interactions 457

Fig. 1. Adjusted frequency of all nonmother interactions with infant males and females by adult males, adult females, and juvenile females. Each point represents an average for each 13 weeks of age. Interactions adjusted for number of interactors available and number of infants available at the time of interaction. 458 Clarke, Glander, and Zucker

Fig. 2. Percentage of total interactions (care plus interest plus harm) to which mother responds negatively, and whether that response was directed toward the nonmother or toward the infant. Infant age in 2-week intervals.

Table I. Survival of Firstborn Infants Nulliparous Group Size Modal No. females Infant Infant Percentage number range females captured survives dies survival

(Established before 1970) 1972-1994

2 14-22 8 4 1 3 25

7 14-26 10 12 2 10 16

(New group in 1980) 1980-1994

19 2-9 2 5 4 1 80 Infant-Nonmother Interactions 459

Adult Reproductive Success

For adult females, interactions with others' infants appeared to be a competitive strategy, which presumably reduced survivorship of other fe- males' infants. Although infant deaths could not be linked directly to adult female aggression, mothers resisted interactions, and loss of first infant was the rule (Table I). Harm was directed toward young, vulnerable infants (0-3 mo) and, again, when they were at the age to emigrate (13-21 mo) (Fig. 3 and the Appendix). There was a positive correlation between amount of aggression received by the infant and the total negative re- sponses to all interactions by mothers (rs = 0.76, P = 0.04; Table II). Maternal resistance to all interactions increased as aggression toward her infant increased. Adult female interest in very young infants was both tense and intense, and most mothers left the group for several days after their infants were born, which effectively allowed them to avoid this interaction.

Fig. 3. Adjusted frequency of aggressive or harmful interactions directed by nonmothers toward infants. All aggression includes all potentially harmful interactions—chase, push, shove, hit, bat—while most injurious include only contact aggression: hit, bat, kidnap. Data are averaged for 3-mo blocks and adjusted for number of infant and interactors available for each interaction. 460 Clarke, Glander, and Zucker

Table II. Infant Directed Aggression/Harm and Mothers' Responses to All Interactions Infant Mother Nonmother-to- Rank of Rank of Name infant aggression aggression Negative negative (sex) indexa index Name responseb response

Bu (m) 3.33 1 Bonniec 38% 2 Sk (f) 3.20 2 Yellow 60% 1 Ru (m) 2.00 3 G/red 14% 6 Gr (f) 1.54 4 Green 17% 5 Da (f) 1.25 5 Dog 24% 3 Pi (0 1.11 6 Purple 19% 4 Be (f) 0.71 7 Blue 11% 7 Al (m) 0.00 8 Apricot 6% 8 aSum of adjusted frequency of aggressive/harmful interactions/animals available per 3-mo block. bPercentage of total nonmother interactions that mother responded to negatively. cAlso referred to as "Silver''' in some publications.

Harmful interactions and dominance were related, both in frequency and in direction. Harm was directed down the female dominance hierarchy (Table III), and there is a positive correlation between rank of nonmother and frequency of harmful interactions (rs = 0.72, P < 0.05). Chances for directing harm at higher- or lower-ranking females' infants were about equal as all females had infants, and high- and low-ranking females had

Table III. Aggression/Harm Directed by Adult Females by Rank Towards Infants" Adult female nonmother interactors (by rank) Mother Infant rank name Aprl Bon2 Pur3 Grn4 Yel5 Blu6 Dog7 G/R8

Aprl Al XX Bon2 Bu 2 XX Pur3 Pe XX Pur3 Pi XX 1 Grn4 Gr 1 XX Grn4 Gl XX Yel5 Yo 5 1 2 3 XX 1 1 Yel5 Sk 4 XX Blu6 Be 2 1 1 XX Blu6 Bi XX Dog7 Da 2 1 1 XX G/R8 Ru 1 XX aData for 3 adult female interactors that were changing ranks are not included in the table, but were included in the correlation coefficient. This involved 11 aggressive interactions toward infants of mothers that rank 3, 4, and 5. Infant-Nonmother Interactions 461

comparable infant survival (453 infant months of low-ranking females, 459 infant months for high-ranking females). Low-ranking mothers could not avoid these approaches from high-ranking females. The direction of harm and maternal resistance supports the hypothesis that interactions of adult females were competitive. Infant-killing and associated infant disappearance when an immigrant male joins and takes over a new group have been well documented in this population (Clarke, 1983; Clarke et al., 1994). This not only eliminated un- related infants as competitors, but since females resumed cycling after losing their infants, the new male could begin to increase his own repro- ductive success more rapidly. Like females, adult males also directed harmful aggression toward nonrelated juveniles of >18 mo (Fig. 3 and the Appendix) (Clarke, 1986; Clarke and Glander, 1984). This harmful aggres- sion preceded emigration and eliminated nonrelated competitors from the social group (Clarke, 1985; Clarke and Zucker, 1989).

Socialization

There were differences in interactions with male and female infants that varied both qualitatively and quantitatively at an early age. Male in- fants <3 mo old received care from adult males and did not interact with males again after that, but all of these focal male infants died by 8.5 mo (Clarke, 1990). Female infants responded positively to most interactions and received fewer harmful interactions from juvenile females than did male infants (Clarke, 1990). While interactions may have helped infants to learn species-appropriate behaviors that they would need as adults, there is no evidence that it increased sociability or reduced weaning stress (Clarke and Glander, 1984; Zucker and Clarke, 1992). None of the male focal subjects survived, and one interaction bout contributed to the death of a male as he fell from the trees into the river and drowned. Overall activity patterns of male and female juvenile howlers are similar (Clarke et al., 1997).

Rescue, Protection, and Adoption

Mothers were the primary caretakers of their own infants, and were the only individuals that rescued them from falls or kidnappings (Clarke, 1985), situations that could be considered life threatening. Minimal care, such as bridging or carrying, occurred (Clarke, 1990), though not along lines of relatedness for females (Table IV). One juvenile occasionally car- ried or bridged for her 6.5-mo injured half-sibling. This care was the only 462 Clarke, Glander, and Zucker

Table IV. Interactions with Half-Siblings and Nonrelativesa Interactions with Tala Interactions with Bonnie (juvenile female) (adult female) % Tala's that were % Bonnie's that were Focal % name totalb Interest Care Harm Play % totalc Interest Care Harm Play

Female Yo 12.6 33 3 3 46 2.3 43 43 14 0 Bed 193 48 20 0 10 4.1 52 24 0 14 Dae 4.4 40 10 0 50 7.0 78 6 0 3 Gr 2.3 63 0 13 13 2.9 100 0 0 0 Pi 0.7 100 0 0 0 2.4 100 0 0 0 Sk Born after Tala emigrated 4.8 100 0 0 0

Males Pe 0.0 0 0 0 0 22.7 100 0 0 0 Al 1.6 100 0 0 0 7.9 100 0 0 0 Ru 2.5 100 0 0 0 7.5 56 44 0 0 Cr 15.8 100 0 0 0 42.1 89 11 0 0 Bu Born after Tala emigrated Born to Bonnie (offspring) aData in bold refer to interactions between half-siblings. Not adjusted for time in group together. bPercentage of total nonmother interactions of focal infant that were with Tala. cPercentage of total nonmother interactions of focal infant that were with Bonnie. dHalf-sibling to Tala. eHalf-sibling to Bonnie.

remarkable interaction with a relative, and it was short-term: only during group movements over a 2-week period. The adult female interacted less with her younger half-sibling than she did with other infants (Table IV). also occurred. Infants and probable fathers (Clarke, 1981) are listed in Table V, where adult males involved in interest, care, or harm with each focal are identified. Probable fathers were in- terested in and cared for infants and never directed aggression or harm toward them—behaviors predicted by individual fitness. Adult female care of others' infants was unusual, and the three cases of temporary adoption involved adult females with no previous history of interacting with the in- fant. The successful adoption appeared to be the result of the individual characteristics of the adult female adopter—supermother—and infant adoptee: superclinger (Clarke and Glander, 1981; Clarke et al, 1994). There is no evidence that an established interaction pattern with an infant predicted whether it would be rescued, protected, or adopted. Infant-Nonmother Interactions 463

Table V. Probable Fathers and Interest/Care/Harm by Adult Males Probable Affiliation Aggression Infant (sex) father or care"a Interestb or harmc

Pe (m) Baker None None None Al (m) Macho All Macho None Ru (m) Macho Macho Macho None Cr (m) Nongroup male None Scar None Bu (m) Macho Macho Macho/Scar Houdini Yo (f) Baker None Baker/Scar Macho Be (f) Baker Baker Baker Macho Da (f) Baker None Baker/Scar None Gr (f) Macho None Macho Houdini Pi (f) Macho None Macho None Sk (f) Macho None Macho/Scar None Bi (f) Houdini None Houdini None

a Carry, cuddle. bWatch, sit near. cBat, bite, hit, chase.

Foraging Efficiency

Nonmothers carried and held 7- to 14-week-old infants while the moth- ers fed. After 15 weeks of age, infants were independent while their mothers fed (Clarke, 1990). Nonmothers carried infants when maternal lac- tation is energetically costly (Dunbar, 1988), but the results are inconclusive since a mother was more likely to be sitting or sleeping than feeding while her 7- to 14-week-old infant was interacting with a nonmother. During these interactions, mothers spent 64.5% of the time sitting or sleeping, 14.5% of the time traveling, and only 21% of the time feeding.

DISCUSSION

The Selfish Howler

The combination of intense competition for group membership and the pattern of juvenile male and female emigration and adult male and female immigration forms the basis for the mantled howler social system (Clarke, 1985; Glander, 1980; Jones, 1980a, 1985). That this system is more competi- tive than cooperative is suggested by the rigid dominance hierarchy for ac- cess to resources among both males and females (Clarke, 1985; Glander, 1980, 1992; Jones, 1980a,b, 1995) and little or no apparent appeasement 464 Clarke, Glander, and Zucker behavior. Grooming is rare (Clarke, 1982; Glander, 1975), and agonistic buffering is nonexistent. The only cooperation is between kin, but these in- teractions are infrequent since most individuals are unrelated. The social dynamics, including interactions with infants, would be expected to be dif- ferent from that in a group of closely related animals, in which help extended to another monkey has a high probability of increasing the inclusive fitness of the helper. The key variable precluding groups of relatives in the La Pacifica howler population appears to be the high turnover in group membership due to male and female juvenile emigration. While an occasional natal monkey remains in the group after it has established dominance over all other group members (4 of 93 during 25 years), emigration is the rule (Clarke and Glander, 1984; Glander, 1980, 1992). Since juvenile emigration coincides temporally, though not causally, with the birth of a younger sib- ling, a mother cannot protect her juvenile from emigration-associated aggression from nonrelated adults. Since her offspring has been forced out of the group, it is in her reproductive interest to ensure that other nonre- lated females' offspring are also forced to emigrate as juveniles. Thus, the advantage of sharing resources with relatives is eliminated. Whereas Glander (1980) suggested that this system might result in a larger kin network in which relatives helped other relatives join new groups, there has been no evidence for cooperation or even reduced dominance interactions when an immigrant attempts to join a new group. Because of the documented emigration pattern, most juveniles do not know their sib- lings or they are exposed to them very briefly. It should be emphasized that an immigrating animal must establish dominance over all group mem- bers to remain in the group. While it may seem to be an advantage to join a new group with a related ally, none of us has observed multiple animals attempting to join a group. In terms of inclusive fitness, it would be dis- advantageous to migrate into a group with relatives, since an immigrant behaving in a manner to reduce fitness of resident animals would reduce its own inclusive fitness (Clarke et al., 1994). Accordingly, the pattern of male and female migration prevents relatives from competing with each other within a group, while allowing them to compete against nonrelatives in a new nonnatal group.

Comparison with Other Species

Field research over the past 10 years indicates more social variability within each species of Alouatta than previously described, precluding a spe- cies-typical characterization of howlers. Among mantled howlers, interac- Infant-Nonmother Interactions 465

tions with immatures, i.e., care and interest from a few relatives, competition from all others, are part of a social pattern typical of a group of nonrelated individuals in which male and female migration, male takeovers associated with infant disappearance, and female-female competition all contribute to and reinforce this pattern. Degree of relatedness within howler groups should be affected directly by the social turnover in groups. Since our long- term studies at La Pacifica indicate more group membership change under less stable environmental conditions (Clarke and Zucker, 1994), within- group relatedness could be affected by habitat quality: less stable habitat, increased migration, decreased relatedness. While interaction patterns of in- fants with nonmothers has not been the focus of long-term study in most howler species, we can examine variability in group size, quality of habitat, and migration patterns of other howler species to predict the potential for high versus low relatedness and to evaluate social interactions, including in- fants and nonmothers, in light of probable relatedness (Table VI). Group size, which was once thought to be species-typical, is variable for red and mantled howlers, in response to both immediate environmental challenges and long-term demographic cycles. Crockett and Rudran (1987a,b) described changes in a population of red howlers, and we re- ported similar processes in mantled howlers (Clarke et al., 1986, 1994; Clarke and Zucker, 1994; Glander, 1992). Reports from other populations of red and mantled howlers confirm this variability (Agormoorthy and Hsu, 1995; Crockett and Eisenberg, 1987; Gaulin and Gaulin, 1982; Izawa, 1988, 1989a, 1994; Lippold, 1988, 1989; Stoner, 1994, 1996). Recent field studies on several populations of Alouatta caraya indicate variability in group size associated with resource distribution (Bicca-Marques and Calegaro- Marques, 1994a,b; Kowaleski et al, 1995; Rumiz, 1990; Zunino and Rumiz, 1986). While group size is less variable in Alouatta pigra (Horwich and

Table VI. Comparison of Alouatta spp.a Adult female Range of Male Infant Female interest in Mother Species group size migration killing migration young infant resistance

A. palliata 3-48 Yes Yes Yes Yes Yes

A. seniculus 2-16 Yes Yes Yes Yes Yes

A. caraya 3-19 Yes Yes Yes Yes Yes

A. fusca 3-10 Yes Yes Yes Yes Unknown

A. pigra 2-10 Unknown Unknown Probable Yes Unknown aReferences for each category in text. 466 Clarke, Glander, and Zucker

Johnson, 1986) and A. fusca (Mendes, 1989). The range of group sizes in these two species is still between 3 and 10. For Alouatta, group size is as variable within species as between species. Both male and female migration have been clearly documented in mantled, red, black, and brown howlers with emigrating animals joining established groups or forming new social groups [Alouatta palliata (Clarke and Glander, 1984; Clarke et al, 1986; Clarke and Zucker, 1994; Glander, 1980, 1992), A. seniculus (Agormoorthy and Rudran, 1993; Crockett, 1984, 1985; Crockett and Pope, 1988, 1993; Gaulin and Gaulin, 1982; Izawa and Lozano, 1992; Sekulic, 1982), A. caraya (Calegaro-Marques and Bicca- Marques, 1996; Kowaleski et al., 1995; Rumiz, 1990; Zunino et al., 1985), A. fusca (Mendes, 1989)]. While female immigration is not specifically documented in Guatemalan black howlers, groups that had 1 female in 1981 (Bolin, 1981) had 2 or 3 females in 1983 (Horwich and Gebhard, 1986), suggesting that females of this species also change groups. There is documentation of infant-killing in association with male take- overs in mantled, red, black, and brown howlers [Alouatta palliata (Clarke, 1983; Clarke et al., 1994), A. seniculus (Agormoorthy and Rudran, 1995; Crockett and Sekulic, 1984; Izawa and Lozano, 1991; Rudran, 1994; Sekulic, 1983a), A. caraya (Calegaro-Marques and Bicca-Marques, 1996, Kowaleski et al., 1995; Rumiz, 1990; Zunino et al., 1985), A. fusca (Galetti et al., 1994)], and most are followed by female proceptive behavior toward the infanticidal male. Intense interest in infants by adult females associated with maternal resistance occurs in free-ranging mantled, red, black, and Guatemalan black howlers. Intense interest in the newborn animal is expressed by adult fe- males (Calegaro-Marques and Bicca-Marques, 1993; Clarke, 1990; Izawa, 1989b; Mendes, 1989; Sekulic, 1983b; Serio-Silva and Rodriguez-Luna, 1994; Shoemaker, 1982), and mothers are retentive (protective) of their young offspring and avoid interactions when possible (Clarke, 1990; Cale- garo-Marques and Bicca-Marques, 1993; Horwich and Gebhart, 1986; Sekulic, 1982, 1983a; Serio-Silva and Rodriguez-Luna, 1994; Shoemaker, 1982). Mack (1979) reported that others pull, touch, and remove the infant from the mother in red howlers, and Shoemaker (1982) reported that both adult male and adult female black howlers approached and touched the infant by the second day of life. These interactions are in marked contrast to the pattern of older immature siblings carrying older infants also re- ported for these species [Alouatta caraya (Calegaro-Marques and Bicca-Marques, 1993), A. palliata (Clarke, 1982), A. seniculus (Crockett and Pope, 1993)]. Horwich and Gebhardt (1986) and Bolin (1981) reported no early interest and protective behavior in Guatemalan howlers, but their study infants were born before the start of their studies (Horwich and Infant-Nonmother Interactions 467

Gebhart, 1986; Bolin, 1981). The intra- and interspecific variability evident in howling monkeys suggests that the quality and quantity of interactions with infants by nonmothers would be expected to vary with relatedness: when group members were unrelated, interactions would be of a competi- tive nature, whereas in groups in which some females remain in the group rather than emigrating, there would be more cooperation and help directed toward related infants. The long-term data from Alouatta palliata indicate that where there are relatives, there is help, and it would be reasonable to expect increased care with increased relatedness. Thus, social behavior of howlers, including interactions with infants, do not appear to be species-typical, but are expected to vary with intragroup relatedness, which in turn varies along a continuum of environmental fac- tors that affect group size and migration patterns. Fifteen years ago La Pacifica howlers were thought to represent an extreme in nonrelated group- ings, but now this pattern appears to be one of several howler adaptations to specific or changing environmental conditions or both. Due to defores- tation, future studies of howler species will focus on disturbed and changing habitats. This natural experiment should allow us to measure and to define the specific relationship among habitat quality, demographic patterns, in- cluding migration, and associated social behaviors of howlers.

APPENDIX

Table AI. Raw Scores for Aggressive Interactions with Immatures by Age-Sex Classa Focal age Number of Immature (weeks) focal subjects Adult males Adult females females 0-13 10 0 (0)b 14 (10) 5 (1) 14-26 9 0(0) 3 (0) 0 (0) 27-39 6 0(0) 4 (1) 3 (0) 40-52 5 0(0) 2 (2) 0 (0) 53-65 4 2(1) 4 (2) 1 (0) 66-78 3 0(0) 2 (1) 2 (2) 79-91 3 4(1) 10 (4) 3 (0) Total 6(2) 38 (20) 15 (3) aThese are raw scores only, and have not been adjusted for the number of focal infants available, the length of the observation period, or the number of interactors available in each age-sex class. bThe first number indicates the unadjusted frequency of all potentially harmful interactions, and the number in parentheses indicates the unadjusted frequency of potentially injurious interactions: bite, hit, kidnap. 468 Clarke, Glander, and Zucker

ACKNOWLEDGMENTS

Our research was supported by Doctoral Dissertation Improvement Grant BNS78-19308; an Explorer's Club Grant; University of California Graduate school funds; funds from the Anthropology Department, Univer- sity of California, Davis; National Geographic Grant 4546-91; School for Field Studies, Earthwatch, Loyola University (New Orleans); Duke Uni- versity; and the resources of the Tulane Regional Primate Research Center (NIH RR00164). We thank the Hagnauer and the Centro Ecologico for permission to work on their property and their continued support and the many individuals who helped us while in Costa Rica. Clarke thanks Myra L. Hidalgo, Darryl J. Mayeaux, Katherine Phillippi Falkenstein, Jen- nifer Snyder O'Neil, and Laurel S. Anderson for invaluable help with the literature search, William Balee for translation from Portuguese into Eng- lish, and Peter S. Rodman and William A. Mason for comments on an early version of the manuscript. A different version of this paper was pre- sented at the 12th meeting of the International Primatological Society in in 1988 as part of the symposium Howlers: Past and Present.

REFERENCES

Agormoorthy, G., and Hsu, M. J. (1995). Population status and conservation of red howling monkeys and white-fronted capuchin monkeys in Trinidad. Folia Primatol. 64: 158-162. Agormoorthy, G., and Rudran, R. (1993). Male dispersal among free-ranging red howler monkeys (Aloutta seniculus) in Venezuela. Folia Primatol. 61: 92-96. Agoramoorthy, G., and Rudran, R. (1995). Infanticide by adult and subadult males in free-ranging red howler monkeys. Alouatta seniculus, in Venezuela. Ecology 99: 75-88. Alexander, R. D. (1975). Search for a general theory of behavior. Behav. Sci. 20: 77-100. Almeida, R. T., Pimental, D. S., and Silve, E. M. S. (1995). The red-handed howling monkey in the state of Perranbuco, northeast Brazil. Neotrop. Prim. 3: 174-176. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour 49: 227-265. Altmann, J. (1980). Baboon Mothers and Infants, Harvard University Press, Cambridge, MA. Bicca-Marques, J. C, and Calegaro-Marques, C. (1994a). Padrao de Utilizacao de uma ilha de mata por Alouatta caraya. (primates: ) Rev. Brasil. Biol. 54(1): 161-171. Bicca-Marques, J. C., and Calegaro-Marques, C. (1994b). Feeding behavior of the monkey (Alouatta caraya) in a seminatural forest. Acta Biol. Leopold. 16(2): 69-84. Bolin, I. (1981). Male parental behavior in black howler monkeys (Alouatta palliata pigra) in Belize and . Primates 22: 349-360. Burton, F. D. (1972). The integration of biology and behavior in the socialization of Macaca sylvana of Gibraltar. In Poirier, F. E. (ed.), Primate Socialization, Random House, New York, pp. 29-62. Busse, C., and Hamilton, W. J., III (1981). Infant carrying by male chacma baboons. Science 212: 1281-1282. Calegaro-Marques, C., and Bicca-Marques, J. C. (1993). Allomaternal care in the black (Alouatta caraya). Folia Primatol. 61: 104-109. Infant-Nonmother Interactions 469

Calegaro-Marques, C., and Bicca-Marques, J. C. (1996). Emigration in a black howling monkey group. Int. J. Primatol. 17(2): 229-238. Clarke, M. R. (1981). Aspects of male behavior in the mantled howler (Alouatta palliata Gray) in Costa Rica. Am. J. Phys. Anthropol. 54: 209. Clarke, M. R. (1982). Socialization, Infant Mortality, and Infant Nonmother Interactions in Howling Monkeys (Alouatta palliata) in Costa Rica, Ph.D. dissertation, University of California, Davis. Clarke, M. R. (1983). Infant-killing and infant disappearance following male takeover in a group of howling monkeys (Alouatta palliata) in Costa Rica. Am. J. Primatol. 1: 469-472. Clarke, M. R. (1985). Behavior of adult females towards group infants in free-ranging howlers. Am. J. Primatol. 8: 336. Clarke, M. R. (1986). Interactions of adult male howling monkeys (Alouatta palliata) with immatures in a free-ranging group. Am. J. Phys. Anthropol. 69: 188. Clarke, M. R. (1990). Behavioral development and socialization of infants in a free-ranging group of howling monkeys. Folia Primatol. 54: 1-15. Clarke, M. R., and Glander, K. E. (1981). Adoption of infant howling monkeys. Am. J. Primatol. 1: 469-472. Clarke, M. R., and Glander, K. E. (1984). Female reproductive success in a group of free-ranging howling monkeys (Alouatta palliata) in Costa Rica. In Small, M. (ed.), Female Primates: Studies by Women Primatologists, Alan R. Liss, New York, pp. 111-126. Clarke, M. R., and Zucker, E. L. (1989). Social correlates of timing of sexual maturity in free-ranging howling monkeys (Alouatta palliata). Am. J. Primatol. 18: 140. Clarke, M. R., and Zucker, E. L. (1994). Population changes in mantled howling monkeys at La Pacifica: A seven-year follow-up. Int. J. Primatol. 15: 61-73. Clarke, M. R., Zucker, E. L, and Scott, N. J., Jr. (1986). Population trends of the mantled howler groups at La Pacifica, Guanacaste, Costa Rica. Am. J. Primatol. 11: 79-88. Clarke, M. R., Zucker, E. L., and Glander, K. E. (1994). Group takeover by a natal male howling monkey (Alouatta palliata) and associated disappearance and injuries of immatures. Primates 35: 435-442. Clarke, M. R., Zucker, E. L., and Phillippi-Falkenstein, K. (1997). Activity and proximity patterns of free-ranging male and female juvenile howling monkeys (Alouatta palliata). Am. J. Phys. Anthropol. Suppl. 24: 93. Coimbra-Filho, A. F., de Gusman Camara, I., and Rylands, A. B. (1995). On the geographic distribution of the red-handed howling monkey Alouatta belzebul in northeast Brazil. Neotrop. Prim. 3: 176-179. Crockett, C. M. (1984). Family feuds. Nat. His. 93: 54-63. Crockett, C. M. (1985). Population studies of red howler monkeys (Alouatta seniculus). Nat. Geogr. Res. 1: 264-273. Crockett, C. M., and Eisenberg, J. F. (1987). Howlers: Variation in group size and demography. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. R., and Struhsaker, T. T. (eds.), Primate Societies, University of Chicago Press, Chicago, pp. 54-68. Crockett, C. M., and Pope, T. (1988). Inferring patterns of aggression from red howler monkey injuries. Am. J. Primatol. 15: 289-308. Crockett, C. M., and Pope, T. (1993). Consequences of sex difference in dispersal for juvenile red howler monkeys. In Pereira, M., and Fairbanks, L. (eds.), Juvenile Primates: Life History Development and Behavior, Oxford University Press, New York, pp. 104-118. Crockett, C. M., and Rudran, R. (1987a). Red howler monkey birth data. I. Seasonal variation. Am. J. Primatol. 13: 347-368. Crockett, C. M., and Rudran, R. (1987b). Red howler monkey birth data. II. Interannual, habitat, and sex comparisons. Am. J. Primatol. 13: 369-384. Crockett, C. M., and Sekulic, R. (1984). Infanticide in red howler monkeys (Alouatta seniculus). In Hausfater, G., and Hrdy, S. B. (eds.), Infanticide: Comparative and Evolutionary Perspective, Aldine, Chicago, pp. 173-191. Deag, J. M. (1980). Interactions between males and unweaned Barbary macaques: Testing the agonistic buffering hypothesis. Behaviour 75: 54-81. 470 Clarke, Glander, and Zucker

Deag, J. M., and Crook, J. H. (1971). Social behavior and "agonistic buffering" in the wild Barbary macaques, Macaca sylvana. Folia Primatol. 15: 183-200. Dunbar, R. I. M. (1988). Primate Social Systems, Cornell University Press, Ithaca, NY. Eberhard, M. J. W. (1985). The evolution of social behaviors by kin selection. Qrtly Rev. Biol. 50: 1-34. Fedigan, L. L., and Rose, L. M. (1995). Interbirth interval variation in three sympatric species of neotropical monkey. Am. J. Primatol. 37: 9-24. Galetti, M., Pedroni, F., and Paschal, M. (1994). Infanticide in the brown howling monkey Alouatta fusca. Neotrop. Prim. 2(4): 6-7. Gaulin, S. J. C., and Gaulin, C. K. (1982). Behavioral ecology of Alouatta seniculus in the Andean cloud forest. Int. J. Primatol. 3: 1-32. Glander, K. E. (1975). Habitat and Resource Utilization: An Ecological View of Social Organization in Mantled Howling Monkeys, Ph.D. dissertation, University of Chicago, Chicago. Glander, K. E. (1980). Reproduction and population growth in free-ranging mantled howling monkeys. Am. J. Phys. Anthropol. 53: 25-34. Glander, K. E. (1992). Dispersal patterns in Costa Rican mantled howling monkeys. Int. J. Primatol. 13: 415-436. Glander, K. E., Fedigan, L. M., Fedigan, L., and Chapman, C. (1991). Field methods for capture and measurement of three monkeys species in Costa Rica. Folia Primatol. 57: 70-82. Hamilton, W. D. (1964a). The genetical evolution of social behavior I. J. Theor. Biol. 1: 1-16. Hamilton, W. D. (1964b). The genetical evolution of social behavior II. J. Theor. Biol. 7: 17-51. Holdridge, L. R. (1967). Life Zone Ecology, Tropical Science Center, Costa Rica. Horwich, R. H., and Gebhard, K. (1986). Relation of allomothering to infant age in howlers Alouatta pigra, with reference to old world monkeys. In Taub, D. M., and King, F. A. (eds.), Current Perspectives in Primate Social Dynamics, Van Nostrand Reinhold, New York, pp. 66-88. Horwich, R. H., and Johnson, E. D. (1986). Geographical distribution of the black howler (Alouatta pigra) in . Primates 27: 53-62. Hrdy, S. B. (1974). Male-male competition and infanticide among the langurs (Presbytis entellus) of Abu, Rajasthan. Folia Primatol. 22: 19-58. Hrdy, S. B. (1976). The care and exploitation of nonhuman primate infants by conspecifics other than the mother. Adv. Study Behav. 6: 101-158. Hrdy, S. B. (1977). The Langurs of Abu: Female and Males Strategies of Reproduction, Harvard University Press, Cambridge, MA. Hrdy, S. B. (1979). Infanticide among animals: A review, classification, and examination of the implications for the reproductive strategies of females. Ethol. Sociobiol. 1: 13-40. Izawa, K. (1988). Preliminary report on social changes of red howler monkeys. (Alouatta seniculus). Field Stud. New World Monkeys La Macarena 1: 29-33. Izawa, K. (1989a). Social changes within a group and reproduction of wild howler monkeys (Alouatta seniculus) in Columbia. Field Stud. New World Monkeys La Macarena Colombia 2: 1-6. Izawa, K. (1989b). The adoption of an infant observed in a wild group of red howler monkeys (Alouatta seniculus). Field Stud. New World Monkeys La Macarena Colombia 2: 33-36. Izawa, K. (19940. Social changes within a group of red howler monkey, V. Field Stud. New World Monkeys La Macarena Colombia 9: 33-39. Izawa, K., and Lozano, H. (1991). Social change within a group of red howler monkeys (Alouatta seniculus.). III. Field Stud. New World Monkeys La Macarena Colombia 5: 1-16. Jones, C. b. (1980a). The functions of status in the mantled howler monkey Alouatta palliata Gray: Intraspecific competition for group membership in folivorous neotropical primates. Primates 21: 389-405. Jones, C. B. (1980b). Seasonal parturition, mortality, and dispersal in the mantled howler monkey (Alouatta palliata Gray). Brenesia 1: 1-10. Infant-Nonmother Interactions 471

Jones, C. B. (1985). Reproductive patterns in mantled howling monkeys: mate choice, estrus, and copulation. Primates 26: 130-142. Jones, C. b. (1995). Alternative reproductive behavior in the mantled howler monkey (Alouatta palliata Grey): Testing Carpenter's hypothesis. Bol. Primatol. Latino 5: 1-5. Kowaleski, M., Bravo, S. P., and Zunino, G. E. (1995). Aggression between Alouatta caraya males in forest patches in northern Argentina. Neotrop. Prim. 3: 179-181. Kurland, J. (1977). Kin selection in the Japanese monkey. Contributions to Primatology, Karger, Basel. Lancaster, J. (1971). Play-mothering: The relations between juvenile females and young infants among free-ranging vervet monkeys. Folia Primatol. 15: 161-182. Lippold, L. K. (1988). A census of primates in Cabo Blanco absolute nature reserve, Costa Rica. Brenesia 29: 101-105. Lippold, L. K. (1989). A wet season census of priates at Cabo Blanco absolute nature reserve, Costa Rica. Brenesia 31: 93-97. Mack, D. (1979). Growth and development of infant red howling monkeys (Alouatta seniculus) in a free-ranging population. In Eisenberg, J. F. (ed.), Vertebrate Ecology in the Northern Neotropics, Smithsonian Press, Washington, DC, pp. 127-136. Mendes, S. L. (1989). Estudio ecological de Alouatta fusca (Primates: Cebidae) na estacao biologica de Caratinga, MG. Rev. Nordestina Biol. 6: 71-104. Neville, M. K. (1972). Social relations within troops of red howler monkeys (Alouatta seniculus). Folia Primatol.. 18: 47-77. Rhine, R. J., Norton, G. W., Roertgen, W. J., and Klein, H. D. (1980). The brief survival of free-ranging baboon infants (Papio cynocephalus) after separation from their mothers. Int. J. Primatol. 4: 401-409. Rudran, R. (1994). Influences of male invasions in red howlers and a review of infanticide in nonhuman primates. Curr. . Rumiz, D. I. (1990). Alouatta caraya: Population density and demography in northern Argentina. Am. J. Primatol. 21: 279-294. Scott, N. J., Jr., Malmgren, L. A., and Glander, K. E. (1976). Capturing and marking howler monkeys for field behavioral studies. Primates 17: 527-534. Sekulic, R. (1982). Behavior and ranging patterns of a solitary female red howler (Alouatta seniculus). Folia Primatol. 38: 217-232. Sekulic, R. (1983a). Male relationships and infant deaths in red howler monkeys (Alouatta seniculus). Z. Tierpsychol. 61: 185-202. Sekulic, R. (1983b). Spatial relationships between recent mothers and other troop members in red howler monkeys (Alouatta seniculus). Primates 24: 475-485. Serio-Silva, J. C., and Rodriguez-Luna, E. (1994). Howler monkey (Alouatta palliata) behavior during the first weeks of life. Universidad Veracruzana, Veracruz, . Shoemaker, A. H. (1982). Fecundity in the captive howler monkey (Alouatta caraya). Zoo Biol. 1: 149-156. Silk, J. B. (1980). Kidnapping and female competition in captive bonnet macaques. Primates 21: 100-110. Smith, C. C. (1977). Feeding behavior and social organization in howling monkeys. In Clutton-Brock, T. (ed.), Primate Ecology, Academic Press, San Francisco, pp. 97-129. Stoner, K. E. (1994). Population density of the mantled howler monkey (Alouatta palliata) at La Selva Biological Reserve, Costa Rica: A new technique to analyze census data. Biotropica 26: 332-340. Stoner, K. E. (1996). Habitat selection and seasonal patterns of activity and foraging of mantled howling monkeys (Alouatta palliata) in northeastern Costa Rica. Int. J. Primatol. 17: 1-30. Struhsaker, T. (1977). Infanticide and social organization in the redtail monkey (Cercopithecus ascanius schmidti) in the Kibale Forest, Uganda. Z. Tierpsychol. 45: 75-84. Taub, D. M. (1979). Dynamics of male care-taking behavior among wild Barbary apes. Am. J. Phys. Anthropol 50: 486. Taub, D. M. (1980). Testing the "agonistic buffering" hypothesis. I. The dynamics of participation in the triadic interaction. Behav. Ecol. Sociobiol. 6: 187-197. 472 Clarke, Glander, and Zucker

Trivers, R. L. (1972). Parental investment and sexual selection. In Campbell, B. (ed.), Sexual Selection and the Descent of Man, Aldine, Chicago, pp. 136-179. Trivers, R. L. (1974). Parent-offspring conflict. Am. Zool. 14: 249-264. Wasser, S. K. (1983). Reproductive competition and cooperation among female yellow baboons. In Wasser, S. K. (ed.), Social Behavior of Female Vertebrates, Academic Press, New York, pp. 349-390. Wasser, S. K., and Barash, D. (1981). The "selfish" allomother. Ethol. Sociobiol. 2: 91-93. Wilson, E. O. (1975). Sociobiology: The New Synthesis, Belknap, Cambridge. Zucker, E. L., and Clarke, M. R. (1992). Developmental and comparative aspects of social play of mantled howling monkeys in Costa Rica. Behaviour 123: 144-171. Zunino, G. E., Chalukian, S. C, and Rumiz, D. I. (1985) [Infanticide and infant disappearance related to male takeover in groups of Alouatta caraya.] In Mello, M. T. (ed.), Primatol. No. Brasil 2: 185-190, Soc. Brasil. Primatol., Brasilia. Zunino, G. E., and Rumiz, D. I. (1986). [Observations on the territorial behavior of the black howler monkey (Alouatta caraya).] Bol. Primatol. Argentino 4(1): 36-52.