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Photographs included in the original manuscript have been reproduced xerographically in this copy. Higher quality 6” x 9” black and white photographic prints are available for any photographs or illustrations appearing in this copy for an additional charge. Contact UMI directly to order. UMI A Bell & Howell Information Company 300 North Zeeb Road, Ann Arbor MI 48106-1346 USA 313/761-4700 800/521-0600 RAPID PHYSICAL DEVELOPMENT AND MATURATION, DELAYED
BEHAVIORAL MATURATION, AND SINGLE BIRTH IN YOUNG ADULT
CALLTMICO: A REPRODUCTIVE STRATEGY
DISSERTATION
Presented in Partial Fulfillment of the Requirements for the
Degree of Philosophy in the Graduate School of
The Ohio State University
By
Donald P. Anderson, B.A., M.A.
The Ohio State University 1996
Dissertation Committee:
F.E. Poirier Approved By
P.W. Sciulli
D.E. Crews Advisor Department of Anthropology UMI Number: 9630841
Copyright 1996 by Anderson, Donald P. All rights reserved.
UMI Microform 9630841 Copyright 1996, by UMI Company. Ail rights reserved. This microform edition is protected against unauthorized copying under Title 17, United States Code. UMI 300 North Zeeb Road Ann Arbor, MI 48103 Copyright by Donald P. Anderson 1996 Dedicated To The Memory Of The Founding Callimico Populat
At
Brookfield Zoo, Brookfield IL ACKNOWLEDGMENTS
I extend my appreciation to my advisor, Dr. F. E. Poirier, for his patience, encouragement, and tireless enthusiasm throughout my graduate school career. Gratitude is also eagerly expressed to the other members of my dissertation committee, Dr. Paul Sciulli and Dr. Douglas Crews, for their support, comments, and suggestions. Singular recognition to
Dr. George Rabb, Executive Director of Brookfield Zoo, for his approval in allowing me to revitalize this project.
Special thanks to Dr. Ben Beck, whose expertise is illustrated by the comprehensive nature of this document.
Further acknowledgment for completion of this undertaking is congenially conveyed to Dr. Ojo Arewa, Saed Bahrami, Dr.
Elissa Derrickson, Dr. Kristen Gremillion, Elizabeth Mathis,
Jim Ogden, Dr. Melinda Pruett-Jones, Jan Ramer, Beate
Rettberg, Rose Scola, Carol and Vince Sodaro, Angel
Thompson, and Mark Warneke. Lastly, my heartfelt appreciation goes out to all members of the staff at
Brookfield Zoo who contributed to and participated in the successful management of the fledgling Callimico colony. VITA
1944 Born Paris, TX, Lamar County
1989...... B.A. Cum Laude Memphis State University, Memphis, TN
1992...... M .A. The Ohio State University, Columbus, OH
PUBLICATIONS
Beck, BB, Anderson, D, Ogden, J, Rettberg, B, Brejla, C, Scola, R, & Warneke, M (1982) Breeding the Goeldi's Monkey at Brookfield Zoo. International Zoo Yearbook 22:107-114.
Anderson, D, (1977) Breeding the Geoffroy's Cat at the Overton Park Zoo. International Zoo Yearbook 18:164- 167.
Anderson, D, (1975) Determination of the Gestation of the Geoffroy's Cat. Animal Keepers Forum.
FIELDS OF STUDY'
Major Field: Anthropology Studies in Callimico Social Behavior, Primate Behavior, Hominid Evolution, Behavior Ecology Theory
iv TABLE OF CONTENTS
DEDICATION...... ii
ACKNOWLEDGMENTS...... iii
VITA...... iv
LIST OF TABLES...... viii
LIST OF FIGURES...... x
CHAPTER PAGE
I. THE GOELDI'S MONKEY
Introduction...... 1 Description of Study Subjects...... 2 Research Goals...... 4 Summary of Study Methods and Data Grand Totals..... 6 Summary of Study Results...... 15 Conclusions ...... 23
II. CALLIMICO LITERATURE REVIEW
Introduction...... 26 Callimico Evolution and Taxonomy...... 27 Callimico Behavior: Naturalistic Studies...... 37 Callimico Behavior: Captive Studies...... 51 Conclusions...... 68
III. CARE OF OFFSPRING BY INDIVIDUALS OTHER THAN THE MOTHER IN SMALL-BODIED NEOTROPICAL PRIMATES
Introduction...... 70 Communal Infant Care...... 74 The Role of the Male in Infant Care...... 75 The Role of Older Siblings in Infant Care...... 87 Conclusions...... 101
v IV. MATERIALS AND METHODS
Introduction...... 104 Study Population...... 104 Study Site...... 108 Sampling Methodology and Techniques...... 112 Data Analysis and Presentation...... 116 Conclusions...... 120
V. ATTAINMENT OF BODY WEIGHT AND BEHAVIOR IN MATURING CALLIMICO
Introduction...... 121 Methods...... 123 Results...... 126 Discussion...... 129 Functional Significance of Rapid Physical and Delayed Behavioral Maturation...... 132 Conclusions...... 135
VI. PARENTS AND INFANT CARE IN CALLIMICO
Introduction...... 137 Methods...... 139 The Role of Callimico Mothers and Fathers in Infant Care...... 141 Sex and the Frequency of Parent-Infant Care-giving...... 152 Conclusions...... 166
VII. OLDER SIBLINGS AND INFANT CARE
Introduction...... 168 Methods...... 169 Juvenile Siblings and Infant Care...... 171 Subadult Siblings and Infant Care...... 179 Conclusions...... 189
vi VIII. PREVIOUS INFANT CARE EXPERIENCE AND PRIMIPAROUS PARENTS
Introduction...... 191 Methods...... 191 Primiparous Mothers and Previous Infant Care Experience...... 193 Primiparous Fathers and Previous Infant Care Experience...... 202 Conclusions...... 209
IX. CALLIMICO IN CAPTIVITY
Introduction...... 212 Impact of Physical and Behavioral Development On Intragroup Behaviors in Callimico...... 213 Callimico and Sociobiology...... 217 Conclusions...... 222
APPENDICES
A: Goeldi's Data Sheet...... 231
B: Figures...... 232
REFERENCES...... 253 LIST OF TABLES
TABLE PAGE
1. Average Age in Days of Attainment of Behavioral Developmental Landmarks in Captive Callimico...... 128
2. Individual Members of each Callimico Group at Brookfield Zoo...... 140
3. Percentage of Time Adults in each Callimico Group At Brookfield Zoo carried Newborns...... 144
4. Proportion of Occurrence Grand Totals of Studied Behaviors between Callimico Parents and Offspring....149
5. Proportion of Occurrence Grand Totals in 10 Interactive Behaviors between Callimico Parents and Offspring by Sex of Actors...... 159
6. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors among First-born Juveniles, Fathers, and Mothers Carrying Newborns...... 174
7. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors among Callimico First-born Juvenile Females and Males, Fathers, and Mothers carrying Newborns...... 178
8. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Group 3's First-born Offspring (Lew) and Parents following Birth of Subsequent Infant...... 183
9. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Group 3's First-born Offspring (Lew) and Parents following Birth of Second Infant...... 186
viii 10. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Group 3's Second-born Offspring(Kris) and Parents following birth of Subsequent Infant...... 188
11. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Juvenile Daughters and Parents during Infancy of Second-born Offspring...... 195
12. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Group 2's First-born Offspring (Judy) and Parents during Infancy of Second-born Offspring...... 198
13. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Group 5's First-born Offspring (Prima) and Parents during Infancy of Second-born Offspring...... 201
14. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Group 4's First-born Offspring (Antonio) and Parents during Infancy of Second-born Offspring...... 204
15. Proportion of Occurrence Grand Totals of Close Proximity and Contact and Passive and Reluctant Share Behaviors between Primiparous Callimico Parents and Offspring during Infancy.....208
ix LIST OF FIGURES
FIGURES PAGE
1. Development of Locomotor Independence in Callimico Infants...... 232
2. Grand Totals: Infant Carry by Callimico Parents...... 233
3. Grand Totals by Week: Infant Carry by Callimico Parents...... 234
4. Infant Carry by Callimico Parents Group 1 by Week....235
5. Infant Carry by Week of Second-born Infant by Callimico Group 5 Parents and Juvenile Sister...... 236
6. Infant Carry by Week of First-born Infant by Callimico Group 5 Parents...... 237
7. Infant Carry Grand Totals by all Callimico Parents and Juvenile Offspring...... 238
8. Infant Carry Weekly Average by all Callimico Parents and Juvenile Offspring...... 239
9. Infant Carry Totals by Week for all Callimico Parents and Juvenile Offspring...... 240
10. Infant Carry Totals by Week for Callimico Group 3 Parents and Juvenile Son (Lew)...... 241
11. Infant Carry Totals by Week for Callimico Group 3 Parents and Subadult Son (Lew)...... 242
12. Callimico Group 3 Juvenile and Subadult Siblings Approach and Sit-by One Another while Subadult carried Infant...... 243
x 13. Callimico Group 3 Parents and Juvenile and Subadult Siblings Passive Share with Infant 244
14. Infant Carry Grand Totals of Second-born Infants by Callimico Parents and Juvenile Daughters...... 245
15. Infant Carry Totals by Week of Second-born Infants by Callimico Parents and Juvenile Daughters...... 246
16. Infant Carry Totals by Week Callimico Group 2 Parents and Juvenile Daughter (Judy)...... 247
17. Infant Carry Totals by Week: Callimico Group 5 Parents and Juvenile Daughter (Prima)...... 248
18. Infant Carry Grand Totals: Callimico Group 5 Parents and Juvenile Daughter (Prima)...... 249
19. Infant Carry Totals by Week: Callimico Group 4 Parents and Juvenile Son (Antonio)...... 250
20. Infant Carry Grand Totals of Second-born Infant by Callimico Group 4 Parents...... 251
21. Infant Carry Totals by Week: Callimico Group 7 Primiparous Parents...... 252
xi CHAPTER I
THE GOELDI'S MONKEY
Introduction
The Goeldi's monkey, Callimico goeldii, is a little known South American primate that inhabits the eastern flank of the Andes mountains and is found in small numbers in
Bolivia, Brazil, Colombia, Ecuador, and Peru. Because it is morphologically intermediate between cebids (true New World monkeys) and callitrichids (marmosets and tamarins), C. goeldii may be a useful model for clarifying the evolutionary history of Neotropical primates (Hershkovitz,
1977). The most striking feature separating C. goeldii from the callitrichids and aligning the species with cebids is the birthing of single infants in C. goeldii as opposed to twinning in callitrichids.
It is proposed that early sexual maturity in C. goeldii offsets the apparent disadvantage of giving birth to single infants as opposed to twins. Although C. goeldii physically develops and matures earlier than the callitrichids, the species appears to reach landmarks of behavioral development 2 later than their callitrichid counterparts. This research examined if delayed behavioral maturation in C. goeldii provides an advantage to maturing individuals by holding them near their natal group through one or more subsequent cycles of infant birth and development. If practicing infant care-giving behavior leads to more developed parental skills as suggested for colobines, where 'aunting' behaviors are prevalent (Nicholson, 1987), this could prepare a young adult Goeldi's monkey to become a successful first-time parent. As a result of C. goeldii's limited geographic distribution in relation to callitrichid populations, its low population density and propensity for birthing single infants, early and consistent reproductive success in young adults likely is imperative for the survival of the species.
Description of Study Sample
The genus Callimico consists of a single species, C. goeldii. Various investigators have placed the Neotropical primates in Callitrichidae (marmosets and tamarins), Cebidae
(true New World monkeys), and Callimiconidae (C. goeldii)(Ford, 1986; Hershkovitz, 1977; Hill, 1957; Martin,
1990; Rosenberger, 1981; Simons, 1972). Recent biomolecular studies have shown that C. goeldii is more closely aligned with the Callitrichidae but has a long evolutionary history, implying it diverged from a lineage leading to the common ancestor of marmosets and tamarins (Dutrillaux et al., 1988;
Fanning et al./ 1989; Seuanez et al., 1989). C. goeldii has been variously referred to in primate literature as the
Goeldi's monkey, Goeldi's marmoset, or Springtamarin. The designation Callimico will hereafter be used to refer to the species. Because Callimico is a monophyletic species, the title will be used in a singular form unless otherwise stated.
Callimico inhabits primary and secondary upper
Amazonian rainforest beyond the headwaters of the Amazon river. Its distribution is limited to the region south of the Caquetci and Japur& rivers (southern Colombia and northwestern Brazil) and north of the Madre de Dios river
(northwestern Bolivia) throughout southern Colombia, northwestern Brazil, and eastern Peru into northwestern
Bolivia. The species is found as far west as the Andean foothills up to an elevation of 500 meters (Hershkovitz,
1977) .
Callimico is sexually monomorphic, with an adult body weight of approximately 550 grams (g), a head-to-rump length of 19.0-26.4 centimeters (cm), and a tail length of 22.0-
32.5 cm (Gateman, 1990; Hershkovitz, 1977; Napier & Napier,
1967). Adults of both sexes have similar pelage and lack conspicuous secondary sexual characteristics. The pelage consists of a thick glossy black coat that covers the head, dorsal and lateral features of the trunk, almost the entire tail and dorso-lateral surfaces of the limbs. The glossy black pigment of the pelage blends with the black skin of the lips, snout, rims of the ears, and the dorsal and volar surfaces of the hands and feet. In contrast to the thick black pelage and darkly pigmented skin areas, the remainder of the animal's skin is flat-white or, infrequently, light pink in color. The skin on the stomach, chest, and flexor areas of the fore-and hindlimbs is lightly haired or exhibits a hairless condition. Erect, black head hair forms a bouffant-like crown beginning just above the eyebrows and extending over most of the frontal, temporal, and parietal areas of the cranium. The face is orthognathous and the bridge of the nose is suppressed, giving Callimico a snub nosed countenance (Heltne et al., 1981; Napier & Napier,
1967) .
Research Goals
Callimico was brought to the attention of North
American science in 1904 by Goeldi & Hagman. It is rare in its natural habitat and is listed in Appendix I of the
Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES) (Wolfheim, 1983). Because of its natural pelage camouflage, diminutive size, crepuscular behavior pattern, and low population density, it has been little studied in the wild. Several investigations of captive populations initially dealt almost exclusively with breeding and maintenance of each collection (Heinemann,
1970; Heltne et al., 1973; Lorenz, 1966, 1969, 1970, 1971,
1972; Lorenz & Heinemann, 1967). A few reports have since targeted Callimico reproductive behaviors and an attendant subtopic, parental behavior of adults toward newborn infants
(Beck et al., 1982; Carroll, 1982; Heltne et al., 1981;
Pook, 1978), but no investigations studied the behavioral relationship of older siblings to the reproductive male
( Reproductive success in young adult Callimico is defined as survival of the infant to locomotor independence, with both parents participating in rearing the offspring during its dependence cycle. Three primary hypotheses are to be tested in this study. They are: 6 1. Delayed behavioral and accelerated physical maturation resulting in limited infant care-giving experience in concert with single births in young adult Callimico are a reproductive strategy; 2. Infant care-giving behavior experience is essential to successful parenting in young adult Callimico; 3. Learned infant care-giving behaviors by yearling subadult Callimico are markedly different from a similar suite of behaviors in a juvenile six- month-old sibling. Summary of Study Methods and Data Grand Totals In July 1977 five adult Parks. The individuals were paired according to size and approximate age. A program of daily systematic observations recording the behavioral activity of each c? and 9 pair was immediately initiated to monitor the behavior and physical condition of the five pairs of Callimico (Beck et al., 1982) . Data were collected continuously in 60 minute sessions for each group. At least one hour daily was set aside to collect social behavior data during the early stages of the Callimico management program. As the mated Callimico groups settled into their daily routine in captivity and the animal management timetable became more flexible, more time each day (one to two hours) was set aside for behavioral observations. Accumulation of data was almost exclusively my responsibility during the first 27 months of the Callimico colony's existence. The behaviors recorded during each observation session included: 1 . Approach and Sit-by 2. Solicit Groom 3. Allogroom 4. Autogroom 5. Pilo/Display 6. Hop Over 7. Tail Over 8. Ventral Tail 9. Genital Mark 10. Active Share 11. Passive Share 12. Reluctant Share 13. Long Call 14. Carrying Time 15. Approximate Nursing Time 16. Pilo/Solicit Display 17. Arm Over Definitions of each behavior appear in Chapter IV, Materials and Methods, in the section subtitled, Sampling Methodology and Techniques. A sample data collection sheet is provided in Appendix A. A brief summary of the collected data grand totals for the listed behaviors is presented to demonstrate the robusticity of the data set and the comprehensive nature of this project. The focus for acquisition of social behavior data were nine nuclear family groups of Callimico, represented by the five Zoo. During the study period, the population grew from 10 to 25 animals. Adult pairs formed the nucleus of the 2402 hours of collected raw data. The offspring, beginning with each individual's first incidence of behavioral interaction with its parent(s), were the focus of 1304 hours of collected raw data. Callimico is a gregarious and social primate. The following data sequences are presented first as interactive behaviors and second as solitary behaviors. Interactive Behaviors. Adults solicited one another to be groomed 13,631 times and grooming occurred 9181 times (67% of the occurrence of grooming solicitation). Adult females (99) solicited males (d'd') 7164 times and were groomed 5509 times (77% of the occurrence of grooming solicitations) . Adult d'd' solicited 99 6467 times and were groomed 3672 times (57% of the occurrence of grooming solicitations). Adult 99 solicited d'd' 2.98 times per hour and the d'd? responded by grooming 9 9 2.29 times per hour. Conversely, adult d'd solicited 9 9 2.69 times per hour, but were groomed only 1.52 times per hour. Adults solicited offspring to groom 1207 times and were in turn groomed by offspring 1935 times (160% of the occurrence of grooming solicitation). During grooming sessions between parents and offspring, young Callimico were often seen to spontaneously groom the parent that had just previously groomed them. Offspring solicited adults to groom 4361 times and were groomed 2711 times (62% of the occurrence of grooming solicitation). Adults solicited offspring to groom 0.93 times per hour and offspring groomed adults 1.48 times per hour. Offspring solicited adults to groom 3.34 times per hour and were groomed 2.08 times per hour. Adults approached and sat by one another 6222 times or 2.59 times per hour. Males approached and sat by ¥? 3719 times or 1.54 times per hour, and ¥9 approached and sat by dd 2503 times or 1.04 times per hour. Adults approached and sat by offspring 619 times or 0.47 times per hour. Adult dd approached and sat by offspring 340 times or 0.26 times per hour, and 9? approached and sat by offspring 279 times or 0.21 times per hour. Offspring approached and sat by adults 5392 times or 4.13 times per hour. Offspring approached and sat by adult dd 2353 times or 1.80 times per hour, and adult ¥9 3039 times or 2.33 times per hour. Adults initiated pilo/displays 7601 times or 3.16 times per hour, and offspring initiated pilo/displays 371 times or 0.28 times per hour. The hop-over behavior, utilized by displayers to activate other group member(s) to participate in the pilo/display, was performed by adults 3161 times or 1.32 times per hour. Adults performed the hop-over behavior toward offspring 522 times or 0.40 times per hour, and offspring performed the hop-over behavior toward adults 2153 times or 1.64 times per hour. The tail- over behavior usually occurred at the completion of a pilo/display and was performed by adults 311 times or 0.13 times per hour. Adults directed the tail-over behavior toward offspring 40 times or 0.03 times per hour, and 11 offspring directed the tail-over behavior toward adults 117 times or 0.08 times per hour. Sharing of resources was variably practiced by Callimico. Active share consisted of a food item being actively proffered to the recipient. Passive share entailed the taking of food items not being proffered, but without resisting the recipient from taking the item. Reluctant share saw an individual resisting another from taking a food item in its possession. Active sharing among adults, and between adults and offspring was a rare occurrence. Adults actively shared with adults on five occasions, adults shared with offspring 21 times, and offspring actively shared with adults five times. Passive sharing among adults was also an infrequent circumstance. Adults solicited adults on 63 occasions and sharing took place 40 times for a success rate of 63%. Adults solicited passive shares from offspring 221 times and sharing was successful 205 times or 93% of the number of solicitations. Offspring solicited passive shares from adults 1489 times and sharing occurred 1264 times for a success rate of 85%. Adults solicited reluctant shares from one another 264 times. A successful reluctant share was taken 39 times 12 (15%). Adults solicited reluctant shares from offspring 98 times and the offspring shared 52 times (53%). Offspring solicited reluctant shares from adults 358 times but were successful only 39 times (11%). While adult 9 9 were in estrus, they performed two obvious behaviors to solicit adult males' attention and interest to copulate. These behaviors have been designated pilo/solicit display and arm over and are defined in Chapter IV, Materials and Methods, in the section subtitled, Sampling Methodology and Techniques. During estrus, when adult 9? were actively soliciting adult cfcf to copulate, individual 99 performed a total of 315 pilo/solicit displays for an average of 3.4 6 per hour, and the arm over behavior occurred 195 times for an average of 1.86 per hour. Infant carrying time, an important component in the complex of infant care-giving behaviors, was variously performed by a variety of nuclear family members. A total of 15 viable births occurred during my observations of the Callimico colony, for which there are data on 13 births. These infants required 607.38 hours of carrying time by other group members. Mothers, the primary care-givers to newborn infants, carried their offspring 441.03 hours. This amounted to 73% of the total carrying time by family members. Fathers carried infants 150.66 hours, 25% of the 13 total carrying time. The newborns' older siblings carried infants 15.66 hours, 2% of the total carrying time. Newly born infants were seen to suckle 915.67 minutes (15.26 hours) during 345 hours of observation time. While being carried by the maternal 9, the 13 newborn offspring nursed an average of 2.65 minutes per hour. Solitary Behaviors. Autogrooming was the second most practiced behavior, behind solicit groom, in the Callimico behavioral repertoire. Adults performed the behavior 11,944 times or 4.97 times per hour. Between the adults, cTcT autogroomed 55% of the total autogrooming time, while 9 9 autogroomed 45% of the time. Offspring autogroomed 2329 times or 1.79 times per hour. Between offspring, cW autogroomed 57% of the total autogrooming time, and 9? autogroomed 43% of the time. Adults performed pilo/displays 7 601 times or 3.16 times per hour. Females took the lead pilo/displaying 57% of the total sum, and d'd' pilo/displayed 43% of the total. Offspring pilo/displayed 371 times or 0.28 times per hour. Offspring cW pilo/displayed 60% of the total, and 9 9 pilo/displayed 40% of the aggregate total. The ventral tail behavior was performed 11,147 times by adults or 4.64 times per hour. Males performed the behavior 55% of the time, and 9 9 performed the behavior 45% of the 14 time. Offspring performed the behavior 1273 times or 0.98 times per hour. Male offspring performed the behavior 98% of the time, while 9 9 only performed the behavior 2% of the time. Adults genital marked 3301 times or 1.37 times per hour. Adult 9 9 genital marked 72% of the adult total, and cfcf genital marked 28% of the total. Offspring genital marked 435 times or 0.33 times per hour. Offspring 9 9 genital marked 67% of the offspring total, while offspring cfd1 genital marked 33% of the offspring total. Adults long called 4593 times or 1.91 times per hour. Adult d'd' long called 51% of the total and 9 9 49%. Offspring long called 256 times or 0.19 times per hour (d'd1 74%, 99 26%) . These data reveal that Callimico is a highly social species. Heltne et al. (1981) reported that Callimico often engage in grooming sessions that are at least five minutes in duration and sometimes last as long as 15 minutes. Because episodes of auto and/or allogrooming behavior at the Brookfield colony were frequently 5-10 minutes in length (but were not precisely timed), an hour's observation schedule was often filled with social activity. Omedes and Carroll (1980) stated that Callimico is the least social of the callitrichid-like primates. The auto and interactive 15 social behavior grand totals from this study, reduced to frequencies per observation hour, indicate the species is markedly social. If Callimico is indeed cryptic in the wild because individuals are most active during the early morning and late afternoon while foraging in a near-ground level dense thicket, predator-abundant microhabitat (Buchanan- Smith, 1991; Cameron et al., 1989; Christen & Geissmann, 1994; Hernandez-Comacho & Cooper, 1976; Hershkovitz, 1977; Izawa, 1979; Pook & Pook, 1981), a major portion of each day will be spent resting, providing an opportunity for intragroup cohesion-promoting social behavior. Summary of Study Results This study will demonstrate that Callimico physically develops and matures more quickly than the callitrichids, but behaviorally matures later than the callitrichids (Chapter V). Ninety five percent of Callimico's adult mass was attained in 409 days as compared with 489 days for the common marmoset (Callithrix jacchus), 457 days for the golden-lion tamarin (Leontopithecus rosalia), and 471 days for the cotton-topped tamarin (Saguinus oedipus) (Abbott & Hearn, 1978; Altmann-Schonberner in Hershkovitz, 1977; Beck, pers. obs.; Benirschke & Richart, 1963; Coimbra-Filho in Hershkovitz, 1977; Cooper in Hershkovitz, 1977; Epple, 1970; Hampton & Hampton, 1967; Hampton et al., 1971; Hoage, 1982; Kaumanns et al., 1986; Kirkwood, 1983; Napier & Napier, 1967; Pook, 1976; Tanioka & Izawa, 1981; Winter & Rothe, 1977, 1978; Wolfe et al., 1975). Early realization of physical maturity in Callimico, resulting in successful reproductive behavior, may offset the disadvantage of giving birth to single infants as opposed to twinning in the callitrichids. Although Callimico ¥? behaviorally mature more quickly than d'd1, the species behaviorally matures less quickly than the three callitrichid species. Infant Callimico are first carried by their fathers or older siblings later than when C. jacchus and L. rosalia family group members first-carry newborns (Box, 1977; Kleiman, 1983). C. jacchus and S. oedipus infants begin to locomote independently earlier than Callimico (Box, 1977; Cleveland & Snowdon, 1984). Callimico infants begin to take food from their parents or older siblings later than L. rosalia infants (Hoage, 1982; Kleiman, 1983). Callimico offspring first play socially later than S. oedipus infants (Cleveland & Snowdon, 1984). The first incidence of a ventral tail mark and genital mark in Callimico occurs later than circumgenital marking in L. rosalia, anogenital marking 17 in S. oedipus, and scent marking in C. jacchus (Box, 1975; Cleveland & Snowdon, 1984; Kleiman, 1983). Callimico remains an infant longer (delayed behavioral development) but becomes an adult earlier (rapid physical development and maturation) than the three callitrichid species (refer to pp. 132-135). This results in a shortened juvenile and subadult development phase in the life cycle of the species. One explanation to account for this brief intermediate developmental state is a reduced need for nonparental infant care-giving behaviors that result from single births as opposed to twins. Although the parents' role in socializing offspring is brief in Callimico, the socialization behaviors learned by offspring soon lead to infant care-giving behavioral experience by older siblings following the birth of a subsequent neonate (Chapters VI and VII). Acquisition of these learned helping behaviors is essential to successful parenting in young adult Callimico (Chapter VIII). Callimico is a small-bodied monomorphic species that practices at least part-time reproductive monogamy. In other small-sized monomorphic primate species that utilize this reproductive strategy (the owl monkey, Aotus trivergatus; titi monkeys, Callicebus spp.; and marmosets and tamarins, Callitrichidae), fathers play an important 18 role in rearing offspring. Fathers in these species generally begin to carry neonates for appreciable lengths of time within the first week postpartum. Callimico fathers, unlike the callitrichids, do not begin to carry infants until several weeks postpartum and mothers carry offspring significantly more than do fathers, p=.003. These results indicate that Callimico fathers assume a lesser role in rearing offspring than the other small-bodied monomorphic Neotropical primates. As a result, the newborn spends more time in close proximity to and in contact with the reproductive ?. This study shows that Callimico is more cebid-like because mothers are more responsible for rearing and socializing their infants. In nine close proximity and contact behavioral sequences from five major behavioral categories (infant carry, solicit groom, allogroom, approach and sit-by, and hop-over), mothers and offspring interact more with one another in five behavioral sequences, while fathers and offspring interact more with one another in four behavioral sequences. In 10 resource sharing behavioral sequences from three major behavioral categories (active share, passive share, and reluctant share), mothers and offspring interact more with one another in nine behavioral sequences, while fathers and offspring interact more with one another in only one behavioral sequence (Chapter VI). Although mothers socialize more with offspring than do fathers, immature daughters are socialized more by their fathers while immature sons are socialized more by their mothers. During the close proximity and contact behavior interactions in the multiple offspring family groups with an equal sexual division of parents and offspring, fathers initiated more interactions with daughters than did mothers, and mothers initiated more interactions with sons than did fathers. Female offspring, in turn, also initiated more interactions with fathers than they did with mothers, and cf offspring initiated more interactions with mothers than they did with fathers. In contrast, fathers and sons and mothers and daughters in the multiple offspring family groups with an equal sexual division of parents and progeny shared provisions most often with each other (Chapter VI). In an early maturing short-lived species such as Callimico, being socialized by the opposite sex parent would seem to better prepare the young adult to more easily adjust to a first-time pair-bonding association with an unknown opposite sex adult. A young adult Callimico equipped with social skills consisting of pair bond social relationship compatibility and "infant care-giving experience" (ICE) would increase the likelihood of first-time reproductive 20 success. Because Callimico 9 9 become sexually mature at one year of age (Beck et al., 1982; Lorenz, 1972), their ICE is limited to the birth of one subsequent offspring in their natal group. The learned infant carrying behavior by juvenile Callimico 9 9 is minimal during this one subsequent infant dependence cycle. They carry the newborn less than 1% of the total carrying time, while fathers and mothers carry the infant 15% and 84% of the time, respectively. Because infant carrying by young 9 9 is severely limited, the suite of close proximity and contact behaviors (solicit groom, allogroom, and approach and sit-by) provides useful information regarding the number of interactions between juvenile 9 9 and their mothers carrying newborns that could result in exposure to ICE. Although juvenile 9 9 interact more with fathers rather than mothers following the birth of a second offspring, mothers approach and sit-by daughters significantly more than sons, pc.OOl. Juvenile daughters also approach and sit-by mothers significantly more than do sons, p=.04. This behavioral interaction preference by mothers and daughters gives daughters more of an opportunity to be near the newborn, observe the mother's infant care-giving behaviors, and perhaps interact with the neonate. Supported by these 21 short-term learned infant care-giving skills, young adult Callimico 9? go on to successfully rear first-born offspring (Chapters VII & VIII). Juvenile dd, unlike 99, do not become sexually mature until they are about 15 months of age. The additional three months give young dd the opportunity, at least in captivity, to experience and carry a second subsequent newborn. Infant transport of the first subsequent newborn by juvenile dd is minimal but as subadults, they carry the second newborn extensively during the middle of its infant dependence cycle. The suite of close proximity and contact behaviors between parents and immature dd also provides information regarding learned ICE by young dd. Analysis of the close proximity and contact behaviors shows that a juvenile son is still being socialized by his mother following the birth of a subsequent newborn. Because mothers are interacting more with their sons than with their daughters, and sons are interacting more with their mothers than with their fathers, juvenile dd consistently find themselves in close proximity to the newborn. They, like juvenile 9 9, are able to closely observe the newborn and the mother's infant care-giving behaviors, and perhaps interact with the neonate (Chapter VII). 22 As a subadult, following the birth of a second subsequent offspring, the behaviors of the Callimico d become noticeably different. Not only does he carry the newborn much more than do juveniles, but there is a profound difference in the number of close proximity and contact interactions between the subadult d, his father and his mother carrying the newborn. As a juvenile, the d interacted with his mother more than his father in four of the six behavioral sequences. The difference was significant in three of the sequences: juvenile d solicits parent to groom, pc.001; parent grooms juvenile d , p=.002; and juvenile d approach and sit-by parent, pc.001. As a subadult, the d interacted with his mother more than his father in all six behavioral sequences. The difference was significant in five sequences: parent solicits subadult d to groom, p=.003; subadult d grooms parent, p=.002; subadult d solicits parent to groom, pc.001; parent grooms subadult d, p=.003; and subadult d approach and sit-by parent, p=.001. As can easily be seen, the differences in the number of behavioral interactions between a juvenile and subadult Callimico d and his mother carrying a newborn are markedly different. As a juvenile, the d interacts slightly more with his mother than his father as she carries the second newborn. As a subadult, 23 the cf interacts with his mother significantly more while she carries the third newborn (Chapter VII). The additional three months it takes for young Callimico cfcT to reach sexual maturity appears to be essential for performance of adequate infant carry skills. A primiparous c? without infant carry behavior experience from two subsequent sibling births in his natal group did not carry his first-born offspring. Another young adult cf parent, with likely infant carry experience, did carry his first-born offspring. Although the primiparous father without adequate infant carry experience did not carry his first infant, there was no significant difference in the quantity of interactive behaviors between the cf and ¥ parent and the newborn. Even though he did not completely fulfill his parenting role, this primiparous father became a successful parent (Chapter VIII). Conclusions In the wild, Callimico is a little studied enigmatic primate that inhabits the upper Amazon basin in small numbers (Hershkovitz, 1977). Because the species exhibits morphological traits of both Neotropical monkeys (Cebidae) and marmosets and tamarins (Callitrichidae), its taxonomic placement is uncertain (Ford, 1986; Hershkovitz, 1977; Hill, 1957; Martin, 1990; Rosenberger, 1981; Simons, 1972). The reports on wild Callimico have concentrated on group composition, habitat preference, conspecific intergroup encounters, home range size, population density, and some social and reproductive behaviors (Buchanan-Smith, 1991; Cameron et al., 1989; Christen & Geissmann, 1994; Heltne et al., 1981; Izawa, 1979; Masataka, 1981a, 1981b; Pook & Pook, 1981, 1982). Primarily due to the long-term success of two colonies, The Jersey Wildlife Preservation Trust (UK) and Brookfield Zoo (USA), the social behavior of captive members of this species is becoming known. Although there have been several publications regarding the social and reproductive behaviors of Callimico in captivity (Beck et al., 1982; Carroll, 1982, 1985, 1988; Heltne et al., 1973; Lorenz, 1972; Lyon et al., 1985; Omedes & Carroll, 1980; Pook, 1977), no data have yet emerged documenting the relationship between the parents' role in socialization of offspring, and ICE and later reproductive success. This study recorded and analyzed new information regarding the physical and behavioral maturation of Callimico, the socialization of offspring by parents, and the effects of ICE on the quality of infant care by primiparous parents. The information from this investigation significantly adds to the body of knowledge 25 concerning Callimico behavior and expands the breadth of the data base regarding the reproductive and social behaviors of a small-bodied, monomorphic, and arguably monogamous primates. CHAPTER II CALLIMICO LITERATURE REVIEW Introduction This review comprises three sections; evolution and taxonomy, studies of the species in its natural habitat, and captive studies. Biomolecular studies of Callimico (Dutrillaux, et al., 1988; Fanning et al., 1989) show that the species has a long evolutionary history (Martin, 1992). These results are supported by the fossil evidence, as the oldest dated South American primate fossil remains, Branisella (26 mya), and primate fossil remains from North Africa, Apidium (32 mya), are morphologically similar to extant Callimico (Fleagle, 1986; MacFadden, 1990; Szalay & Delson, 1979). Classifying Callimico has been difficult because the species exhibits morphological features of both New World monkeys (Cebidae) and marmosets and tamarins (Callitrichidae). Different investigators have placed Callimico in Cebidae or Callitrichidae, while others have placed the species in its own family, Callimiconidae (Hershkovitz, 1977). 26 27 Comprehensive documentation of species specific behaviors could help clarify the taxonomic placement of Callimico. Because Callimico is small-bodied and exhibits a cryptic pelage color, while inhabiting a nearly impenetrable bamboo forest habitat, studies in its natural environment have concentrated primarily on group composition, habitat preference, intergroup encounters, home range size, and population density (Buchanan-Smith, 1991; Cameron, et al., 1989; Christen & Geissmann, 1994; Heltne et al., 1981; Izawa, 1979; Masataka, 1981a, 1981b; Pook & Pook, 1981, 1982). Little has been done to document the species' social behaviors (Masataka, 1981a, 1981b; Pook & Pook, 1981). This is not the case in captivity, where continuous access to the animals at close range has led to several publications documenting intragroup social behaviors (Carroll, 1985, 1988; Omedes & Carroll, 1980; Pook, 1977). Callimico Evolution and Taxonomy Callimico is unique among Platyrrhini because it shares morphological features of both major groups of New World monkeys. The callitrichids (marmosets and tamarins) are small bodied (range of species means is 110-700 g), exhibit claws on all digits except the big toe (hallux), possess only two molar teeth in each dental quadrant, and give birth to twins. The cebids (true monkeys) tend to be generally larger in body size. The range of body weight means for the different species varies from 730 g to approximately 13 kilograms (kg). The cebids display nails on all digits, have three molar teeth in each dental quadrant, and give birth to single offspring. Callimico resembles callitrichids in its small body size (approximately 550 g), possessing claws on all digits except the hallux, and a locomotor complex that utilizes vertical clinging and leaping as well as quadrupedal walking and running. Callimico resembles cebids in retaining a third molar. The first molar (M1) is quadricuspid (with development of a well-formed cingular conule, a hypocone), quite distinct from the M1 tricuspid pattern of callitrichids. In Callimico I1(2 and Ca are tall, narrow, and high crowned, also similar to cebid dentition. The claws of Callimico are less falcate (long, narrow, and curved) and more tegulate (short, broad, and flat). This trait appears nearer the cebid grade than the long, curved, and pointed claws of the callitrichids. The most obvious feature aligning Callimico with the cebids is the species' disposition for birthing single infants (Hershkovitz, 1977; Martin, 1992; Rosenberger, 1981). At the heart of the uncertainty concerning Callimico's taxonomic placement is whether the traits that separate the callitrichids and Callimico, and the cebids and Callimico are derived or primitive features (Rylands et al., 1993). Martin (1992) thinks it might be possible on the basis of this evidence to determine the evolutionary relationships of callitrichids and interpret the intermediate position of Callimico in terms of phylogenetic affinity. Hershkovitz (1977) and Le Gros Clark (1971) viewed small body size, possession of claws, and the occurrence of twinning as primitive characteristics. This proposition could lead to the conclusion that Callimico shares a limited number of advanced traits (the birth of single infants) with cebids and therefore is more closely related to cebids than to callitrichids. On the other hand, Martin (1992) thinks that a reduction in body size during the evolution of callitrichids and Callimico led to special adaptations consistent with development of claws, loss of third molars, and giving birth to twins (Ford, 1980, 1986; Leutenegger, 1980; Rosenberger, 1981, 1984). If this is the case, Martin (1992) sees Callimico sharing a set of derived traits with the callitrichids and together, they form a monophyletic group. 30 The debate concerning the distinctive morphology of Callimico has resulted in uncertainty about its phylogenetic relationships. These have, in turn, influenced and led to alternative classifications of the New World primates. Martin (1990), Simons (1972), and Simpson (1945) placed Callimico with the true monkeys (Cebidae), while Dutrillaux et al. (1988), Fanning et al.( 1989), Ford (1986), Napier & Napier (1967), Rosenberger (1981), Seuanez et al. (1989), and Szalay & Delson (1979) included Callimico with marmosets and tamarins (Callitrichidae). Lastly, some authors have preferred to place Callimico in a separate taxonomic family, Callimiconidae (Dollman, 1933; Hill 1957; Hershkovitz, 1977). Although the biomolecular evidence suggests Callimico is more closely related to the Callitrichidae, for consistent and convenient reference, marmosets and tamarins will be referred to as Callitrichidae, while Callimico will be referred to as Callimiconidae. Investigation of the phylogenetic relationships between cebids, callitrichids, and callimiconids have been hampered by a general scarcity of fossil remains attributed to the smaller, latter two New World primates. A few fragmentary specimens have recently been interpreted as possible relatives of callitrichids and Callimico on the basis of dental features and small size. Laverxtiana annectens, 31 Micodon kiotensis, and Mohanamico hershkovitzi, from the middle Miocene beds in the La Venta area of southwestern Colombia, have provided dental and mandibular remains, and a talus suggesting an ancestral callitrichid/Callimico occupation about 15-12 million years ago (mya). Rosenberger et al.(1991) suggested that Laventiana, represented by a mandible and talus, provided supporting evidence for derivation of the callitrichids and Callimico from a Saimiri-like ancestor. In counterpoint, Martin (1992) asserted that Laventiana does not share any derived features with extant callitrichids and Callimico; the third molar was still present (although probably relatively small, as in Cebus, Saimiri, and Callimico) and the talus does not resemble that of callitrichids or Callimico. Micodon, represented by a single isolated upper molar, with an upper incisor and lower premolar tentatively referred to the genus, is comparable in size to extant callitrichids. Whereas Micodon's molar morphology is poorly known, its most distinctive trait is a moderately well developed hypocone, as is today seen in Callimico but not in the callitrichids (Rosenberger et al., 1990). Although the Callimico condition suggests an ancestral state, Rosenberger and his colleagues (1990) argue this proposition cannot be taken literally as its morphology is different from extant 32 cebids and some callitrichids and other relevant fossils, such as the 26 mya Branisella from Bolivia. Mohanamico is known from a mandible containing the right P2-M2, left I2, C3, and P3-M2 and roots for the central incisors, right canine, and both M3s. Luchterhand et al.(1986) placed this fossil in the Pithecinae, although they recognized that this specimen shared several similarities to callitrichids and Callimico. Luchterhand et al.(1986) and Rosenberger et al. (1990) state that Mohanamico and Callimico share a possible derived similarity in the structure of P2. Both sets of authors describe this tooth as large relative to the other premolars and its protoconid projects well above the level of the other cheek teeth. Rosenberger et al. (1990) observed a feature of the anterior dentition that may also be uniquely shared by Mohanamico and Callimico. This is the combination of a gracile, moderately tall second incisor with a canine having an enlarged mesiodistal fossa. The latter is conditioned by the development of a strong lower canine precristid that flares from the body of the crown. Kay (1990) asserts that Mohanamico foreshadows pithecines whereas Callimico retains a primitive platyrrhine condition. Like pithecines, the incisors of Mohanamico are derivedly high-crowned and moderately mesiodistally compressed, while in Callimico the incisors are small, spatulate, and low-crowned. Furthermore, the Cj of Mohanamico has a sharp lingual crest, a structural detail that Kay (1990) thinks foreshadows the chisel-like arrangement seen in extant pithecines, whereas in Callimico this crest is more rounded. If Mohanamico is a sister taxon of Callimico, Kay (1990) maintains the pithecine-like characters must have evolved convergently in Mohanamico and pithecines, or Callimico must have reverted to a more primitive condition. As stated above, Callimico shares several defining features that identify the callitrichid genera. Martin (1992) thinks these characters indicate that Callimico and the callitrichids are dwarf forms derived from a larger- bodied common ancestor of New World monkeys. He sees these small-bodied species as specialized forms united by a set of derived characteristics linked to a secondary reduction in body size. Martin (1992) concludes that the most parsimonious interpretation of the evidence is that Callimico branched away from the dwarfing lineage prior to the emergence of the common ancestor of the callitrichids. According to this explanation, reduction in body size and reduction in size of the third molars, along with development of claws and reduction of the grasping adaptation of the hallux, all occurred prior to the 34 divergence of Callimico. Subsequently, the complete loss of third molars and the emergence of twinning occurred in the lineage leading to extant callitrichids. Biomolecular investigations of the similarities and differences between cebids, callitrichids, and Callimico, have provided support for the suggestion that Callimico and the callitrichids constitute a monophyletic unit. Various chromosome banding patterns have been used to karyotype Callimico, Callithrix jacchus (the common marmoset), and Saguinus labiatus (the red-bellied tamarin) (Dutrillaux et al., 1988). These have been compared to those of New World monkeys: Aotus (the owl monkey), Ateles (spider monkeys), Brachyteles (the woolly spider monkey), Cebus (capuchin monkeys), Chiropotes (bearded saki monkeys), Lagothrix (woolly monkeys), Pithecia (saki monkeys), and Saimiri (squirrel monkeys). Callitrichids and Callimico share six chromosomal rearrangements along their common stem, indicating substantial commonality prior to the divergence between Callimico and the marmoset and tamarin lineage. Callithrix jacchus and S. labiatus also shared four rearrangements prior to their divergence (Dutrillaux et al., 1988). Martin (1992) suggests this evidence fits well with the interpretation that the Callitrichids and Callimico share a common phylogeny, with an initial separation by 35 Callimico followed later by a divergence of the various callitrichid genera. Detailed comparisons of chromosomes and repetitive DNA sequences in Neotropical primates, including Callimico, provide additional confirmation that marmosets and tamarins, and Callimico form a monophyletic group, Callitrichidae (Seuanez et al., 1989). This investigation did not confirm that Callimico was the first to branch away from a common callitrichid/Callimico ancestor. Comparison of restriction maps of LINE-1 middle-repetitive DNA sequences yielded a phylogenetic tree in which Saguinus branched first, followed by Leontopithecus. This result partially corroborates an earlier study that generated a serologically-based phylogenetic tree indicating the division of Callimico and Callithrix + Cebuella as an event subsequent to Leontopithecus first branching away, followed by Saguinus (Cronin & Sarich, 1975, 1978). Cronin & Sarich's (1978) electrophoretic study of 11 isozymes yielded a similar tree, although Cebuella was shown to branch away first, followed by the Callimico and Callithrix split. Regardless of any variability in different biochemical phylogenetic trees, an investigation of satellite DNA sequences in Callimico indicated that the genus probably diverged long ago, perhaps from some other small-bodied 36 Neotropical primate (Fanning et al., 1989). Some Callimico amplified DNA sequences are not known in any other New World primate. Assuming these sequences are unique to Callimico and subject to a neutral substitution rate of 1,5><10~9/site per year, Fanning et al. (1989) conclude that Callimico separated from other New World primates at least 30 mya. The most ancient group of primate fossils to exhibit a dental quadrant comprised of a three premolar pattern is the genus Apidium, found in Oligocene deposits from the Fayum region, south of Cairo, Egypt (Africa), dating to approximately 32 mya (Fleagle, 1986; Szalay & Delson, 1979). Branisella, discovered at La Salla, Bolivia, is the most ancient example of a fossil platyrrhine, dating to approximately 26 mya (MacFadden, 1990). This specimen exhibits a dental morphology similar to Callimico (Rosenberger et al., 1990; Takai & Anaya, 1996). Takai and Anaya (1996:315) suggest that Branisella "is an ancestral group that produced ancestral, primitive callitrichines, that is, the common ancestor for Callimico and other callitrichines." Given that the ancestor of Callimico is suggested to have separated from other platyrrhines about 30 mya (the same approximate date as the occurrence of African Apidium), and that Callimico shares morphological similarities with the most archaic New World fossil remains, it appears that Callimico has experienced a long evolutionary history. Callimico Behavior: Naturalistic Studies Callimico has been difficult to study in the wild because of its darkly shaded natural camouflage coat coloration, diminutive size, habitat preference, crepuscular behavior (when shadows are longest and diurnal vision most disabled), and low population density. The reports have often been contradictory in terms of group composition, habitat preference, conspecific intergroup encounters, home range size, and population density (Buchanan-Smith, 1991; Cameron, et al., 1989; Christen & Geissmann, 1994; Heltne et al., 1981; Izawa, 1979; Masataka, 1981a, 1981b; Pook & Pook, 1981, 1982). The following synopsis of field research on Callimico is presented in several ecological components: Habitat Use; Height Preference; Locomotion; Diet and Feeding; Social Group Composition; Day Range, Territory Size, Population Density; Interspecific Associations; Social Behavior; and Reproductive Behavior. Habitat Use. Callimico seems to favor primary forest (both upland and swamp forest), but the species can also be found in small patches of secondary scrub forest within or near stands of bamboo (Buchanan-Smith, 1991; Cameron et al., 38 1989; Christen & Geissmann, 1994; Moynihan, 1976b). Izawa (1979) and Pook and Pook (1981) term Callimico a habitat specialist. Izawa (1979) observed Callimico in second growth woods, e.g., bamboo forests and forests with discontinuous canopies and a well-developed underbrush. The author designated the tree cover as a "shabby forest." Pook and Pook (1981), like Izawa, observed Callimico in a habitat of mixed forest with a discontinuous canopy cover, a well- developed undergrowth and frequent stands of dense bamboo. Izawa and Pook and Pook also reported that Callimico are not found along large rivers, but are located on a topography of rolling hills and lowlands adjacent to small river and stream beds. Pook and Pook (1981) suggested that the preference for land areas adjacent to small water courses by Callimico is dictated by a year-round consistent damp earth terra firma covered by a lush, impenetrable undergrowth. Height Preference. Callimico shows a strong partiality for remaining within a few meters of ground level within a microhabitat of a dense understory. Buchanan-Smith (1991) generally saw Callimico at heights from 1 to 5 m in scrub forest with bamboo, but observed them to ascend to heights above 12 m to eat fruit. Cameron et al. (1989) found that Callimico spent 75% of its time within 5 m of ground line, and the remaining 25% at heights between 5 and 10 m. 39 Christen and Geissmann (1994) noted that Callimico generally occupied a habitat zone ranging from ground-line to 7 m, and in only 17% of their sightings was Callimico seen at a height greater than 10 m. Pook and Pook (1981) recorded a height preference for Callimico at 2-3 m above ground line. They observed Callimico at heights of less than 5 m 88% of the time, seeing them above heights of 10 m only 4% of their observation time. In contrast, Moynihan (1976b) saw Callimico moving through all levels of bush and trees. He observed them ascend to the canopy when undisturbed, but bolt to the ground when surprised by predators. Christen and Geissmann (1994), Izawa (1979), and Pook and Pook (1981) also documented the peculiar proclivity of Callimico to often descend to the ground in search of prey and move downward to hide in the dense thicket understory. Locomotion. Because of Callimico's inclination to be most active in the lower levels of the forest, where new growth vegetation is vertically oriented, the species seems to prefer a locomotor method characterized by vertical clinging and leaping. A vertical posture appears to be essential to a locomotor method utilizing the cling and leap strategy. Izawa (1979) and Moynihan (1976a) observed Callimico vertically clinging to tree trunks, and often leaping or hopping from trunk to trunk with its head and body in a vertical position. Pook and Pook (1981:296) validated this locomotor technique as the most expedient means of travel in the understory, "the major means of support up to a height of 3-4 m were the vertical trunks and stems of trees and saplings of all ages and the most efficient way to utilize these was to travel in a vertically upright position." At the higher elevations in the forest, Callimico utilized a quadrupedal walking gait as is most often used by anthropoids. Callimico did occasionally utilize the more typical callitrichid leaping style of jumping horizontally with limbs outstretched to grasp whatever vegetation was available when moving between clusters of terminal branches (Christen & Geissmann, 1994/ Izawa, 1979; Pook & Pook, 1981). Diet and Feeding. Moynihan (1976b) reported that Callimico eats insects and berries, similar to callitrichid feeding behavior, but may ingest more fruit than most callitrichids living in a natural condition. Hernandez- Comacho and Cooper (1976) reported that the Callimico diet included small berries and fruits. Izawa (1979) and Pook and Pook (1981) observed that Callimico ate mainly insects and spiders in the lower layers of the forest, berries of scrub plants in the understory, and fruit in taller trees. Hernandez-Camacho and Cooper (197 6), Izawa (1979), and Pook and Pook (1981) chronicled Callimico feeding on the fruits of Cecropia morassi. Pook and Pook (1981) reported that Cecropia and the large sticky pod of Pitadenia sp. were staples in the Callimico diet near the end of the dry season. Although they had to climb 25-30 m to gain access to Pitadenia, they were seen more frequently feeding in less tall trees, Pourouma sp. Buchanan-Smith (1991) also observed Callimico to ascend to heights of about 12 m to feed from Pseudolmedia macrophylla trecul and Pourouma cecropia-folia trees. Pook and Pook (1981) documented that during the wet season a great variety of soft sweet fruits were taken by Callimico. These fruits became available in succession and, for periods of 4 to 10 days, their study group tended to visit one, two, or three particular types of trees that were laden with ripe fruit. Insects were also a significant element in the diet of Callimico. Pook and Pook (1981) observed that the most sought after foodstuffs during foraging were insects. It was not atypical to see an individual jump to the ground from a half meter in height, capture a large insect, and return to a height of 1-2 m to devour the prey. Pook and Pook (1981) divided the feeding behavior of an observed group of Callimico into two separate categories: (1) visits to particular feeding trees, and (2) individual 42 foraging during meandering travel. Visits to feeding trees (fruit and nonfruit) were of short duration as the study group only fed for 3-10 minutes. Foraging was most frequently observed late in the morning and during the afternoon/ and took place as the group traveled slowly, in an undirected fashion, within a few meters of the ground. Although buds, young leaves, and some fruit (Araceae) were taken during foraging, the most preferred edibles were insects, spiders, and possibly small amphibians and reptiles. Social Group Composition. Moynihan (1976) suggested that the primary group size for Callimico in southern Colombia was three, the adult pair and one offspring. Hershkovitz (1977) reported that Callimico traveled in pairs or a small family group consisting of parents and one young. Izawa (1979) received information in southern Colombia, eastern Peru, and northern Bolivia that Callimico lived in small groups of no more than five individuals. Heltne et al. (1981), after reviewing Moynihan (1976), Izawa (1979), and Pook and Pook (1979), concluded that the fundamental social group for Callimico was a nuclear family numbering between two and four individuals, an adult cf and 9 and a juvenile and/or infant. Pook and Pook (1981) observed eight Callimico in their study group in northwestern Bolivia. It 43 appeared to be composed of six adults and two subadults, which led them to assume there were perhaps two reproductive 99 in the group. Masataka (1981) recorded as many as nine individuals in his study group in northern Bolivia. He recorded a group composition of three adults, one and two 99, and six juveniles and infants. Masataka, like Pook and Pook (1981), argued that there could be more than one reproductive 9 in the social group. Cameron et al. (1989) observed Callimico in numbers from one to six individuals in northern Bolivia. Single individuals were seen on four occasions, with the probability that others were present but not observed. Groups of three individuals were twice seen, with no evidence to suggest there were other Callimico in the vicinity. A group of six individuals was observed for some time as they fed in one location. Buchanan-Smith (1991) documented a Callimico social group in northwestern Bolivia composed of seven or eight adults, one juvenile, and one carried infant. She considered the group to be cohesive as they traveled through the forest. She also thought there was more than one reproductive 9 in the group. Christen and Geissmann (1994) observed Callimico groups on six separate occasions during their survey of primates inhabiting the rainforest of northwestern Bolivia. The social group size at first encounter during the first survey 44 was documented as three individuals. The second survey recorded a single encounter with a Callimico social group consisting of five individuals. The third survey counted a single social group consisting of two individuals. During the fourth survey Callimico groups were seen on three occasions, numbering between two and three individuals. The recorded social group size and composition of wild Callimico are diverse and contradictory. Although more than one reproductive ? per social group cannot be discounted, it could be there was more than one mated pair of adults per social group or more than one family group in an extended social group. The calculations and resultant numbers describing Callimico day ranges, territory sizes, and population densities are also contradictory. Day Range, Territory Size, Population Density. Pook and Pook (1979) registered the daily travel range for a single group of Callimico as one kilometer (km). The group covered its entire home range every three to four days. Pook and Pook (1981) calculated a minimum home range size for their study group at 30 hectares (ha), but went on to speculate, because their investigation was brief and incomplete, that the study group's home range may be as large as 50-60 ha. In a report documenting the polyspecific association between Saguinus fuscicollis, S. labiatus, and 45 Callimico, Pook and Pook (1982) recorded a shared home range for the three groups at 30-35 ha. They, in turn, argued that the home range of the Callimico group may have been slightly larger than the combined species home range. Christen and Geissmann (1994) estimated the home range size for their primary polyspecific study group consisting of five or six S. labiatus, seven or eight S. fuscicollis, and three adult-size Callimico at > 80 ha. Pook and Pook (1981) calculated a Callimico group population density in their study area as approximately one group per four km2, and 0.5-2.0 individuals per one km2. Heltne et al. (1981) used the Pooks' (1979) report, recording a group of eight individuals ranging over a 35-60 ha area, to establish an individual population density. They calculated an expected population density distribution, if territories are contiguous, of approximately 10-25 animals per one km2. Their estimate was one order of magnitude greater than that determined during the census by Pook and Pook. Cameron et al. (1989) reported, from Pook and Pook (1979, 1981), a figure of 0.25 Callimico groups per one km2. From the results of their investigation, Cameron et al. (1989) calculated a social group population density of 1.6 Callimico groups per one km2. This is markedly different from reports by Pook and Pook. Cameron and 46 colleagues also calculated approximately 9.6 individuals per one km2, also quite dissimilar from the Pook and Pook data that computed 0.5-2.0 individuals per one km2. Interspecific Associations. Cameron et al. (1989) and Pook and Pook (1982) also reported on polyspecific associations between Callimico, S. labiatus, S. fuscicollis, and Callicebus cupreus. Cameron et al. (1989) found that Callimico associated with S. fuscicollis + S. labiatus 13% of the total observation time, and with S. fuscicollis + S. labiatus + C. cupreus 13% of the total observation time. Pook and Pook (1982) documented that Callimico, when in close association with S. labiatus and S. fuscicollis, spent only 23% of its time out of contact with one or both callitrichid species. Callimico showed a marked preference for associating with S. fuscicollis rather than with S. labiatus. The time spent with only one of the Saguinus groups was 30% for S. fuscicollis, but only 3% for an association with just S. labiatus. The bulk of this trilateral association took place during feeding in fruit trees or foraging for insects, larvae, and perhaps small reptiles and amphibians. Pook and Pook (1982) suggested there was little competition for food among the groups because of the use of different levels of the forest for traveling and foraging. Callimico traveled and foraged 47 almost exclusively in the undergrowth, less than 5 m above the ground. S. labiatus, on the other hand, did 77% of their traveling and foraging above 10 m, in the canopy. 5. fuscicollis were more generalized in their foraging behavior and did nearly 40% of its foraging in an ecological band between 5 and 10 m in height, sometimes climbing higher and sometimes descending lower in the forest. Christen and Geissmann (1994) briefly commented on the mixed species association phenomena. They documented Callimico, again in association with S. labiatus and S. fuscicollis. Whereas the previous reports have the three species often in close association with one another, Christen and Geissmann recorded that Callimico always kept their distance from the two Saquinus species, usually at intervals between 5 and 20 m, and at a lower elevation from them. Social Behavior. Pook and Pook (1981) documented that during traveling, foraging, and feeding, very few overt social interactions were observed to take place in the Callimico group. During rest periods when different members of the group were seen in close proximity, the most commonly observed behavior was grooming, both grooming other group members (allogrooming) and self-grooming (autogrooming). Pook and Pook accepted allogrooming as a non-exclusive form 48 of social behavior, as all adult members of the group groomed each other in turn. The Pooks' also observed the pilo-display and/or pilo-solicit, and ventral-tail behaviors (see Chapter IV for definitions). Pook and Pook (1981) recorded a single instance of what they interpreted as play behavior by a subadult Callimico. While the two parents were resting nearby, this individual climbed up and down a tree trunk, occasionally jumping to the ground and investigating among the foliage. The Pooks' think this type of behavior serves as an exploratory and learning function in young Callimico. The Pooks' also documented at least seven different Callimico vocalizations. They regarded their estimate of the number of call-types as arbitrary since in some cases different calls seemed to form a graded continuum rather than discrete types. The Callimico vocal assemblage included one long-distance call, five warning and/or agonistic calls, and one feeding location vocalization. Masataka (1982) performed a rigorous study recording the vocal repertoire of Callimico. While recording the vocalizations, the identity and behaviors of the vocalizer were recorded as were its responses to other individuals. In his report, Masataka described and defined long-distance location calls, long-distance contact calls, short-distance 49 contact calls, alarm calls, warning calls, short-distance location calls, agonistic calls, and specific calls of infants. Because there were newborns in Masataka's study group, he was able to document the ontogeny of distinctive vocalizations during infant development cycles. Masataka (1981b) also documented relationships within a Callimico group consisting of nine individuals. He recorded aggressiveness and approach-avoidance interactions among individuals in relation to subgrouping patterns, grooming relations, agonistic interactions, and food dominance at an artificially baited food station in northern Bolivia Reproductive Behavior. Masataka (1981a) described intragroup social behaviors of a Callimico group following the birth of two infants. He observed that approximately 10 days postpartum the maternal ? copulated with an adult cf. Following Masataka's estimate of an approximate gestation of 150-180 days, the observed post-parturition reproductive behavior indicated a postpartum estrus cycle that resulted in two births a year. Because the two study group infants were born just prior to the onset of the rainy season, Masataka considered that biannual Callimico births were synchronized to occur just prior to the beginning of the tropical wet and dry seasons. The infants, carried solely by their mothers for the first 10 days of life, began to receive care from other members of the social group until about seven weeks of age, when they began to locomote independently. The two obvious infant/adult interactive behaviors were infant transport and food sharing, and both were performed by all group members. The frequencies of these behaviors were highest when the infants were four to five weeks of age. Following locomotor independence, the infants spent more time with individuals closer their own age than they did with their parents. Masataka suggested that the function of the age-graded subgroup was to accelerate the infants' socialization process, while their mothers were again preparing to deliver another neonate. As this summary has shown, reports documenting the ecology of free-ranging Callimico have often been somewhat vague and conspicuously contradictory, although social and reproductive behavior may be variable depending on local environmental conditions. If inconsistent interpretation of naturalistic Callimico ecology is in part the result of inhospitable, arduous, and sometimes unpredictable fieldwork logistics, the study of captive populations should provide more consistent and uniform results. 51 C a m m i ng Behavior: Captive Studies. There are numerous studies of Callimico in captivity. Heltne et al. (1981) describe early captive studies of Callimico by Heinemann (1970), Heltne et al., (1973), Lorenz (1966, 1969, 1970, 1971, 1972), and Lorenz and Heinemann (1967) as efforts to document management and husbandry, breeding, births, parent-offspring interactions, and some social behaviors. Hershkovitz's (1977) comprehensive publication summarized results of early captive Callimico investigations. The founding of two long-term successful captive colonies of Callimico in the mid-1970s at the Jersey Wildlife Preservation Trust, Isle of Jersey (UK) and the Chicago Zoological Park (Brookfield Zoo), Brookfield, IL (USA), have generated numerous publications. The first reports concerned husbandry, management, and reproduction (Beck et al., 1982; Carroll, 1982; Pook, 1976, 1978; Wojcik & Heltne, 1978), while later publications concentrated on social and reproductive behaviors (Altmann, et al., 1988; Carroll, 1985, 1988; Carroll et al., 1989; Christen et al., 1989; Feistner & Price, 1991; Jurke et al., 1994; Lyon et al., 1985; Masataka, 1983; Omedes & Carroll, 1980; Tardif, 1994; Zeigler et al., 1989). A summary of these publications will be presented under the subheadings: Captive Living Environments; Diet; Medical History; 52 Reproductive Behavior; Care of Offspring; and Social Behavior. Captive Living Environments. The captive housing accommodations for Callimico during the early studies were simple affairs. Lorenz (1969) kept an individual in his office where it had free run of the facility. The Heinemann's (1970) kept a pair of Callimico in their apartment. They erected an artificial bamboo tree, upon which the adult pair was to live and socialize. After a surviving offspring was born, the Callimico family was installed in a plastic-sided l-2*l-5xl-0 m cage equipped with branches set at different heights, a resting perch, and nestbox. The animals were irradiated with ultraviolet light for 10 minutes every other day to supplement natural sunlight. Lorenz (1972) did not supply any supporting data but specified that the minimum enclosure size in which to keep nuclear family groups of Callimico was to be at least 2-0x2-0><2*0 m in size. Each unit was to be equipped with sufficient branches, boards, and perches to promote adequate exercise and subdivide the enclosure into microhabitats. A nestbox was provided for animal security and used as a transport device following capture of an individual. Lorenz (1972) suggested an ambient room temperature between 21-28° 53 C. Ultraviolet light was provided for 10-15 minutes every second or third day to supplement under-exposure to natural sunlight. Carroll (1982) kept Callimico in two indoor enclosures that measured l-2x0-9xi*5 m and l*8x0-9xi*5 m. Each indoor unit abutted an outdoor enclosure approximately 2-5 m in height, with a floor area of 7-9 m2. The indoor units were constructed of Darvic, a robust PVC, and fitted with an infrared heat source, several horizontal perches, a corner shelf, feeding platform, and nestbox. As the nestboxes went unused, they were replaced by an additional shelf in several enclosures. The outdoor habitats were decorated with natural wood perches, live shrubs, and climbing plants. Indoor temperatures ranged from 22-25° C, with a relative humidity between 60-70%. Beck et al. (1982) stated that living quarters for Callimico should be at least 3*0x2*0x2-5 m in dimension. They suggested covering the frame with 4-5x4-5 cm wiremesh, although tile, glass, or plastic siding are suitable. A nestbox, several wooden and wiremesh-covered perches placed approximately 2 m above the floor, and a three dimensional climbing network of natural or simulated branches (2-5-5*0 cm in diameter) should be provided to assure adequate exercise. A temperature of 25° C ± 1° was maintained at the Brookfield 54 colony, with a relative humidity of approximately 60%. The animals were kept under fluorescent light with a constant photoperiod, 0700-2100 hours, followed by ten hours of darkness. Without 14 hours of constant light there was inadequate food consumption. Because vitamin D was a regular supplement in the Callimico diet at Brookfield, the colony did not require natural or artificial ultraviolet light. Diet. Lorenz (1969) maintained an individual Callimico on a diet of fruits, vegetables, bread, and animal protein. Approximately 50% of the animal's diet consisted of protein from locusts, grasshoppers, minced meat, mice, and chicks. Vitamin D3 was administered in large doses in the drinking water to facilitate calcium absorption. The Heinemanns' (1970) fed their individuals a combination of apples, bananas, grapes, raisins, bread, raw egg, and up to 50 mealworms daily. Later, ground beef, mice, and lizards were added to the dietary regimen. A concentrated vitamin D formulation was administered to expedite absorption of calcium. Beck, et al. (1982), Carroll, (1982), and Lorenz (1972) followed the original concept of providing two categories of food. A staple of dry, manufactured carbohydrate rich primate diet was supplemented by a variety of fresh fruits 55 and vegetables, domestic meat produce, hard boiled eggs, peanuts, and some dairy products. The basic diet consisted of the manufactured product and fruits and vegetables and was augmented with a wide variety of live protein. Carroll (1982) fed live insects and freshly killed newborn mice. Beck et al. (1982) provided crickets, mealworms, live hairless mouse pups, earthworms, and anoles when available from a vendor. Drinking water was provided ad libitum in each setting. Carroll (1982) provided a vitamin B12 and E supplement, while Beck et al. (1982) issued a supplement of vitamin C and vanilla flavored powdered protein. Medical History. Lorenz (1972) observed that the most common medical problem in Callimico was intestinal parasites. This disorder did not become dangerous as long as the animals were minimally stressed and kept in good condition and there was prophylactic administration of prescribed parasite control medications. Carroll (1982) found little evidence of internal parasites, but lost individuals from septicemia, congestive heart failure, and Yersinia pseudotuberculosis infection. There are two confirmed cases of colonic adenocarcinoma and hepatic myelolipomas in Callimico (Hauser & Baumgartner, 1991; Richter et al., 1980). This rare tumor-like but apparently metaplastic lesion resulted in the loss of both individuals. 56 Callimico, being a gregarious and active primate, is regularly susceptible to small skin injuries that commonly occur on the face, chin, hands, and feet (Beck et al., 1982; Lorenz, 1972). These wounds usually healed rapidly without medical treatment. Reproductive Behavior. Although related to callitrichids, Callimico differs markedly in its reproductive biology (Hershkovitz, 1977). As callitrichids usually give birth to twins, only rarely do Callimico give birth to twins (Hill, 1966; Altmann et al., 1988). Given the past practice of assuming monogamy in small-bodied Neotropical primates, the utilized optimum reproductive unit for captive Callimico is a mated male and female pair (Beck et al., 1982; Carroll, 1982; Heinemann, 1970; Heltne et al., 1973; Heltne et al., 1981; Hershkovitz, 1977; Lorenz, 1966, 1969, 1972; Lorenz & Heinemann, 1967; Pook, 1976, 1978; Wojcik & Heltne, 1978) . Because Callimico ¥9 deliver single offspring and may not require the number of infant care-giving helpers seen in callitrichids, Carroll (1988) predicted that mating exclusivity is not a prerequisite of Callimico. Breeding ¥¥ may be more tolerant of other ¥9, and multi-¥ breeding groups might be stable in the wild and in captivity. Carroll (1988) tested the Pook and Pook (1979) and Masataka 57 (1981a) hypothesis of polygyny in Callimico as the Pooks' observed two infants of similar size and predicted age in their study group and Masataka observed two 9 9 both carrying infants in his study group. Carroll (1988) established three breeding groups of Callimico, each with one cf and two unrelated 99. In Group 1 both 99 successfully birthed and reared infants, whereas in Group 2 neither infant that was born survived beyond three days postpartum. Group 3 was stable for slightly more than one month, and neither 9 was pregnant when the relationship broke down between the 99. All three trios were disbanded following severe fighting between the groups' two 99. In all three cases both 9 9 sustained injuries and one 9 emerged dominant to the other following the confrontation. In Group 2, a two-day-old infant was killed during the fighting. Carroll states that a breakdown in the relationship between the 9 9 was not observed prior to initiation of physical conflict. Carroll (1988) asserted, in the absence of data from field studies of Callimico, that it was impossible to interpret these findings. He predicted that multi-9 breeding groups may occur and be more stable in the wild, where a subordinate 9 has more opportunity to avoid direct conflict with her dominant counterpart. Beck et al. (1982) and Lorenz (1972) determined that Callimico 99 become reproductively mature at 12 months and cfcf at 14-18 months of age. There is a postpartum estrus cycle (Beck et al., 1982; Zeigler et al., 1989) and copulations can occur three to seven days following birth (Beck et al., 1982). Several recent studies registering the occurrence of different hormone peaks in urine indicate that postpartum ovulation occurs in Callimico approximately three weeks following the birth of an infant. Carroll et al., (1989) measured concentrations of urinary oestrone conjugates in four reproductively viable Callimico 99. Their results suggested that oestrone 3- glucuronide was the most abundant urinary oestrogen of those measured, and this metabolite provided a good indicator of ovarian cyclicity and pregnancy. Their work resulted in determination of a mean ovarian cycle length of 23.8 ± 0.6 days. Christen et al., (1989) isolated and extracted urinary oestradiol from two Callimico 99. Both individuals displayed regular cycles in urinary oestradiol levels. Their results indicated that Callimico ovulations occur approximately mid-way through each period of elevated oestradiol levels, which can be divided into a follicular phase, an ovulatory phase, and a luteal phase. The mean 59 cycle length for nine complete ovarian cycles was calculated to be 27.8 ± 5.2 days. Jurke et al. (1994) measured pregnanediol-3«glucuronide (PdG) in the urine of six Callimico ¥? during pregnancy and the postpartum estrus period. A conception cycle was defined as one in which the concentration of urinary PdG remained above 0.20 jt/g/mgCr in all urine samples collected between day one and day 20 after ovulation. Their work resulted in determination of a mean ovarian cycle length of 22.6 ± 4.7 days. Zeigler et al. (1989) collected first morning void urine in four multiparous Callimico ¥¥, beginning at one birth and continuing until the next birth. Urine samples were assayed for creatinine (Cr), bioactive luteinizing hormone (LH), and estrone conjugates (EjC) . This assay used a PdG rabbit antiserum and measured estrone in its conjugated form directly in the urine without hydrolysis, extraction, or column chromatography. From their results, Zeigler et al. (1989) computed a mean ovarian cycle length following the birth of an infant at 17.8 ± 6.3 days for Callimico. These investigations agree with previous estimates of postpartum estrus cycles based on behavioral evidence in the absence of hormonal evidence. Lorenz (1972) reported a mean ovarian cycle length of 22 days, while Beck 60 et al. (1982) suggested a 24-day interval. During estrus the ¥ pilo-solicits the in an arched back posture, with limbs extended and pelage erect on the dorsal aspect of her trunk. From this posture standing motionless or slowly walking, she stares directly at the male (Beck et al., 1982; Lorenz, 1972). Carroll (1982) did not observe this solicitation behavior by ovulating ¥¥. While the ¥ is in estrus, the follows her more closely, frequently sniffs her genital area, and directs a tongue flicking behavior toward her. Copulations are dorsal- ventral and may include multiple mounts with intromission over short periods of time. Copulations generally cease during pregnancy (Beck et al., 1982; Carroll, 1982; Lorenz, 1972) . Jurke et al. (1994) calculated a gestation length of 151.6 ± 1.6 days, while Zeigler et al. (1989) estimated a gestation length of 148 ± 6.3 days for Callimico. These numbers are in close agreement with previous gestation lengths calculated from behavioral indicators. Beck et al. (1982) and Carroll (1982) recorded a mean gestation of 160 days, while Lorenz (1972) determined a mean gestation of 154 days. The duration of gestation is slightly longer in Callimico than in the callitrichids, as the gestation for Cebuella, Callithrix, Saguinus, and Leontopithecus is 138, 61 137, 140, and 133 days, respectively (Hershkovitz, 1977). Abdominal swelling is not obvious until the second trimester of pregnancy in Callimico. Genital marking increases during pregnancy and, as parturition approaches, the 9 moves more slowly and urinates more frequently. From about 30 days before birth, the base of her tail is clearly and continually wet with urine. Her appetite may dissipate several days before delivery, and her vagina may swell and open slightly (Beck et al., 1982; Lorenz, 1972). The litter size for Callimico is one. Beck et al. (1982) recorded the weights for six newborns; three 9 9 at 63, 55, and 46 g, and three cfcf at 45, 46, and 66 g respectively. This is approximately 10% of the body weight of an adult. Healthy infants cling to the back of their mother's neck, beneath a heavy pelage cape, and are difficult to detect. They are fully furred and appear as miniature replications of adults, although some depigmentation of the pelage has been seen to occur. Their eyes appear to be open at birth and the newborns are relatively active as they crawl over their mother's shoulder into a ventral nursing position (Beck et al., 1982). Care of Offspring. Parental behavior in Callimico is quite different from the callitrichids. Callitrichid fathers begin to carry newborns between day one and three 62 postpartum, while Callimico fathers do not begin to carry newborns until they are about three weeks of age (Heltne et al., 1981; Pook, 1978). Beck et al. (1982) reported that mothers carried newborns for the first three weeks, after which fathers began to carry the neonates. Carroll (1982) reported the age of newborns at first transfer to fathers to be 23 days. Heinemann (1970) and Heltne et al. (1973) reported that newborns are first carried by their fathers during the third week postpartum. Pook (1978) gave an average of 23 days, and Arentsen (1977) gave 25 and 30 days postpartum as the time of first newborn transfer to fathers. Beck et al. (1982) found that older siblings began to carry newborns in the fifth week postpartum. Carroll (1982) reported that other group members began to carry newborns about 34 days postpartum. Arentsen (1977) reported siblings carrying newborns 36 days postpartum. Pook (1978) reported an average of 45 days postpartum before older siblings began to carry newborns. During this time the infants are not held, cradled, or otherwise assisted and must actively cling to or, during transfer, crawl from one animal to another. Beck et al. (1982) reported that, if they are to become successful parents, immature Callimico require infant care- giving experience (ICE). One of the principal costs of 63 learned infant care is reflected by increased size of the social group and the concomitant escalation of stress associated with large group numbers. Lyon et al. (1985) witnessed increased aggression and peripheralization of a young adult ? following the birth of a subsequent sibling. Beck et al. (1982) discovered that the average age at which infants are first seen to leave a parent or sibling was 43 days, the earliest departure was 24 days postpartum. Carroll (1982) recorded a mean of 44 days postpartum when infants were seen moving independently around the enclosure. In contrast, Pook (1978) reported an average age of 37 days, Heinemann (1979) estimated one month of age, and Arentsen (1977) and Heltne et al. (1973) reported infants independent of their parents at six weeks of age. Beck et al. (1982) saw many young Callimico fall from varying heights in their initial attempts at practicing independent locomotor skills. They recommended that the enclosure floor be properly cushioned to decrease the chance of injury during such events. Carroll (1982) recorded that infants were weaned by about 16 weeks of age. In contrast, Heltne et al. (1981) documented complete weaning as being accomplished by week 12 or shortly thereafter. From about four weeks of age, Carroll (1982) observed infant Callimico taking food from 64 parents and older siblings. Active food sharing, in which the offering is proffered, by other social group members with infants has been reported by Feistner and Price (1991). They suggested that adults vocalize a willingness to share food with infants. Carroll (1982) observed that by the time Callimico are one year old, they are of adult size and weight and have developed full adult pelage. Beck et al. (1982) separated young adult family-reared offspring from their natal group at 12-18 months of age for mated pairings. This was in response to increased levels of stress in the family group, successful reproductive behavior had increased group numbers beyond the capacity of a limited spatial environment. Tardif (1994) addressed the relative energetic cost of infant care in Aotus, Callicebus, Callimico, Saimiri, and the Callitrichidae, and its relation to infant care patterns. Her results suggest that factors other than the immediate energetic costs of lactation and transport affect the participation of mothers in infant transport and their need for helpers in infant care. She concluded that energetic cost is a relatively poor predictor of the mother's need for infant care helpers. Tardif suggested two factors which could better explain patterns of infant care by mothers versus social group others in small-bodied 65 primates. Comparison of the relations between anti-predator strategies and foraging rate efficiency could suggest differences which affect the need for non-maternal infant care. Tardif also suggests that differences in the availability of suitable helpers are likely to affect the degree to which mothers may relinquish care to others. Social Behavior. As described in Chapter I, Callimico in captivity is a gregarious and social species. Heltne et al. (1981) and Hershkovitz (1977) reported that autogrooming and allogrooming are fairly frequent activities in captivity. Episodes of allogrooming that continued for five minutes were common and bouts of 15 minutes or longer were observed. Heltne et al. (1981:189) described grooming behavior as, "using its hands, the groomer will usually search carefully through the pelage of its partner, parting a few hairs at a time and peering closely at the underlying skin surface. Occasionally the groomer may bend to nibble or lick at the skin or pull a few hairs up between the teeth." Omedes and Carroll (1980), performed a short-term comparative study of pair behavior in Callithrix jacchus, Leontopithecus rosalia, Saguinus fuscicollis, S. oedipus, and Callimico. They determined that Callimico pairs interacted least in close proximity behaviors: approach, 66 leave, walk by, and hop over partners They also demonstrated that Callimico pairs spent less time in contact or close proximity than did other paired species. Because Kleiman (1977) found that monogamous pairs show high amounts of nonsexual social interaction, Omedes and Carroll (1980) suggest that Callimico may not be as strictly monogamous as callitrichids. Carroll (1985) investigated pair-bonding behavior in Callimico to determine whether behavior interaction frequency and duration between and ? predicted a monogamous reproductive strategy for the species. Kleiman (1977) enumerated distinct characteristics of monogamy. (1) Reduction in behavioral and physical sexual dimorphism. (2) Paired individuals spend long periods of time in close physical proximity, and display synchronized behaviors. Callimico shows no physical sexual dimorphism (Beck et al., 1982, Carroll, 1982; Lorenz, 1972), although Carroll (1985) reports there are several behaviors where dimorphism can clearly be seen. The two areas where behavioral dimorphism was apparent were in initiation and maintenance of proximity and in group defense. Initiation and maintenance of contact and proximity were both due primarily to actions by the cf. During group defense, when displaying toward neighboring 67 groups or animal management personnel, cfcf displayed significantly more than did ??. Kleiman (1977, 1981) suggested that ?? in monogamous pairs should be equally, if not more so, involved in territorial defense. Carroll (1985) concluded that, although Callimico shows rapid formation of very strong social bonds, the two partners do not maintain bonding equally. Carroll asserts that Callimico does not meet the criteria for strict monogamy; which may not represent the species' full range of reproductive strategies. Wojcik and Heltne (1978) observed and recorded tail marking behavior (ventral tail) in Callimico, differentiating between two categories, full tail and half tail mark. The behavior was described as: The tail is extended in the sagittal plane, the proximal one-third elevated as the distal two-thirds coil ventrally toward the base . . . The animal sweeps the genito-anal region with this coil, vertically and from left to right, using the tail base as the driving lever (1978:507). Wojcik and Heltne suggest that tail marking functions as a grooming solicitation, an indicator of sexual receptivity, or a territorial signal. Masataka (1983) recorded and analyzed responses to natural and synthesized alarm calls in captive Callimico. He found significant differences in the alarm calls that 68 signal the presence of arboreal and terrestrial predators. Masataka concluded by speculating that species differences in alarm calls may result from environmental influences which have forced the warning to take on a specific form in accordance with the physical situation in which the call must be executed. Conclusions Fossil and biomolecular evidence suggest that Callimico has a long evolutionary history (Dutrillaux et al., 1988; Fanning et al., 1989; Kay, 1990; Rosenberger et al., 1990; Seuanez et al., 1989; Takai & Anaya, 1996). Perhaps the phylogeny of Callimico is reflected in the unique suite of morphological traits that align it with both Neotropical monkeys (Cebidae) and marmosets and tamarins (Callitrichidae). If the evolutionary history of Callimico predates all current New World primates, the species could be viewed as an extant ancestral archetype (Dutrillaux et al., 1988; Takai & Anaya, 1996). The mixed morphology shown by Callimico might, then, be expected in a group related to a common ancestor of true monkeys, and the marmoset/tamarin group. Because Callimico exhibits a shared morphology with the two major families of New World primates, it has been placed in Cebidae (Martin, 1990), in Callitrichidae 69 (Dutrillaux et al., 1988), and in its own family, Callimiconidae (Hershkovitz, 1977). Callimico has been little studied in its natural habitat, and most investigations have concentrated on the ecological mechanics of adaptation to the environment (Buchanan-Smith, 1991; Cameron, et al., 1989; Christen & Geissmann, 1994; Heltne et al., 1981; Izawa, 1979; Masataka, 1981a, 1981b; Pook & Pook, 1981, 1982). A small number of investigations attempted to document the intragroup social behavior of family groups (Masataka, 1981a, 1981b; Pook & Pook, 1981), but these have been of short duration. Although captive studies of Callimico cannot document daily travel path length, territory size, population density, frequency and duration of interspecific behavioral encounters, and the age of young adults when they disperse from the natal group; these investigations could provide an accurate account of the frequency and duration of intragroup behaviors. If free-ranging Callimico groups are indeed most active during early morning and late afternoon and are in seclusion and resting for the remainder of the day, the suite of behaviors performed while the social group is sedentary may be reflected in behaviors performed while at rest in a captive environment. CHAPTER III CARE OF OFFSPRING BY INDIVIDUALS OTHER THAN THE MOTHER IN SMALL-BODIED NEOTROPICAL PRIMATES Introduction Infant care-giving behavior by individuals other than the mother is neither unique to nor prevalent in mammals. Kleiman (1977) and Lack (1968) report that more than 90% of all avian species exhibit high levels of parental investment, whereas this is the case for less than 3% of mammalian species. What is unique to mammals, especially the small-bodied New World primates, is the degree to which fathers and other group members (older siblings and nonrelated adults) play a role in the care of newborns. These individuals display myriad behaviors (carrying, food sharing, play, grooming) relating to the care and socialization of infant(s). Fathers play a primary role in performance of infant care behaviors, but older siblings also participate in infant care, perhaps to learn behaviors that will result in successful parenting. 70 71 In a review of the interactive relationship between primate infants and adult d'd', Whitten (1987) developed five categories (intensive caretaking, affiliation, occasional affiliation, tolerance, use and abuse), and documented the occurrence of these behaviors. Whitten (1987:343) defined an infant as, "any immature animal still dependent on its parent(s) for milk or transport." The five categories defining the cf parent/infant behavioral association begin with intensive caretaking, in which the cf spends a large part of each day engaged in infant care-giving that includes performance of parental behaviors for all infants. This behavioral complex can be seen in Callithrix jacchus (Box, 1977), Saguinus fuscicollis (Cebul & Epple, 1984), Hylobates syndactylus (Chivers, 1974), Macaca sylvanus (Deag, 1974, 1980; Taub, 1984), Callitrichidae and Callimiconidae (Hershkovitz, 1977), Callitrichidae (Tardif et al., 1993; Vogt, 1984), and Aotus trivirgatus and Callicebus spp. (Kinzey et al., 1977; Wright, 1984). Affiliative care-giving behaviors involve an adult cf spending part of his day engaged in associative interactions with one or more specific infants. These associations generally lack extensive care-giving but often involve strong and enduring relationships, and have been observed in 72 Alouatta pigra (Bolin, 1981), M. arctoides (Estrada, 1984), Gorilla gorilla beringei (Fossey, 1983), Papio spp. (Hamilton, 1984), P. cynocephalus anubis (Ransom & Ransom, 1971; Smuts, 1985), and P. c. cynocephalus (Stein, 1984). Occasional affiliation consists of short-term associations between adult d'd' and infants. In this category 1973), Theropithecus gelada (Dunbar, 1984), M. fuscata (Gouzoules, 1984; Itani, 1959; Takahata, 1982), and P. hamadryas (Kummer, 1968). Tolerance is seen by Whitten (1987:350) as, "males are generally indifferent to infants but tolerate their occasional proximity." Species that practice this behavior are Cercopithecus diana (Byrne et al., 1983), M. fascicularis (Mitchell & Brandt, 1972), Presbytis melalophus (Curtin, 1980), P. potenziani (Wittenberger & Tilson, 1980), and Papio spp. (Vogt, 1984). Whitten considered this category to be under-represented because current lack of knowledge, rather than an absence of interactions with infants, was the primary obstacle in defining this classification of male/immature behavioral relationships. The most controversial infant care-giving behavior, most prominently seen in Papio spp. (savanna baboons), is a cf carrying or holding an infant during an interaction with another cf. Whitten (1987) termed this behavior as "use and abuse," while other investigators have defined such interactions as "agonistic buffering" (Deag & Crook, 1971), "kidnapping" (Popp, 1978), "infant use" (Strum, 1984), "infant carrying" (Busse & Hamilton, 1981), "countercarrying" (Hamilton, 1984), "tripartite relations" (Kummer, 1967), and "triadic male-infant interactions" (Taub, 1980). The most common context surrounding these encounters appears to be tension between the cfcf, as the approach or proximity of one cf to the carrier Investigators have proposed three different strategies to account for this behavior: (1) exploitation of the infant for one male's advantage (Hrdy, 1976; Strum, 1984), (2) protection of the infant from harassment and aggression (Packer & Pusey, 1985), and (3) development of relationships with the infant's mother (Smuts, 1985). Smith and Whitten (1988), after reviewing the evidence, concluded there are probably multiple factors at work, but the development of social relations between the cf and the infant's mother is an influential issue. 74 Because Callimico fathers participate in intensive infant care-giving behaviors, I will henceforth concentrate on this aspect of Whitten's (1987) description of male- infant interactive relationships observed in primates. Expansion of the father's role as infant care giver to include other social group members is necessary because intensive communal care of newborns seems to be a signature behavior among mammals for the small bodied cebids, the callitrichids, and Callimico. This summary will evaluate familial infant care behaviors in petite Neotropical primates and will focus on infant care-giving actions of older siblings, the non-reproductive helpers in the social group. Communal Infant Care Intensive infant care-giving behaviors in primates by other social group members are most common in, but not limited to, small-bodied Neotropical species (Dixson & Fleming, 1981; Goldizen, 1987; Hershkovitz, 1977; Rothe & Darms, 1993; Tardif et al., 1993; Whitten, 1987; Wright, 1984, 1990). Leutenegger (1980) argued that small body size resulted in social and sexual monogamy which, in turn, resulted in twinning and a high mother-to-litter weight ratio. These costs to the mother resulted in infant care- 75 giving behaviors by the father and other members of the social group (Hershkovitz, 1977). Although New World callitrichids were once thought to be exclusively monogamous and live in small family groups, there is now disagreement whether the modal mating system of some species in the wild is monogamy or polyandry (Dietz et al., 1994; Garber et al., 1984; Rothe & Darms, 1993; Sussman & Garber, 1987; Terborgh & Goldizen, 1985; Wright, 1990). Whatever the adopted reproductive strategy, the inability of a single adult ¥ callitrichid to raise multiple offspring with a high total litter weight created selection for care of newborns by the father and other social group members (Wright, 1990). With a mother/litter weight ratio as high as 24% in Cebuella (Hampton et al., 1977; Soini, 1988), infant carrying represented an unacceptable cost to a small-bodied callitrichid mother. Consequently, infant carrying by other members of the social group became a necessity. The Role of the Male in Infant Care Goldizen (1987), Vogt (1984), and Whitten (1987) present excellent reviews of paternal care in New World primates. Goldizen (1987) documented, from various captive studies, the percent of time adult New World primate genera Aotus, Callicebus, Callimico, Callithrix, Cebuella, Leontopithecus, and Saguinus all perform these intensive infant care-giving behaviors. Aotus and Callicebus. The cebids Aotus trivirgatus and Callicebus moloch exhibit extensive paternal infant care. Both primates are small, approximately one kg in weight, practice reproductive monogamy, and give birth to single infants. The data from captive studies show the Aotus father to be the primary infant carrier from the first day postpartum. During the next 11 weeks, the father carried the infant 51-81% of the time. By five months of age the infant was completely independent of its parents (Dixson & Fleming, 1982; Fragaszy et al., 1982; Wright, 1984). Wright (1984), during a study of wild C. moloch, documented the father as being the primary carrier of a newborn from the first week postpartum. By the third week, the father carried the infant 92% of the time. By eight weeks of age, 77 the infant was carried 57% of the time by its father and was independent 40% of the time. At 12 weeks, the infant was independent 60% of the time and carried by its father 38% of the time. At 16 weeks of age, the infant was carried by the father only 1% of the time. Fragaszy et al. (1982), following a study of two captive groups of C. moloch, reported that infants spent substantially greater proportions of time in contact with fathers than with mothers. The results of this study showed that infants were in contact with mothers between 5 and 25% of the time, while they were in contact with fathers 57-75%. Fragaszy and colleagues argue that extensive paternal care in C. moloch is associated with the development of a strong attachment by the infant for its father. As a result, social relations between the mother and infant are substantially different from those reported for species in which maternal care is prevalent. In conclusion Robinson et al. (1987) reported that in both Aotus and Callicebus, between birth and weaning (six to seven months), the infant is only carried by its mother 3% of the time. The Callitrichids. Captive and wild investigations of callitrichid behavior have shown that fathers generally carry infants as much or more than mothers. In the wild 78 this has been seen in Callithrix humeralifer (Rylands, 1985), Cebuella pygmaea (Soini, 1988), Leontopithecus rosalia (Dietz et al., 1994), Saguinus fuscicollis (Goldizen, 1987b; Terborgh & Goldizen, 1985), and S. mystax (Garber, 1986). In captivity this is also the case for C. jacchus (Box, 1975; Ingrain, 1977, 1978; Rothe et al., 1993; Tardif et al, 1986; Yamamoto, 1993), C. pygmaea (Christen, 1974; Hershkovitz, 1977); Leontopithecus rosalia (Hoage, 1978), S. fuscicollis (Cebul & Epple, 1984; Epple, 1975b; Vogt et al., 1978), and S. oedipus (Tardif et al., 1986). Callithrix jacchus. All members of the genus Callithrix are approximately the same size and sexually monomorphic. They are smaller than Saguinus but larger than Cebuella. Adults weigh between 300-450 g and a newborn weighs 22-38 g (Hershkovitz, 1977). The mother/litter weight ratio for twins is approximately 18%. Box (1975) observed and recorded infant carrying behavior for C. jacchus during the infants' first four weeks of life. During week one, the father carried one or two infants 23.9% of the total carrying time. During weeks 2-4, the father carried infant(s) 10.0%, 13.2%, and 6.8% of the time, respectively. In contrast, from weeks 1-4, the mother carried infant(s) 30.8%, 27.3%, 30.3%, and 24.8% of the time. In a later long-term investigation of one main and 79 three secondary groups of C. jacchus, Box (1977) determined that adults principally carried newborns during their first four weeks of life only in the absence of nonreproductive helpers. Ingram (1977), in an infant care study of four groups of C. jacchus, found that fathers carried infants considerably more than did mothers. During the first week postpartum, fathers carried infants approximately 45% of the time, while mothers carried only 36%. During weeks 2-6, fathers carried 22%, 45%, 17%, 20%, and 10% of the time, respectively. In contrast, mothers during the same period carried infants 34%, 32%, 20%, 12%, and 5%. Following week six postpartum, the infant is independent of its parents about 80% of the time. Engel (1985) observed and recorded the social interactions between adults carrying infants and group members without infant care experience in three reproductively successful groups of captive C. jacchus. She found that parents and adult offspring monopolized carrying newborns. In Group 1, the parents and a pair of adult daughters carried the newborns 91.8% of the time. In Group 2, the parents and a pair of adult sons carried the newborns 90.5% of the time. In Group 3, the parents and a single adult son carried newborns 93% of the time. Infant 80 transport was equally distributed among the three groups of adults with the exception of Group 2. In that group the mother and adult sons carried newborns 85.3% of the time, while the father only carried 5.2%. Yamamoto (1993), following an investigation of the interactive behaviors between C. jacchus infants and social group others, determined that mothers and fathers carried infants for equivalent amounts of time. From weeks 2-4 postpartum, infants were carried by parents 96% of the time. Between 5-10 weeks of age, infants were only carried by parents 29.5% of the time, and 12-16 weeks postpartum, infants locomoted independently of their parents. Cebuella pygmaea. C. pygmaea is a monospecific genus and the smallest member of the Suborder Anthropoidea. Soini (1988) determined the mean weight for adults as 119 g and the weight for a newborn as 13-15 g. Because the mother/litter weight ratio for twins is 24%, prohibitively high for a small-bodied Cebuella mother, it is imperative that the father supplements the mother in regard to infant transport (Soini, 1988) . During a short-term study of the early development and care of a single newborn in a group of eight free-ranging individuals, Soini (1988) recorded that the father contributed 0-12% of the total carrying time, with a mean of 81 2.4%. The bulk of infant transport was performed by an associate cf and the oldest sibling, a 9 approximately 1-5 years old. These two individuals carried the infant about 61% of the time, the older sibling being the principal carrier until the third week postpartum. Soini suggested the subadult 9 relinquished carrying duties because the infant had grown too heavy to be supported by her body weight. In a captive study of C. pygmaea, Christen (1974) noted that parental carrying of newborns was variable as the mother carried infants 41% of the total time during week two postpartum, but only 21% of the time during the third week. The infants locomoted independently by seven weeks of age. Leontopithecus rosalia. Members of the genus Leontopithecus are monomorphic and the largest of the callitrichids. The mean body weight for captive adults is approximately 710 g and the mean weight for a newborn is about 60 g (Hershkovitz, 1977; Hoage, 1978, 1982). The mother/litter weight ratio for twins is about 17%. L. rosalia seems to occupy an intermediate position between the callitrichids and Callimico in regard to the role the father plays in infant care. Hoage (1978) recorded infant care behavior among all family group members in seven reproductively successful groups of L. rosalia. His results 82 showed that, with the exception of one 10-minute infant steal, fathers never carried infants during the first week postpartum. During the second week, fathers carried 16.4% of the total carrying time, while mothers carried infants 87.1%. Changes were dramatic during the third week as mothers carried 59.5% of the time and fathers carried 38.8%. During the fourth and fifth weeks, fathers carried 53.3% and 42.6% of the time, while mothers carried infants 41.1% and 44.7%, respectively. From weeks 6-12, as the infants became independent, fathers carried an average of 26.9%, while mothers carried 13.0% of the total carrying time. Hoage (1978) learned that infant carrying patterns for L. rosalia differed distinctively from the rest of Callitrichidae. Fathers rarely began to carry infants in the first week postpartum and, on average, only began to carry infants during the second or third week postpartum. They became the primary infant carrier during weeks 4-12 of an infant's life. Saguinus fuscicollis. Saguinus are larger than Callithrix but smaller than Leontopithecus. S. fuscicollis are monomorphic, d'd' weigh about 328 g and ?? 338 g (Soini, 1983). The weight of a newborn is approximately 43 g (Hershkovitz, 1977). Twin births result in a high mother/litter weight ratio (24%) making infant transport by 83 other group members advantageous. Epple (1975b) recorded infant carrying behavior in seven groups of S. fuscicollis during the first 40 days following births of infants. She found that all group members shared in carrying newborns. However, there was considerable variability both within and between groups. The least active father performed only 29.9% of all infant carrying in his group, while the most active father carried infants 95.6% of the time. The percentages obtained by mothers carrying infants outside of nursing time also varied greatly. The most active mother performed 69.1% of all carrying in her group, while the least active mother only carried 1.0% of the time in her group. Vogt et al. (1978) observed one family group of S. fuscicollis through three consecutive sets of newborn twins. Data on infant carrying, from birth through 12 weeks of age, showed that the father carried more than did the mother. The father carried infants 32%, 57%, and 42% of the time for the three litters, while the mother carried 21%, 12%, and 5%. The data also revealed that, generally, cfcf (immature and mature) carried more than ??. The d'd' in the group carried the three litters 77%, 72%, and 76% of the time, while ?? carried infants 23%, 28%, and 24%, respectively. 84 Following a study of seven reproductively successful S. fuscicollis groups, Cebul and Epple (1984) showed that the ratio of infant carrying during nursing versus infant transport independent of nursing varied significantly for mothers. The least active mother only nursed infants 12.7% of all intervals when she was in possession of her offspring. The remaining 87.3% of the time, she carried them free of the cost of suckling. The most active mother nursed offspring 90.9% of her carrying time, but only carried 9.1% of the time free of nursing bouts by infants. Other social group members were responsible for carrying the infants outside the mother's nursing/infant transport direct contact time. In two wild S. fuscicollis groups, Terborgh and Goldizen (1985) found that probable fathers carried newborns. One cf carried 18%, while the second cf carried 58% of the total infant transport time. During observations of a free-ranging polyandrous group of S. fuscicollis, Goldizen (1987b) found that the two cfcf carried infants more than double the time the mother carried the newborns. Infant carrying data was recorded for the first seven weeks postpartum. The cfcf carried 50.1% and 48.7% of the total time, while the mother carried only 20.0%. In another group, where data was collected for the 85 first four weeks postpartum, the father carried infants 47.1% of the total carrying time, while the mother and two associate adult 99 carried infant(s) 32.3%, 33.8%, and 20.0%, respectively. Saguinus oedipus. S. oedipus is a sexually monomorphic species, cfcf weigh about 410 g and 99 420 g (Neyman, 1977) . A newborn weighs about 43 g (Hershkovitz, 1977) resulting in a mother/litter weight ratio of approximately 20% for twins. Following a study of the social development of S. oedipus oedipus infants during their first twenty weeks of life, Cleveland and Snowdon (1984) found that d'd1 (fathers and brothers) were much more involved in carrying infants than were 99. However, they theorized their results were strongly influenced by group composition. In groups with older siblings, infant care by mothers was greatly reduced while care by fathers remained the same. Yet, when no older siblings were present the mother carried infants as frequently as the father. Mixed Species Comparisons. In a comparative infant care study of C. jacchus and S. oedipus during the first eight weeks of the newborns' life, Tardif et al. (1986) found little difference in maternal care. However, S. oedipus fathers carried infants significantly more during weeks 5-8 (28.1%) than did C. jacchus fathers (9.6%). These 86 results seem to corroborate Cleveland and Snowdon's (1984) earlier proposition that the male's participation in infant care is more critical in tamarins than in marmosets. This has since been correlated with differences in dietary ecology resulting in a smaller home range and shortened daily travel path lengths in marmosets (Callithrix) versus tamarins (Saguinus) (Tardif & Harrison, 1994). In a rigorous investigation, Tardif and Harrison (1994) reviewed and compared infant carrying behavior in C. jacchus, S. fuscicollis, S. oedipus, and L. rosalia. During the first four weeks postpartum infant carrying rates were roughly equivalent for the four species. Following week four clear differences emerged in the patterns of infant carrying behavior. By week eight, C. jacchus parents carried infants only 11% of the time, while S. fuscicollis, S. oedipus, and L. rosalia infants were still carried 64%, 60%, and 42%, respectively. Tardif and Harrison (1994) concluded that the duration of infant care is significantly reduced in Callithrix because they are obligate exudate (gum) feeders, which results in smaller territories and shorter daily travel path lengths. While these studies show that infant carrying time by fathers is variable, there is no doubt they actively participate in caring for newborns. There is also no disagreement that fathers begin to show parental behavior, if not hours following the birth of offspring, within a day or two postpartum. A primary consideration to account for the father's role in infant care is the high mother/litter weight ratio in small-bodied callitrichids. I have calculated a mother/litter mean weight ratio for C. jacchus, S. fuscicollis, S. oedipus, and L. rosalia, where the weight of twins is approximately 18.6% of the mother's total weight (Box, 1975; Christen, 1974; Hoage, 1978; Kleiman, 1977; Leutenegger, 1973; Pook, 1984; Tardif et al., 1986). In addition to the severe cost of carrying a heavy litter weight, a free-ranging reproductive 9 must negotiate a long daily travel path. C. jacchus, S. fuscicollis, S. oedipus, and L. rosalia travel approximately 704 m, 1849 m, 1750 m, and 1496 m respectively, on a daily basis (Garber, 1988; Hubrecht, 1985; Newman, 1977; Peres, 1986). Given that infant care costs to mothers become physically unmanageable, it is imperative that fathers assume an active role in the shared responsibility of parent/infant care. The Role of Older Siblings in Infant Care Goldizen (1987a:42) defined helping behavior as, "the care of offspring by individuals who are not their parents." Brown (1987) and Reidman (1982) reported this behavior in 88 222 bird species and 120 mammal species. The Cebids. Neotropical primates are perhaps best known for infant care helping behavior by nonreproductive social group members. This behavioral complex occurs in two cebid genera (Aotus and Callicebus) and, possibly, all the callitrichids. Wild studies of A. trivirgatus and C. moloch were performed by Wright (1984) and captive studies of A. trivirgatus and C. moloch were conducted by Dixson and Fleming (1981), Fragaszy et al. (1982), and Wright (1984). While observing three family groups of A. trivirgatus, Dixson and Fleming (1981) recorded that older offspring carried newborns between 1% and 9% of the total observation time. Wright (1984) documented that during week three postpartum, an A. trivirgatus older sibling carried the newborn 28% of the time. As the infant increased in age and size, carrying by the older sibling decreased proportionately (14% at day 23, down to 13% by day 30). The individual that benefited most from sibling infant carrying appeared to be the father. The mother consistently carried about 5% of the time, but the father carried less when the older sibling assumed that responsibility. During an investigation of infant helping behavior by C. moloch, Wright (1984) recorded that older siblings carried a newborn approximately 2% of the time in the first 89 weeks postpartum. Although these studies show marginal infant care behavior by older siblings toward newborns, they do not compare with the frequency and duration of infant helping behaviors performed by callitrichid older siblings. Fragaszy et al. (1982) chronicled infant carrying behavior by a single yearling C. moloch ?. She was seen in contact with the newborn infant about 6% of the total carrying time. The yearling ? seemed startled and annoyed the first few times the infant crawled on her back; she was observed tugging and nipping the infant's limbs and tail, vocalizing loudly, and moving rapidly around the enclosure. After several carrying experiences, she became both more attentive to signs of an impending infant transfer attempt and more tolerant of the infant when it did cling to her. The Callitrichids. Given their unique position in regard to infant care within the primate order, helping behaviors of juvenile and subadult callitrichids are perhaps better understood through comparison with nonprimates for three reasons (Goldizen, 1990). (1) The helping behavior of young callitrichids is atypical of primates in terms of the high frequency of interactions and the energy cost expended though alloparenting. (2) Unlike most other primates, the young of both sexes participate equally in infant care- giving behaviors. This is frequently seen in cooperatively 90 breeding bird species (Brown, 1987; Curry, 1988; Ligen, 1981; Rabenhold, 1985; Reyer, 1980; Woolfenden & Fitzpatrick, 1984). (3) Few systematic studies of infant helping behavior in primates have been completed, while numerous studies of this behavior are available in birds (Brown, 1987). Infant helping behavior is an interesting phenomenon because it is not easily resolved in terms of individual selection. Seemingly, this suite of behaviors would potentially reduce the helper's individual fitness, but Goldizen (1990) discussed three possible benefits of infant helping behavior in young callitrichids: (1) inclusive fitness benefits increase through improved survival of younger siblings; (2) delayed benefits from reciprocal- altruism; and (3) direct benefits through infant care experience (ICE) that may increase an individual's reproductive success. In all callitrichid species that infant care has been studied, nonreproductive older siblings commonly carry their younger siblings. This behavior occurs among wild C. humeralifer (Rylands, 1985) and S. fuscicollis (Goldizen, 1987b; Terborgh & Goldizen, 1985), and among captive C. jacchus (Box, 1975; Ingram, 1977; Tardif et al., 1986), S. fuscicollis (Epple, 1975b; Cebul & Epple, 1984; Vogt et al., 91 1978), S. oedipus (Tardif et al., 1986), and L. rosalia (Hoage, 1978). Although infant carrying time is not similar among all age-sex classes of older siblings, several consistent trends have materialized. The amount of infant carrying done by older offspring increases with age in wild C. humeralifer (Rylands, 1985) and S. fuscicollis (Goldizen, 1987), and in captive C. jacchus (Tardif et al., 1986) and S. fuscicollis (Vogt et al., 1978). As long as infant care-giving behavior does not reduce reproductive success, its adaptive significance to older siblings is obvious. Perhaps older sibling caretakers benefit by gaining experience that increases their own infant-rearing skills as parents (Cleveland & Snowdon, 1984; Epple, 1975b, 1978; Epple & Katz, 1983; Hoage, 1978, 1982; Ingram, 1977; Kirkwood et al., 1983; Snowdon, 1990; Sussman & Garber, 1987; Tardif et al., (1984); Yamamoto, 1993). Although this proposition may generalize to all primates, it has been criticized. Rothe and Darms (1993:197) argue, "that infant care need not be learned directly, but rather depends on social competence in general, obtained in a complete family up to subadulthood." Tardif et al. (1984) assert that previous experience in rearing infant siblings appears to be beneficial but not essential to the development of adequate 92 maternal behavior in C. jacchus. Contrary to Rothe and Darms (1993) and Tardif et al. (1984)., several investigations of callitrichid reproductive behavior have reported that primiparous adults are more successful at rearing newborns when they have previously carried and cared for infant siblings (Epple, 1975b; Hoage, 1978; Tardif et al., 1984). Callithrix jacchus. Box (1975) showed that elder siblings carried infants appreciably more than their parents or younger siblings. Subadult twin siblings carried infants 59.2%, 68.8%, 40.0%, and 44.4% of the total time during the first four weeks following the birth of ensuing newborns. In contrast, juvenile twin siblings only carried infants 44.1%, 28.6%, 18.6%, and 14.0% of the time during the first four weeks postpartum. Box (1977) also completed a long-term evaluation of infant care in C. jacchus, observing four family groups during the first four weeks postpartum (usually twins and 18% of an adult's weight). He consistently found that older siblings, in multi-generational sibling family groups, carried newborns more often than their younger brothers and sisters, and that parental infant carrying decreased as the number of offspring increased. The individual that benefited most from infant carrying by older siblings 93 appeared to be the father. In multi-generational offspring family groups during the first week postpartum, the father carried infants no more than 10% of the time. During ensuing weeks, he did not usually handle the newborns. Ingram (1978) also investigated infant care by older siblings in three groups of C. jacchus. The siblings in Group 1 were 5-10 months older than the infants; in Group 2 they were 10-15 months older, and in Group 3 they were over 15 months older than the newborns. The older siblings in Groups 2 and 3 carried infants more often than did older siblings in Group 1. Ingram (1978) proposes two reasons for this behavior. Subadults are larger than partially grown juveniles, and are more able to carry the weight of one or two infants. Second, subadult siblings are more experienced at handling newborns since they received previous infant care by briefly carrying their now juvenile siblings. Engel (1985) studied the behavioral interactions between infant carrying and non-carrying individuals in three groups of C. jacchus. He found that older siblings carried infants much more than did their younger brothers and sisters. In the three groups studied, adult siblings carried neonates 36.0%, 46.2%, and 34.9% of the total observation time. Younger siblings only carried their infant siblings for 5.9%, 8.1%, and 7.0% of the time. 94 Experienced infant carriers generally did not tolerant individuals without ICE in close proximity. Once an inexperienced individual had successfully handled an infant, agonistic interactions between infant transport experienced and inexperienced individuals ceased. During a study of infant carrying behavior in four reproductively successful groups of C. jacchus, Rothe et al. (1993) observed that as the 'number of nonreproductive helpers increased per group, older siblings provided more infant transport relief, thereby reducing carrying costs to parents. Data were grouped into three periods coinciding with the age of newborns, period one weeks 1-3 postpartum, period two weeks 4-7, and period three when infants reached eight weeks of age. The end of the first period apparently coincided with conclusion of the mother's postpartum estrus, while the end of the second period was identified by a significant increase in the infants' locomotor independence (Engel, 1985; Stevenson & Rylands, 1988). Pooling all groups contributions to infant carrying showed an increase from 24.6% to 43.6% by nonreproductive helpers. At the same time, mothers reduced their carrying from 52% to 27.4%. Fathers carried 23.3% in period one and 29% in period two. Rothe et al. (1993) conclude that nonreproductive helpers 95 compensate for reduced infant transport by mothers. LeontopithBCUs rosalia. Hoage (1978) investigated infant carrying behavior in a family group of L. rosalia. From weeks 2-7 postpartum, juvenile ?? carried one or two infants 6.5% of the total carrying time. Between weeks 3-8 postpartum, juvenile d'd' carried one or two neonates 8.0%. Following week eight, juvenile siblings were incidental infant carriers only. Hoage (1978) also discussed the relationship between infant survival and ICE in multiparous and primiparous groups. Eight of ten newborns survived in multiparous reproductive groups, while only three of seven infants survived in primiparous groups. Although Hoage detailed the lack of ICE in the primiparous parents, he suggested their inexperience in relation to unskilled parenting remained to be demonstrated. Two primiparous couples with 191 and 242 days of prior infant care, successfully reared twin and single births, respectively. In contrast twin births to two primiparous couples with 159 and 22 days ICE, died within three days. Three of the dead infants were severely bitten and showed signs of mutilation. Although Hoage did not suggest it, it seems that deficient parenting skills were an important factor in the reproductive failure of inexperienced first-time parents. 96 Saguinus fuscicollis. Cebul and Epple (1984) investigated parental carrying, food sharing, and socialization of infants in seven reproductive groups of S. fuscicollis. They also recorded the frequency of infant transport by other group members, including older siblings. Cebul and Epple (1984) show that infant carrying by older brothers and/or sisters is variable and dependent on how frequently infants are carried by parents, especially fathers. In one group the father carried 95.6% of the time, and two sibling d'd' together carried 3.3%. Conversely, in two groups where fathers carried only 39.3% and 59.5% of the time, older siblings carried infants 32.2% and 36.7%, respectively. Cebul and Epple (1984) argue that older sibling carrying time is directly proportional to the age of the sibling and the willingness of the parents to allow siblings to carry. Epple (1975b) investigated infant helping behavior in S. fuscicollis. A seven-month-old juvenile cf carried newborns 2.2% of the total time, but at 18 months of age carried newborns 15.3%. Similarly, a 6.5-month-old 9 carried newborns 11.4% of the total time, but at 18 months of age carried 54.8%. Epple suggested that additional infant care by older siblings follows from their limited experience as juveniles and their increased size. 97 Epple (1975b) also reports that first-time parents with ICE skillfully performed their infant care duties. First time parents with ICE successfully reared all seven litters (100%). Parents where only one individual had ICE reared two of seven litters (28.6%), and parents with no ICE reared one of four litters (25.0%). Epple (1978) also showed that 76.5% of the infants born to primiparous mothers without ICE died or were severely mutilated shortly after birth. In contrast, survival of offspring of primiparous mothers with ICE was 80%. This is clear support for the hypothesis that skillful parenting behavior is learned in at least some callitrichid species. Vogt et al. (1978) document substantial infant transport by nonparents in a long-term study of one multi- generational family of S. fuscicollis. During three consecutive infant birth and development cycles, nonparents carried infants 47%, 30%, and 53%, while mothers and fathers carried 53%, 70%, and 47% of the total time. Saguinus oedipus. Cleveland and Snowdon (1984) studied the first 20 weeks of life of S. oedipus infants. They suggest one mechanism for acquiring parental care skills. They observed that juvenile animals initiated play with infants but rarely carried them. They suggest that through play older siblings learn to tolerate infants crawling over 98 them, and temporarily riding them in a dorsal position. After juveniles reach subadult s.tatus, they tolerate infants on them for longer periods of time. As a result of this experience, subadults appear better prepared to become successful parents. Following a review of the records from a captive breeding colony, Tardif et al. (1984) report that no first litter offspring survived among inexperienced S. oedipus mothers , while among experienced mothers 54.5% survived. Subsequently, inexperienced mothers successfully reared zero litters, while experienced mothers reared 100% of their litters. Autopsy records of the dead infants showed evidence of physical abuse. Infants from all inexperienced S. oedipus mothers showed signs of mutilation. Tardif et al. (1984) also observed that ICE by S. oedipus fathers is not necessary for infant survival. In the colony, 75% of infant mortality occurred during the first week of life, a period when the mother carried infants most often. Thus, the father's experience did not appear to be essential for successful reproduction. Price (1992) observed 21 S. oedipus infants for their first 12 weeks of life. His study focused on infant carrying and food sharing by parents and older siblings. His results show that carrying by mothers consistently decreased throughout the 12 week interval. In contrast, fathers and older siblings increased carrying during weeks 3-5, then carrying declined as infants learned to locomote independently. Price (1992) also observed that older siblings carried more than either parent, but both parents carried more than individual siblings. Parents also shared food with infants more than did older siblings. Lastly, older siblings contributed more to infant care than did younger siblings, and adult sons carried more than adult daughters. Conversely, immature daughters carried more than immature sons. Mixed Species Comparisons. Tardif et al. (1986) completed a comparative study of infant care in family groups of C. jacchus and S. oedipus. They subdivided older sibling infant carrying behavior into two block; Block 1, weeks 1-4, and Block 2, weeks 5-8 postpartum. Ages of older siblings ranged from 7.0 to 16.5 months. Three C. jacchus d'd', aged 10-16 months, carried infants 36.1% of the total during Block 1. In contrast, two S. oedipus dd1 of equivalent age carried infants only 7.7% of the total. Three C. jacchus ??, aged 10-16 months, carried newborns 17.5% of the total during Block 1. In comparison, two S. oedipus ?¥, aged 12.5 and 14.9, carried newborns 25.7% of the total. During Block 2 when infants were independently 100 locomoting, carrying by all older siblings, excepting S. oedipus subadult 9¥, declined. During Block 2, S. oedipus ? siblings carried infants 28.9% of the time. Tardif et al. (1986) hypothesized that maturation differences account for species differences in infant carrying. Reviewing infant carrying behavior in C. jacchus, S. fuscicollis, S. oedipus, and L. rosalia, Tardif (1993) argues that the cost of carrying neonates is less for parents in family groups with nonreproductive siblings. During weeks 1-4 postpartum, fathers carried infants less in groups with than in groups without helpers. Mothers carried less overall than did fathers, with or without nonreproductive helpers present. The data suggest that mothers may limit their infant carrying more than fathers and that fathers benefit more from the presence of helpers. Tardif et al. (1993) hypothesize that species differences in duration and intensity of infant care may alter the value of helpers. They further suggested that helpers, in addition to parents, may not be as critical to infant survival in Callithrix as they are in Saguinus. This appears related to the dietary preference of Callithrix for exudate (gum) of trees, which shortens daily travel distances and decreases energy expended in territorial defense (Harrison & Tardif, 1994). 101 Such preliminary data support the hypothesis that parental care is learned through infant carrying experience. Furthermore, such training is necessary for primiparous parents to successfully rear offspring. As yet, no comprehensive data sets have been reported that compare the reproductive success of experienced first-time parents with that of first time parents without infant handling experience. However, to date all such studies have used small samples and cannot be viewed conclusively. Studies of callitrichid behavior never will involve large samples such as are common in many avian studies. Therefore, it will be much more difficult to establish relationships between reproductive success and the presence of nonreproductive helpers in a procreating group. Conclusions Fathers and unrelated adult cfcf and older siblings in family groups of small bodied cebids and callitrichids ' actively participate in carrying newborns. Excepting L. rosalia, all callitrichid species studied carry newborns within the first few days postpartum and often within hours following birth. L. rosalia's delay in paternal and sibling infant care may be related to newborn weights. These are considerably above those of Callithrix and Saguinus. The 102 increased bulk of Leontopithecus mothers may allow them to better balance the initial cost of their extreme mother/litter weight ratio (Hoage, 1978). Callimico may be pushing the temporal limit regarding the time when fathers begin to aid mothers by carrying newborns. Callimico fathers do not begin to carry newborns until about three weeks postpartum. This may coincide with cessation of the mothers' postpartum estrus cycle that often results in conception of future offspring. Costs to mothers from lactation, infant carrying, conception, and uterine fetal growth may overwhelm their reserves. Given these conditions, parenting aid may be essential to rearing current offspring. Evolutionary implications for Callimico older siblings assisting in infant care are possibly two-fold. First, it contributes to their inclusive fitness by alleviating costs incurred by their parents. Second, it contributes to egos' own future reproductive success by preparing them for successful first-time parenthood. Hoage (1978) maintains that the likelihood of first-time parents skillfully participating in rearing offspring is increased when as juveniles and subadults they had exposure to multiple infant birth and development cycles. The purpose of this research is to demonstrate that experience is necessary for young 103 adult Callimico, especially cfcf, to skillfully rear first born offspring. Results of this research will show that Callimico physically develop, mature, and reproduce sooner than the callitrichids. Results will support the hypothesis that primiparous mothers need ICE from at least one subsequent sibling birth and development cycle in their natal group to obtain adequate ICE to rear their first newborn. Primiparous fathers will be shown to require ICE from two subsequent sibling birth and development cycles to skillfully assist the mother in rearing their first offspring. CHAPTER IV MATERIALS AND METHODS Introduction This chapter reviews the history of Callimico at Brookfield Zoo and logistics of their living sites. This review is followed by a description of techniques and methods used to collect social behavior data. Last, the techniques for data analysis are presented. Study Population In June 1977, the United States Fish and Wildlife Service, Department of the Interior, confiscated five cf and five ? Callimico at the Miami (FL) International Airport. Temporarily housed at the Crandon Park Zoo (later named Metrozoo) in Miami, they were placed on indefinite breeding loan at Brookfield Zoo, Brookfield, IL. All members of the founding population successfully reproduced. Fifteen infants were born during the study period, including two Fx 9? that later produced offspring. One founding 9 died, and one adult cf was acquired from the Oklahoma City Zoo. 104 105 Although Callimico is morphologically intermediate between Cebidae and Callitrichidae (Hershkovitz, 1977), the published literature at the time suggested they be managed as callitrichids. Reproductive success at Brookfield Zoo validated publications reporting Callimico as more likely to reproduce when quartered in pairs (Heinemann, 1970; Heltne et al., 1973; Lorenz, 1966, 1972; Pook, 1975). Given this background, the basic social unit at the Brookfield colony was one adult pair and up to three subsequent offspring. Breeding. Males were removed from their natal group to form adult pairs at 14-16 months of age, 9? at about 12 months. If no suitable mate was available, both sexes remained with the family until about 20 months of age. Young adult pairs were age-matched unless there were no partners of equivalent age. Pairings were successful between old and young individuals, although young animals, especially immature d'd', paired with older experienced mates showed signs of disturbance. These included continued running and vocalizing for up to two days following pairing. Young age-matched pairs adjusted quickly, and experienced animals quickly accepted mates. Copulations usually occurred within 24 hours of the pairing, and serious aggression was never observed between mates or newly formed pairs. Callimico exhibits an estrus cycle in captivity that generally occurs about three weeks postpartum. As a result, two founding 9 9 gave birth three times within a year. All normal births occurred at night, possibly between midnight and 0600 hours. Placentas were not observed by animal management personnel at morning rounds following births suggesting that mother's likely ate the placenta after birthing. Callimico 9 9 at Brookfield Zoo gave birth to more infants in December/January and July/August than at any other time. Of the 13 births for which there are data, three were born during December/January (23%) and six during July/August (46%). The other four infants were born in February, March, December, and June (31%). This suggests possible seasonal breeding. However, it is unclear whether these peaks represent a genuine species birth seasonality, or simply synchronization of the reproductive activity of 9 9 at Brookfield. Pregnancy. Abdominal swelling was not noticeable until after the 9 9 were 60 days pregnant. Genital marking by 9 9 increased during pregnancy and, as parturition approached, they moved more laboriously and urinated more frequently. From approximately 30 days before birth, in some cases slightly earlier, the base of the female's tail and upper hind-limbs were clearly and continually wet with urine. 107 No additional dietary supplements were administered to pregnant ¥¥, as hyper nutrition appeared to result in large fetuses and more difficult births. Third trimester pregnant ¥¥ generally ate less, and suffered from diarrhea and vomiting, especially in the last month of pregnancy. Food intake and general motor activity decreased markedly several days prior to parturition. Birth. Callimico births single infants. Healthy infants cling to the dorsal aspect of the mother's neck. Beneath a thick cape of black hair, they are difficult to see. Born as fully furred miniature adults, there is often some depigmentation of the distal pelage. The newborns' eyes are open and appear alert. They also have been seen head-turning and locomoting on the mother shortly after birth. Nursing usually occurs within eight hours postpartum, and often sooner. Suckling is difficult to observe in newborns, however, since teats are under the female's arms. Young infants are seen to crawl over or under their mother's shoulder to the nursing position. Nursing session times are approximate as the infant often falls asleep following suckling clinging to its mother in the ventral nursing position. 108 Care of Young. Mothers carry infants for the first three weeks. Following that, fathers will carry infants until they can locomote independently. One father carried his 18-day-old infant, but fathers are characteristically reluctant to carry infants before the fifth week. Young infants are not held, cradled, or otherwise assisted. They must actively cling or, during transfer to another individual, crawl from one animal to another. Older siblings also begin to carry infants for short periods about five weeks postpartum. Siblings that are about one year old participate more in infant care-giving behaviors than do juveniles. As will be shown in Chapters VII and VIII, if offspring (especially cfcf) are to become skillful first-time parents, juvenile/subadult Callimico require ICE in carrying and interacting with infant siblings. Study Site Housing. After their arrival at Brookfield Zoo and following quarantine, the founding Callimico population was installed in l*5xl-5*2-5 m wiremesh-covered cages within a no public access facility. Inside each unit were several resting and feeding perches at varying heights, a nestbox located on the highest resting perch, and a three 109 dimensional network of small diameter horizontal wooden dowels and branches (2-5-5 cm in diameter). The placement of the components of the climbing network was intended to simulate a low elevation arboreal habitat. About eight months after arrival, the colony was moved to a secluded larger building to accommodate increased population. Each group was installed in wiremesh-covered cages that measured 2-0xl-5x2-0 m. The internal cage features on which the animals rested, socialized, fed, locomoted, and exercised were similar to structures already described. The colony was again relocated one year later. Because four of the family groups now numbered four individuals, they were housed in 3-7x4-6*2-4 m room-size enclosures with tile walls and concrete floors, and fronted with a 4-5 cm2 stainless steel mesh. Within each enclosure there were a series of perches at various elevations and a nestbox. To simulate a near-ground thicket-like arboreal understory, a three dimensional jungle-gym-like climbing apparatus, constructed from an interlocking network of small diameter plastic pipes, was assembled for each enclosure. The pipe diameter was small enough to effect a spring-like reaction under a jumping animal. Each jungle-gym measured approximately 2-4x3-0x2-l m. The multi-dimensional climbing network provided simultaneous access to the nestbox and 110 resting and feeding perches. To avoid risk of contamination by feces and urine, feeding, areas were raised and placed so that the bowls were never directly beneath perches and the climbing frame. The internal cage features were dry cleaned so as to preserve all olfactory markings. Food and Water. The animals were fed twice a day between 0900-1000 and again between 1500-1600 hours. The food was offered in heavy ceramic dishes 17 cm in diameter and 5-5 cm deep. Tap water was provided ad libitum, in 12 cm diameter bowls. Young Callimico are completely self-feeding by 12 weeks of age and between 12-18 weeks of age they are offered 50- 75% of the adult ration. Individual differences determined the exact amount fed to juveniles, but most received a complete adult ration between 28-52 weeks of age. When four or more individuals comprised the nuclear family group two food bowls were provided to lessen the stress of competition for preferred food items. Infants and juveniles commonly and normally begged or stole food from parents and older siblings, and adults sometimes stole food from juveniles. Daily Routine. Callimico thrived on a strict routine and were buffered against unanticipated environmental stresses, such as sudden and loud noises. Noise from above was especially stressful and to mask outside noise and Ill activity, a radio, tuned to a 'soft rock' station, played continuously with the volume increased during the day and decreased at night. Contrary to the observations of Lorenz (1972), it was found that Callimico thrive in close proximity to conspecifics. Auditory contact and some olfactory and visual contact did not appear to negatively affect their health and reproductive capability, although prolonged visual contact caused excessive pilo-displays (locomoting or standing with arched back, stiffly extended limbs, and erect pelage) and other signals of disturbance. Any alteration in the daily routine of the Callimico colony resulted in minor gastro-intestinal disturbances, and frequent change had serious negative effects on health and reproduction. The curatorial and veterinary staff, and other support personnel entered the colony only when necessary. Although a zoo's primary responsibility is displaying exotic species to the public, the Callimico colony at Brookfield Zoo was not on exhibit during this study. As part of their regular animal management duties, staff assigned to the Callimico colony conducted at least two one-hour sessions of systematic behavioral observations each day. These sessions provided an invaluable opportunity 112 to monitor the behavior and physical condition of the animals, and collect other useful data. Each session was scheduled to occur after the AM feeding but before the PM feeding. This time frame was utilized so as not to reflect higher than normal behavioral frequencies that sometimes occurred just after feeding. Each Callimico group was observed at least one hour per week. To insure that data collection were free of observer-subject interaction bias, caretakers minimized interacting with the Callimico. The protocol during each close-proximity encounter, such as daily enclosure maintenance and feeding, was not to make visual contact or in any way associate with Callimico individuals and/or groups. Sampling Methodology and Techniques I developed a behavioral ethogram that objectively characterized the behavior of each individual in the social group. Each behavior was designated as a discrete action, defined either by its morphology (part of the body involved), or inferred function. The behaviors documented during each observation period included: — Approach and Sit-by: An individual approaches and sits by (close physical proximity, ^5.0 cm) another group 113 member. Solicit Groom: An individual approaches and crouches or reclines in front of a potential groomer. Allogroom: An individual manually parts and picks at the pelage or hairless area of another group member. Autogroom: An individual manually parts and picks at its own pelage or picks at hairless areas of its face, ventrum, or perineum (not scratching). Pilo/Display: Locomoting or standing with arched back, stiffly extended limbs, and erect pelage. Hop Over: One individual hops over another individual once or multiple times during the duration of a pilo/display (a solicitation behavior used to motivate another individual to pilo/display). Tail Over: An individual positions its tail across the dorsal aspect of another individual, usually at the cessation of a pilo/display. Ventral Tail: The tail is alternately extended in the sagittal plane beneath the body and coiled ventrally so as to sweep the anogenital and glandular fields. This behavior appears to distribute urine and glandular secretions used in olfactory communication (Carroll, 1985; Wojcik and Heltne, 1978) . Genital Mark: Rhythmic rubbing of the anogenital region on an environmental feature while in a squatting position 114 (Carroll, 1985). Active Share: An individual proffers solid food to another and does not resist the recipient taking it. Passive Share: An individual allows another to take food without proffering it but without resisting the recipient taking it. Reluctant Share: An individual resists another from taking a food item in its possession. Long Call: A monosyllabic vocalization, generally utilized to maintain contact with other individuals over distances exceeding 20 meters (Masataka, 1982). Carrying Time: Infant is carried by its mother or climbs onto and is carried by another group member. Approximate Nursing Time: Infant seen clinging to superior ventral aspect of the maternal female with its head in a position to nurse. Pilo/Solicit Display: Female standing (with arched back, stiffly extended limbs, and erect pelage) in front of or to the side of the male and staring directly at him. Arm Over: Female sitting in physical contact longitudinally to the male with her head facing his rump and her arm thrown over his dorsum in an attempt to pull him into a ventral/dorsal mating position. Independent Locomotion: Infant supports its own weight on substrate (not after falling). 115 — Play: Chasing or wrestling involving rotational components (Wilson & Kleiman, 1974). All behaviors by members of a social group were sampled continuously over one hour intervals allowing collection of a wide range of data for later analyses. Noninteraction between observers and subjects insured there were no interruptions during data collection. All observation records include 'header and footer information', consisting of group identifier, date, start and end time of observation period, observer's identification, identity of each animal; and a separate section for ad libitum observations (Appendix A) . Development stages of maturing animals have not been defined the same by all investigators (Walters, 1987). In this dissertation, I define Callimico infancy as the period between birth and locomotor independence (12-17 weeks postpartum). I divide adolescence into juvenile and subadult phases. Juvenile is the period between locomotor independence of ego and the birth of ego's second sibling, usually about one year following birth of the first offspring (ego). By this time, the first-born has almost reached adult mass. Subadult is defined as the period between birth of ego's second sibling and ego's dispersal from the natal group, usually about three months following 116 birth of the 2nd sibling. Data Analysis and Presentation Data were separated into five categories for analysis. Category 1 is reported as frequency grand totals of each behavior by each individual. Grand totals provide an overall picture of recorded social interactions in each nuclear family group. These data are used for comparative analysis. Four additional categories are subsets of the grand totals. Category 2 includes all behaviors where parents and offspring interact. These data provide a thorough record of offspring socialization. Category 3 includes all solitary behaviors. Category 4 is all adult social interactions. The basic Callimico social group was a mated pair, therefore behaviors are classified by sex. These data detail the level of social interaction that characterizes Callimico. Category 5 is parent/infant social interactions categorized by sex. These interactive data record frequency with which all & and 9 offspring interacted with their parents. Category 5 provides data to determine if sex influences which parent socializes most with a particular offspring. Initial analyses include three dimensional cross tabulations of all interactive behaviors between parents and 117 offspring. All statistical analyses were completed using Quattro Pro for Windows® and QBASIC®. Frequencies examined include all behaviors by parents and offspring directed to all possible age-sex recipients in the group. Frequencies represent total behavioral occurrences during the study period. Since observation times of all offspring were equivalent and completed during the same daily time period, behavior frequencies may be further analyzed. Growth rates for Callimico were estimated using two techniques. As early growth in mammals is generally linear (Case, 1978; Zullinger et al., 1984), Callimico growth during the first 150 days postpartum is calculated as the arithmetic mean increase in mass {(Mass 150 days - Birth Mass)-^150)}. Growth was also estimated by the growth rate constant K calculated from the sigmoidal Gompertz equation (Zullinger et al., 1984). This estimate of growth has units of day"1 and estimates the rate of attaining adult mass. Comparisons of growth are not direct among Callithrix jacchus, Saguinus oedipus oedipus, Leontopithecus rosalia, and Callimico because adult masses differ between the callitrichids and Callimico. Early growth rates and the rate of attaining adult mass change predictably with the adult mass of a species. Larger mammals exhibit faster early growth and slower attainment of adult mass compared to 118 smaller species. This effect of adult mass must be considered when making interspecific comparisons. The effect of adult mass on early growth was estimated by Case (1978) for 11 anthropoid species: log GR = -0.65 + 0.35 log A where GR = early growth during the linear phase, and A = adult mass. The effect of adult mass on the rate of attaining adult mass (K) was estimated by Derrickson (1986) for 22 primate species: log K = -0.570 - 0.532 log A These equations were used to calculate predicted rates of early growth and predicted rates of attaining adult mass in Callimico and the three callitrichid species considered here (Beck et al., unpublished). Sex differences in attainment of behavior landmarks in Callimico infants were determined using binomial and two- tailed median tests. The binomial test was used because the samples were classified into exactly two categories, i.e., differences in ages of attainment of behavior landmarks between ¥ and cf infants. The median test was used because there were a few extreme values in each sample not representative of the majority of values in the distribution. 119 Analyses of interaction frequencies between parents and offspring utilized MONTE CARLO, a randomization statistic written by Dr. Paul Sciulli, Department of Anthropology, The Ohio State University, Columbus, Ohio. This statistic was used to examine frequency differences between single sets of interactions between fathers or mothers and offspring. All tests used data grand totals from 13 offspring (n=13) or data weekly totals from seven infant dependence cycles, 12- 17 weeks long (n=12-17). MONTE CARLO computed the means of the two samples and observed difference of the means between the two samples. It then pooled the two samples and 999 times randomly selected a pair of numbers and compared the difference between each frequency count to the observed difference of the means. Last, it calculated the number of comparisons > or < than the observed difference of the means. From these computations, the statistical significance of the difference between the paired sample was calculated by dividing the number of random comparisons > the observed difference of the means into the random comparison total (999). A primary consideration for usage of MONTE CARLO is that the accuracy of its results are not dependent on satisfying a set of assumptions (Gravetter & Wallnau, 1988). The level of statistical significance for each test is set at p<.05. Biological significance is also 120 proposed for directed interaction frequencies between parents and offspring. This term suggests that parent- offspring behavioral association preferences have been selected for to insure early reproductive success in young adult Callimico. The numbers displayed in each behavioral interaction sequence are absolutes, the grand totals of each interaction. The data presented in the tables show the behavioral interaction sequences displayed as proportions. Some results are graphically presented. These include and behavior rate frequencies and occurrence percentages. Conclusions Management of the Brookfield Zoo Callimico colony was unique. Callimico are rare in captivity and endangered in the wild. These specimens were taken directly from the wild. Therefore, special husbandry techniques were used. Systematic collection of social behavior data was initiated to maintain health in the Brookfield population. But there is little published information regarding intragroup social behaviors in Callimico. Thus, the ethological nature of these data is significant. Its analysis provide an integral view of the species' social behaviors and evolved survival skills. CHAPTER V ATTAINMENT OF BODY WEIGHT AND BEHAVIOR IN MATURING CALLIMICO Introduction Hershkovitz (1977) described Callimico as enigmatic because they are small, sexually monomorphic, and usually give birth to one infant. The equally small, monomorphic callitrichids typically give birth to twins, while the larger, dimorphic cebids give birth to singles. Eisenberg (1977) and Leutenegger (1980) proposed that small body size in callitrichids created obstetrical limitations on neonatal size and thus increased the selection for twinning. Callimico in captivity infrequently give birth to twins and have never been observed to care for both infants (Altmann et al., 1988). A litter size of one appears to be an established aspect of Callimico life history. However, single births appear to be less advantageous than giving birth to twins. Beck et al. (1982) and Carroll (1982) suggest that Callimico may become sexually mature earlier than callitrichids. Age at sexual maturity, like body size and 121 122 litter size, is an important component of species life history (Bekoff et al., 1984; Bekoff & Byers, 1985; Eisenberg, 1981; Millar & Zammuto, 1983). Rate of behavioral development to maturation is also an important aspect of species life history. For example, Tardif et al. (1986) report that captive common marmoset (Callithrix jacchus) infants locomote independently earlier than do cotton-topped tamarins (Saguinus oedipus). They suggest this difference is due to species differences in resource acquisition in the wild. This report focuses on rates of physical growth and behavior development of Callimico born at Brookfield Zoo. These findings are compared with infant development cycles of similar-sized but twin-producing callitrichids. The data concerning body size, growth rates, age at sexual maturity, behavioral development, and social behavior suggest that a litter size of one is a successful reproductive strategy for Callimico. Data on attainment of body weight and behavior in Callimico were developed by Dr. Ben Beck, The National Zoo, Washington, D.C. This manuscript (Beck et al. unpublished), co-authored by me, shows accelerated early growth and attainment of adult mass but delayed behavioral maturation in Callimico, when compared to three callitrichid species 123 (Callithrix jacchus, Saguinus oedipus, and Leontopithecus rosalia). Data examined in this dissertation document that Callimico exhibits a brief adolescent life cycle that results in an abbreviated period of learned infant care- giving experience (ICE) by older siblings. These data fit well with early attainment of adult mass and dispersal from the natal group by Callimico. This strategy effects early reproductive success and may justify single births in Callimico, opposed to twinning as in callitrichids. Methods The Brookfield Callimico colony has been prominent in establishing a self-sustaining international captive population (Rettberg, 1986; Warneke, 1992). Data used in this study to determine acquisition of body weight and behavior were collected during a period when there were over 40 births. Body Weight. The Callimico colony at Brookfield was a nonintervention setting. Therefore rearing of newborns by humans was discouraged. Animal weights were obtained opportunistically during management activities. Reported weights of Callimico (Carroll, 1982; Lorenz & Heinemann, 1967) were included to estimate growth. These additional data constitute approximately 30% of the set. 124 Behavior. The ages of infants in days of first occurrence of each developmental behavior listed below were designated as a behavior landmark. A definition of each behavior appears in Chapter IV, Materials and Methods, in the section subtitled, Sampling Methodology and Techniques. 1. Solicit Groom 2. Allogroom 3. Autogroom 4. Play with Parent 5. Play with Sibling 6. Pilo/Display 7. Ventral Tail 8. Genital Mark 9. Active Food Share by Parent 10. Passive Food Share by Parent 11. Passive Food Share by Sibling 12. Carry by Father 13. Carry by Sibling 14. Independent Locomotion Each infant was not observed each day. Comparison of first occurrences of developmental landmarks are comparable because all infants were sampled for equal times at equivalent ages; each infant was observed at least one hour per week for the first six months of life. As a result, 125 average age for attainment of each landmark is slightly overestimated. Still, age at attainment of behavioral landmarks are similar to those reported in other Callimico colonies (Arentson, 1977; Carroll, 1982; Heinemann, 1970; Heltne et al., 1973; Pook, 1978). When observations were infrequent, values greater than two standard deviations above the mean were eliminated. Observations during periods of social disruption (e.g., removal of an individual for veterinary treatment) were also eliminated. Data collected on infants who died or were removed, even when all landmarks had not been attained, were retained. Thus, sample sizes differ. At minimum, data from 13, and at maximum 40 infants were used to determine age of attainment of behavioral landmarks. Comparative Analysis. Reported weights for callitrichids were compared to Callimico body weights. Average weights of healthy animals of known-age were used to establish estimates at different ages. Mean species weights at any particular age are based on samples of one to 50. Growth of Callimico was compared to Callithrix jacchus (Abbott & Hearn, 1978; Beck, pers. obs.; Cooper in Hershkovitz, 1977; Epple, 1970; Hampton et al., 1971; Pook, 1976; Tanioka & Izawa, 1981; Winter & Rothe, 1977, 1978), Saguinus oedipus oedipus (Cooper in Hershkovitz, 1977; 126 Hampton & Hampton, 1967; Hampton et al., 1971; Kaumanns et al., 1986; Kirkwood, 1983; Pook, 1976; Wolfe et al., 1975), and Leontopithecus rosalia rosalia (Altmann-Schonberner in Hershkovitz, 1977; Beck, pers. obs.; Benirschke & Richart, 1963; Coimbra-Filho in Hershkovitz, 1977; Cooper in Hershkovitz, 1977; Dietz et al., 1994; Epple, 1970; Hoage, 1982; Napier & Napier, 1967). BaauJ-tg Body Weight. Callimico are sexually monomorphic in body weight. Average birth weight for six term birth d'd' at Brookfield was 49.2 g, that of six 9? was 51.6 g. Average weight of 14 adult d'd' (>730 days of age) was 560.3 g and 15 adult 9 9 was 532.2 g. Development of body mass over two years indicates that Callimico gain an average of 1.87 grams/day during the first 150 days postpartum, compared to 0.88 grams/day in C. jacchus, 1.31 grams/day in S. oedipus, and 1.65 grams/day in L. rosalia. No difference was seen in growth patterns of d'd1 and 99. Using growth parameters estimated with a Gompertz equation, ninety-five percent of adult mass was estimated to be attained at 409 days of age in Callimico, 489 days in C. jacchus, 471 days in S. oedipus, and 457 days in L. rosalia (Beck et al., unpublished). 127 Behavior. Average age of attainment of each of the 14 behavioral landmarks is displayed in Table 1. Females reach 10 of 14 landmarks earlier than do d'd', but these differences are not significant (Binomial Test, p>.05). Differences are statistically significant for four landmarks when analyzed individually using two-tailed median tests, Independent Locomotion, x2=7.90, pc.Ol; Passive Food Share by Sibling, xz=5.56, p<.02; Autogroom, x2=6.31, p<.02; Genital Mark, x2=4.17, p<.05. Comparative Analysis. Callimico exhibited the fastest rate of attaining adult mass, and achieved 95% of its adult mass 48-80 days earlier than the three callitrichids. Both Callimico and L. rosalia attained adult mass (0.0092 and 0.0085) at a rate similar to that predicted for a primate of their adult body mass (0.0091 and 0.0085). Callithrix jacchus and S. oedipus grew considerably more slowly (0.007 6 and 0.0081) than predicted (0.0124 and 0.0102). Early growth patterns showed similar results, with Callimico growing most rapidly (1.87 g/day) and C. jacchus growing least rapidly (0.88 g/day). Both estimates of growth show that Callimico grows more quickly than callitrichids (Beck et al., unpublished). 128 Table 1. Average Age in Days of Attainment of Behavioral Developmental Landmarks in Captive Callimico. Landmark Grand Mean n Male n Female n (Mean) (Mean) Carry by 27.2 40 27.2 20 27.2 20 Father Carry by 34.4 23 36.9 13 31.1 10 Sibling Independent 40.0 39 42.7 21 36.8 18 Locomotion Passive 54.0 31 58.9 16 48.7 15 share by Parents Play with 68.3 20 66.6 14 72.0 6 Sibling Active Share 71.4 13 75.0 4 69.8 9 by Parents Passive 75.3 22 81.6 14 64.1 8 Share by Sibling Autogroom 88.2 27 109.5 13 68.4 14 Solicit 98.3 36 106.6 18 89.9 18 Groom Threat 100.2 23 87.3 10 110.2 13 Attack Allogroom 103.1 33 112.7 15 95.2 18 Play with 124.3 19 120.8 11 129.1 8 Parents Ventral Tail 126 31 127.9 15 124.2 16 Genital Mark 130.9 29 148.6 14 113.8 hu 129 Discussion Body Mass. Growth of Callimico in this study differs little from summaries by Hershkovitz (1977). However, the current sample is larger than Hershkovitz and yielded smaller neonates and heavier adults. Altmann et al. (1988) reported an average birth weight of 55.5 g for nine Brookfield newborns. Carroll (1982) reported an average birth weight of 49.0 g for three Callimico newborns at the Jersey Preservation Wildlife Trust. The average weight of six Jersey Trust adults was 581.5 g. Except for C. jacchus, rates of attaining adult mass were similar to those previously reported by Zullinger et al. (1984). The slower growth rate of C. jacchus in this study may be due to the larger data set, use of growth data from more than one colony, and inclusion of more sets of triplets (Tardif, pers. comm., reports that triplets grow more slowly than twins, but litter sizes of weighed infants are rarely specified in the sources). Callimico obtain adult mass at an earlier age than do the three callitrichid species. They appear to reach sexual maturity more rapidly. For ??, sexual maturity is estimated as average age at which captive ??, when paired with unrelated fertile d'd', will conceive. For d'd', sexual maturity is the average age at which captive d'd1 will 130 inseminate unrelated fertile ??. Based on these criteria, Callimico ?? are sexually mature at 12 months, and d'd1 at 14 months of age (Beck et al., 1982). Age of sexual maturity for ? and cf C. jacchus is 18-24 months (Abbott & Hearn, 1978; Hearn, 1982); 15-24 months for S. oedipus (Tardif, 1984; Hershkovitz, 1977); and 16-20 months for L. rosalia (Kleiman, 1981; Kleiman & Jones, 1977). Behavior. The Callimico schedule of developmental landmarks cannot be precisely compared to callitrichids because of different observation methods. Despite reaching sexual maturity earlier than the callitrichids, Callimico achieves behavioral landmarks later. Kleiman (1983) determined that L. rosalia infants first climbed onto and were carried by fathers or older siblings at an average of 8 days of age. Box (1977) reported that C. jacchus infants are carried by fathers during the first week of life and by older siblings in the first or second week postpartum. The comparable figures for Callimico are 27 days for fathers and 34 days for older siblings. L. rosalia infants first locomote independently at 21 days of age (Hoage, 1982; Kleiman, 1983) . S. oedipus infants first locomote independently at 30 days of age (Cleveland & Snowdon, 1984) and C. jacchus infants in the third week (Box, 1977) . The average age of first 131 independent locomotion for Callimico infants is 40 days postpartum. L. rosalia infants first take food from their parents or older siblings at six to eight weeks following birth (Kleiman, 1983; Hoage, 1982), whereas Callimico infants first take food from family members at 54 to 75 days of age. S. oedipus infants first play socially at an average of 33 days (Cleveland & Snowdon, 1984), while Callimico infants are found to first play socially at an average of 68 days. The earliest age of circumgenital marking is 11 weeks postpartum in L. rosalia (Kleiman, 1983), anogenital marking in S. oedipus occurs at 63 days (Cleveland & Snowdon, 1984), and "scent marking" in C. jacchus occurs at 30 days (Box, 1975). Average age of first ventral tail in Callimico is 126 days and first genital mark is 131 days. Hoage (1982), citing other examples of ages of developmental behavior landmarks, supports the conclusion that Callimico reaches these milestones later than callitrichids. This would not be predicted for Callimico given its accelerated growth and early attainment of adult mass, and early realization of sexual maturity. This contradiction is resolved if Callimico parents teach offspring adult behaviors, and offspring learn at an accelerated rate. This appears to be true in Callimico, 132 where both parents socialize adolescent offspring. Callimico is unique in that fathers socialize with daughters more than do mothers and mothers with sons more than do fathers (Chapter VI). Functional Significance of Rapid.Physical, and Delayed Behavioral Maturation Callimico, Callithrix, Leontopithecus, and Saguinus all tend toward monogamy, although groups with more than one reproductive cT or ? are sometimes observed ( Baker, 1991; Carroll, 1988; Dawson, 1978; Dietz & Kleiman, 1986; Garber et al., 1984; Neyman, 1977; Rothe & Darms, 1993; Sussman & Garber, 1987; Sussman & Kinzey, 1984; Terborgh & Goldizen, 1985; Wright, 1990). In these genera, helping behavior, specifically carrying newborns and sharing food with them, is typical of fathers, older siblings, and nonreproductive adults of the group. The constellation of monogamy and helping behavior is accompanied by delayed reproduction of offspring, who presumably increase their inclusive fitness by enhancing reproductive success of their relatives (Baker, 1991; Garber et al., 1984; Goldizen, 1990; Ingram, 1977; Kleiman, 1977; Leutenegger, 1980; Wilson, 1975). Older siblings contribute by transporting one or two twins that at birth weigh 17% to 24% of the mother's weight, and by 133 providing food to the growing infants. The contribution of older siblings to infant care in Callimico may be less crucial (Kleiman, 1985). There is only one infant and its initial mass is only 9.2% of adult weight. With one sibling and the father, a Callimico infant has two additional care givers. To enjoy a 2:1 nonmaternal care-giver ratio (assuming that infant mortality is equal to that of Callimico), a pair of callitrichid twins would require three older siblings and a father. There may be a greater net genetic advantage in early attainment of adult mass, sexual maturation, dispersal, and reproduction in Callimico. The present data demonstrate early attainment of adult mass and sexual maturation in captive Callimico compared to several callitrichid species. Field studies should confirm early dispersal and reproduction. Curiously, although the growth rate for Callimico is more rapid than in the callitrichids, behavior landmarks are attained more slowly when compared to the callitrichids. Apparently, Callimico remains an infant longer, but becomes an adult at an earlier age than the callitrichids. These results indicate that adolescence (juvenile and subadult), that period between dependency and sexual maturity, is shorter in Callimico. This is the specific life stage when nonparents provide infant care. Its 134 brevity in Callimico is consistent with a reduced need for nonparental infant care. Apparently, both Callimico and the callitrichids require training and experience in the care of younger siblings if they themselves are to become fully competent parents (Beck et al., 1982; Kleiman, 1977; Cleveland & Snowdon, 1984; Tardif et al., 1984). From this conclusion, it is reasonable to predict that Callimico would not disperse before the birth and developmental cycle of at least one subsequent sibling. The reproductive experience of parents, the number of older siblings present, resource availability, and a variety of other environmental factors can influence infant growth and development. However, ecological variables are superimposed on genetically determined development (Bekoff & Byers, 1985; Caro & Bateson, 1986). There seems no reason to suppose that ecological factors function differently in the development of individuals of these four species. All data have been gathered in similarly managed captive colonies. A proximate cause for the more rapid growth of Callimico could be greater availability of subsistence resources for a single individual compared to twins. But this effect would be dampened in captivity where food is virtually unlimited and there is a reduction of energetic 135 demands on lactating ??. While captive callitrichids weigh more than wild conspecifics (e.g., Savage et al., 1990 for S. oedipus; Dietz et al., 1994 for L. rosalia), it could be expected that the interspecific differences reported here exist between free ranging populations of the same four species. They might be even more exaggerated since subsistence sources in the wild are limited and there are greater demands on energy expenditure. This examination concludes that the single Callimico infant is programmed to attain adult mass and sexual maturity earlier than callitrichids, and that this represents a derived alternative to twinning as a successful reproductive strategy for a very small and geographically isolated primate. Conclusions There apparently are several contradictory forces that dictate life history parameters of Callimico. (1) Callimico shows faster early growth, attains adult weight and reaches sexual maturity earlier than callitrichids. (2) Callimico attains developmental behavioral landmarks later than do callitrichids. (3) Callimico appears to have a shorter period between infant dependency and adulthood (a shorter 'adolescence' than callitrichids). (4) Longer adolescence 136 in callitrichids may provide a larger pool of helpers to carry and provide food to younger dependent twin siblings. There may be less need for older siblings as infant care helpers in Callimico, where there is only one dependent infant. Given that there are competing evolutionary forces at work in Callimico that govern the reproductive success of the species, what bearing do these tactics have on the actions of young adults? Relatively short-lived Callimico 9 9 seem to experience a never-ending, life-long succession of estrus/ovulation, pregnancy, birth, lactation, and infant care-giving behaviors. Because these are demanding costs and could affect the health and welfare of the individual, it is essential to species survival that 9 9 become reproductively active at an early age. Because young adult Callimico 99 have shown the ability to procreate at about 12 months of age (Lorenz, 1972), they may not undergo the prolonged or intense ICE that characterizes callitrichids. Nonetheless, this suite of behaviors is exceedingly important to successful reproductive behavior in primiparous parents. As will be shown Chapters VII and VIII, ICE, especially by d'd', is imperative to skillful first-time parenting. CHAPTER VI PARENTS AND INFANT CARE IN CALLIMICO introduction Intensive infant care-giving behavior is most prominently seen in small-bodied Neotropical primates. Leutenegger (1980) suggested that small body size led to monogamy which, in turn, generated twin births and a high mother/litter weight ratio. Energetic costs of a litter that may weigh 25% of maternal body weight likely led to infant care-giving behavior by fathers and nonreproductive others (Hershkovitz, 1977). In Chapter III it was shown that infant carrying by callitrichid parents and others is variable and group specific. Part of this variability appears to result from limitations imposed by the number of helpers in each group. The prohibitive costs of twinning and the need for helpers may have led to the later evolution of alternative reproductive systems which resulted in additional infant care-givers. Multiple field investigations document that strict monogamy is not the sole reproductive strategy of 137 138 callitrichid-like species. Suspected polygyny and/or polyandry have been reported for several species (Garber et al., 1984; Masataka, 1981a; Pook & Pook, 1981; Rylands, 1985; Terborgh & Goldizen, 1985). Alternative reproductive schemes shed light on the importance of infant care-giving behaviors by nonreproductive members of each social group. Unrelated adults of both sexes provide care-giving behaviors in the absence of older siblings. Whatever the reproductive pattern, it appears that high mother/litter weight ratios that result from twinning have led to helping behaviors by other social group members. Because Callimico does not deliver twins and the initial mass of a single infant is only about 9% of an adult's weight, the contribution of the father and older siblings to infant care is probably less critical than in callitrichids (Kleiman, 1985). To offset the apparent fitness disadvantage of birthing single infants compared to twinning in callitrichids, this study has shown that Callimico attains adult mass, reaches sexual maturity, and probably disperses approximately one year postpartum. This chapter examines parent-offspring interactions and their contribution to reproductive success in young adult Callimico. 139 Methods Data on infant care-giving behaviors by the 10 founding adults and several of their offspring are now analyzed and discussed. The focus is on interactive close proximity and contact behaviors shown by parents when a newborn or older offspring are present in the group. These actions have been defined as infant carry, solicit allogroom, allogroom, approach and sit-by, and hop-over, in addition to a group of food sharing behaviors. The term infant transport will also be used to describe the behavior infant carry. MONTE CARLO is used to test for significant differences resulting from parent-offspring interactions. Each test compares interaction frequencies between mothers and fathers, and 13 offspring (n=13). There were seven reproductively successful groups of Callimico during the data collection phase of this investigation. Multiple offspring were produced by the mated pairs in Groups 2, 3, 4, and 5, while Groups 1, 6, and 7 each produced one offspring. Individuals and groups are listed and identified in Table 2. Once acknowledged by group number and given name, each individual will afterward be referred to by name. Some confusion may occur concerning the founding (Will), as he fathered the offspring in both Groups 1 and 2. 140 TABLE 2. Individual Members of each Callimico Group at Brookfield Zoo. Group Adult Adult Infant Infant Infant Infant Number cP 9 1 2 3 4 1 Will Tango Gabriella 9 born 7/19/79 2 Will Eunice Judy Vicki 9 born 9 born 2/20/78 8/11/78 3 Jos6 Tina Lew Kris Minnie Jiminez cP born 9 born 9 born cP born 3/6/78 8/15/78 1/23/79 7/6/79 4 Rob Marie Antonio Juan cP born cP born 1/9/78 7/23/78 5 Scruffy Betty Prima Ken 9 born cP born 12/20/78 6/5/78 6 Antonio Prima ? 9 born 7/23/79 7 Pep6 Judy Bea 9 born 7/6/79 141 Will first fathered two infants in Group 2. Then, following an illness, he was paired with another founding ? and fathered an infant in Group 1. The founding population includes all adult cf The Role of Call iminr, Mothers and Fathers in Infant Care Infant carry is a basic helping behavior and is foundational to other infant care-giving behaviors. Infant care and carrying are individually variable in captive Callimico. This could be due to individual differences in motivation, or could be an artifact of lack of infant care experience (ICE) as a juvenile and/or subadult. Previous reports agree that mothers exclusively carry newborns the first two to three weeks (Beck et al., 1982; Carroll, 1982; Heinemann, 1970; Heltne et al., 1973). Fathers generally carry newborns more than mothers during weeks four to seven (Heinemann, 1970; Heltne et al., 1973). After week six, when infants increase their independence and exploration of 142 the environment, parents carry their offspring less (Heltne et al., 1973). Infant Carry by Parents. Attainment of locomotor independence varies in captive Callimico. Infants locomote independently for short periods as early as five weeks, although some infants are still carried at 16 weeks (Figure 1). While both mothers and fathers carry newborns, data on 13 infants show that mothers carry infants more than do fathers. Overall, between the two parents, mothers carry infants 75% of the time (Figure 2). Throughout the infant development cycle, for 8 of the 13 births at Brookfield, mothers carried their offspring more than 70% of the time (Table 3). This demonstrates a consistent intensive infant care commitment by Callimico mothers when compared to bi- parental infant care in callitrichids. Only during week six did fathers carry infants more than 50% of the time (Figure 3). Only once was an infant carried less than 49% of the time by its mother. The mother in Group 1 (Tango) carried her infant exclusively for its first three weeks of life. She then assumed a secondary role and the father did nearly all the carrying until the infant locomoted independently in week 14 (Figure 4). In contrast, in Group 5, the mother (Betty) carried her second infant 98.6% of the time. Only during weeks 5, 7, and 8-10, did the father even minimally 143 share infant carrying duties (Figure 5). Will, the original Group 2 and later Group 1 cf, carried his Group 1 newborn, Gabriella, 68.3% of the time. Will did not transport the newborn during its first three weeks of life (see Figure 4). Following week 4, he was responsible for the majority of infant carrying. Will's motivation and timing to assume primary responsibility for infant transportation may have been influenced by the end of Tango's postpartum estrus cycle and ensuing pregnancy. In contrast to Will's attentive infant carrying behavior, the Group 5 cf, Scruffy, only carried his two offspring 1.4% and 8.1% of the time, respectively (Figures 5, 6). There is no obvious explanation for these low carrying rates, or for the differences in carrying seen among cfcf. Lack of experience, leading to nonperformance of critical care behaviors, could account for Scruffy's aversion to transporting infants. His infrequent infant carrying behavior is likely part of a continuum from extreme activities to even more extreme disregard for the welfare of mothers and infants. Such an extreme may have been exemplified by another father at Brookfield. Antonio, an Fx cf from the Brookfield colony and Group 6 parent, never carried his first offspring (Table 3). This apparent anomaly in Antonio's behavior likely is traceable 144 Table 3. Percentage of time Adults in each Callimico Group at Brookfield Zoo carried Newborns. Group Number Birth Sequence % of Time Father % of Time Mother Infant Sex Carried Newborn Carried Newborn 1 birth 1 of 1, 9 68.3 31.7 2 birth 1 of 2, 9 43.6 56.4 2 birth 2 of 2, 9 28.0 72.0 3 birth 1 of 4, 38.3 61.7 3 birth 2 of 4, 9 23.7 76.3 3 birth 3 of 4, 9 51.4 48.6 3 birth 4 of 4, & 28.9 71.1 4 birth 1 of 2. c? 23.7 76.3 4 birth 2 of 2, 31.2 68.8 5 birth 1 of 2, 9 08.1 91.9 5 birth 2 of 2, d1 01.4 98.6 6 birth 1 of 1, 9 00.0 100.0 7 birth 1 of 1, 9 16.8 83.2 145 to his lack of ICE as a juvenile and subadult. The logic used to support this assumption is discussed in Chapter VIII. Because of differential parental roles with regard to the frequency of infant transport (see Figure 2), it might be expected that a significant difference exists between each parent's performance of this behavior. There were 13 infant dependence cycles/ the longest being 17 weeks (n=17). A comparison was made, by week, of each parent's carrying time. Mothers carried infants 441.03 observation hours, fathers did so 150.66 hours, p=.003. Further evidence that parents provide differential input toward socialization of immature Callimico is seen in parent-infant interactive behaviors. These behaviors, particularized by solicit allogroom; allogroom; approach and sit-by; hop-over; and active, passive, and reluctant food share, provide additional evidence regarding parental input to offspring socialization. Solicit Allogroom, and Allogroom by Parents and Offspring. Fathers solicited offspring to groom 679 times and mothers did so 528 times, p=.33. Still, offspring groomed fathers fewer times (872) than they groomed mothers (1063), p=.32. Although fathers solicited offspring more than mothers, the data grand totals show that offspring are 146 more attentive to their mothers. Offspring Callimico also show sex preferences in soliciting parents to groom and which parent groomed them. Offspring solicited fathers to groom 2379 and solicited mothers 1982 times, p=.34. Fathers groomed their offspring 1578 times, mothers groomed them 1133 times, p=.26. The data grand totals show that immature Callimico solicited fathers to groom more than mothers, and were groomed by fathers more than mothers. Approach and Sit-by by Parents and Offspring. Fathers approached and sat-by offspring 340 times, mothers did so 279 times, p=.48. In contrast, offspring approached and sat-by fathers and mothers 2353 and 3039 times, p=.23. The data grand totals show that fathers somewhat more than mothers approached and sat-by offspring, and offspring approached and sat-by mothers more than fathers. Hop-over by Parents and Offspring. Hop-over is usually seen during pilo/display behavior. The displaying animal appears to be soliciting another family member to engage in display. Adults focused their hop-overs on other adults 6822 times, and on offspring only 522 times. Because pilo/displays initiated by offspring (371) are less frequent than hop-overs directed toward adults (2153), hop-over is likely a form of play among offspring. 147 Offspring about equally directed hop-overs toward fathers (1070) and mothers (1083), p=.49. Parents also about equally directed hop-overs toward their offspring. Fathers and mothers hopped-over offspring 259 and 263 times, p= .49. Active Share by Parents and Offspring. Active sharing between parents and offspring was infrequent. Fathers actively shared food with offspring on 11 occasions, and mothers shared with offspring 10 times, p=.50. Offspring never actively shared with fathers and shared with mothers only 5 times, p=.24. Apparently fathers and mothers do not show sex bias when actively sharing food with offspring. Offspring rarely shared with parents but did so with mothers more than fathers. Passive Share by Parents and Offspring. Passive sharing between parents and offspring occurred at a higher frequency than active sharing. Offspring solicited passive shares from fathers 604 and mothers 885 times, p=.ll. Offspring received 507 shares from fathers and 757 shares from mothers, p=.07. These results show that offspring interact with mothers more than fathers. Fathers and mothers solicited passive shares from offspring 36 and 185 times, p=.009. In return, offspring passive shared with fathers 31 and mothers 174 times, p=.008. Not only did 148 mothers solicit passive shares from offspring more than did fathers, but offspring shared with mothers more than fathers. Reluctant Share by Parents and Offspring. Offspring solicited reluctant shares from fathers and mothers 130 and 218 times, p=.22. In return, fathers and mothers shared with offspring 16 and 23 times, p=.31. The data grand totals show that offspring solicited and received reluctant shares from mothers more than fathers. Fathers and mothers solicited reluctant shares from offspring 19 and 79 times, p=.04. In response, offspring shared with fathers 5 and mothers 47 times, p=.05. Mothers not only solicited reluctant shares from offspring more than did fathers, but offspring shared with mothers more than fathers. Data on 10 major behavioral categories with 19 specific sequences of performed interactive behaviors have been reported (Table 4). In 14 of 19 sequences, mothers interacted with offspring more than fathers. In five sequences from two major categories, infant carrying and food sharing, mothers interacted with offspring significantly more than did fathers. Only in the parent- offspring interactive behaviors; offspring solicit parents to groom (55%), adults groom offspring (58%), adults solicit offspring to groom (56%), and adults approach and sit-by 149 TABLE 4. Proportion of Occurrence Grand Totals of Studied Behaviors between Callimico Parents and Offspring. Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence Adult dtf Infant Carry Totals 1 1 255 l l Adult 9 9 Infant Carry Totals 1 All Offspring Solicit cT Parent to 1 .546 Groom All Offspring Solicit 9 Parent to I .454 Groom Adult tfV Groom all Offspring I .582 Adult 9 9 Groom all Offspring I .418 Adult c W Solicit Offspring to 1 1 .563 | Groom Adult 9 9 Solicit Offspring to Groom •437 1 All Offspring Groom cf Parent .451 H All Offspring Groom 9 Parent .549 U All Offspring Approach and Sit-by d" .436 Parent All Offspring Approach and Sit-by 9 .564 Parent Adult cW Approach and Sit-by .549 | Offspring Adult 9 9 Approach and Sit-by •4si Offspring H All Offspring Hop-over Parent 11 * 4 97 H All Offspring Hop-over 9 Parent 1 .503 | Adult cfcf Hop-over Offspring 1 .496 H Adult 9 9 Hop-over Offspring 1 . 504 | 1 150 Table 4 (continued) Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence H Adult d d Solicit Passive Share 1 -163 from Offspring H Adult 9 9 Solicit Passive Share I .837 from Offspring All Offspring 1 Passive Share with d I .151 I Parent All Offspring I Passive Share with 9 I .849 I Parent All Offspring Solicit Reluctant .374 Share from d Parent All Offspring Solicit Reluctant .626 Share from 9 Parent Adult d d Reluctant Share with .410 Offspring Adult 9 9 Reluctant Share with .590 Offspring All Offspring Active Share with d .00 Parent All Offspring Active Share with 9 1.00 Parent Adult d d Active Share with .524 Offspring Adult 9 9 Active Share with .476 Offspring All Offspring Solicit Passive Share .406 | from d Parent All Offspring Solicit Passive Share .594 I from 9 Parent Adult d d Passive Share with .4°! H Offspring Adult 9 9 Passive Share with . 5 " | Offspring Adult dcf Solicit Reluctant .194 H Share from Offspring Adult 9 9 Solicit Reluctant .806 Share from Offspring All Offspring Reluctant Share with .096 cf Parent All Offspring Reluctant Share with .904 I 9 Parent 151 offspring (55%), did fathers interact more with offspring than mothers. These results provide new information on the father's role and contradict the proposition that fathers provide for infant stability during weaning and development of locomotor independence in Callimico. It does appear that, when mothers become pregnant, fathers take a more active role as physical and social caretakers of offspring. These findings, by reflecting cebid-and cercopithecid- like (New and Old World monkeys) mother-infant offspring socialization patterns rather than those of the callitrichids, align Callimico with the former. The callitrichids employ at least part-time monogamy, and practice intensive father-infant care-giving (Box, 1975; Cebul & Epple, 1984; Christen, 1974; Dixson & Fleming, 1982; Epple, 1975b; Fragaszy et al., 1982; Garber, 1986; Goldizen, 1987b; Hershkovitz, 1977; Hoage, 1978; Ingram, 1977, 1978; Robinson et al., 1987; Rothe et al., 1993; Rylands, 1985; Soini, 1988; Tardif, et al., 1986; Terborgh & Goldizen, 1985; Vogt et al., 1978; Wright, 1984; Yamamoto, 1993). Callimico is also at least part-time monogamous and fathers practice intensive care-giving. However, this is quite variable because mothers physically sustain pre-weaned infants and equip them with the social skills needed to 152 insure future reproductive success. Sex and the Frequency of Parent-Infant Care-aivina. Callimico mothers interact more with infants than do fathers. This leads to an assumption that mothers are the principal socializers of young. Several questions remain: 1. Do the sex of the parent and offspring affect the frequency of selected parent-offspring interactive behaviors? 2. Are clear interaction preferences shown by same or opposite sex parents and offspring? 3. What evolutionary implications do such behavioral patterns have? Parent-offspring behaviors specific to sex of the parent and offspring being socialized are examined to determine the direction of parent-offspring interactions. These behaviors include allogroom; approach and sit-by; hop- over; and active, passive, and reluctant food share. MONTE CARLO is used to test for a significant difference in the number of interactions between fathers and offspring, and mothers and offspring. The number and sex of offspring are eight 9? and five cfcf (^=8, n2=5) . Infant Carry by Parents. Fathers carried daughters 96.8 hours and sons 53.9 hours, p=.39. Mothers carried 153 daughters 253.2 hours and sons 187.9 hours, p=.29. The data grand totals show that fathers and mothers carried daughters more than sons. However, fathers displayed a greater propensity to carry daughters. Solicit Allogroom and Allogroom by Parents and Offspring. Daughters and sons solicited fathers to groom 1095 and 1284 times, p=.19. The data grand totals show that sons solicited fathers more than did daughters. Daughters and sons solicited mothers to groom 832 and 1150 times, p=.10, showing that sons interacted with mothers more than did daughters. Fathers groomed daughters 593 and sons 985 times, p=.09, showing that fathers groomed sons more than daughters. Mothers groomed daughters 390 and sons 743 times, p=.05, showing that mothers were more attentive to sons than to daughters. Fathers solicited daughters to groom 396 and sons 283 times, p=.48. Mothers solicited daughters to groom 258 and sons 270 times, p=.27. The data grand totals show that fathers solicited daughters more than sons and mothers solicited sons more than daughters. Daughters and sons groomed fathers 490 and 382 times, p=.36. They groomed mothers 361 and 702 times, p=.05. While the data grand totals show that daughters groomed fathers more than did sons, sons groomed mothers significantly more than did 154 daughters. Approach and Sit-by by Parents and Offspring. Daughters and sons approached and sat-by fathers 1431 and 922 times, p=.48. They did so toward mothers 1550 and 1489 times, p=.18. The data grand totals show that daughters approached and sat-by fathers and mothers more than did sons. Fathers approached and sat-by daughters 283 and sons 57 times, p=.30. Mothers did so toward daughters 176 and sons 103 times, p=.47. The data grand totals show that both parents approached and sat-by daughters more than sons. Hop-over by Parents and Offspring. Daughters and sons directed "hop-over" toward fathers 611 and 459 times, p=.36. The data grand totals show that daughters hopped-over fathers more than mothers. Daughters and sons directed the behavior toward mothers 480 and 603 times, p=.08, showing that sons interacted with mothers more than did daughters. Fathers directed hop-overs toward daughters 147 and sons 112 times, p=.36. Mothers directed hop-overs toward daughters 137 and sons 126 times, p=.22. The data grand totals show that fathers and mothers performed "hop-over" more with daughters than with sons. Active Share by Parents and Offspring. Active sharing was infrequent in Callimico. Fathers actively shared with daughters only 5 and sons 6 times, p=.28. Similarly, 155 mothers actively shared with daughters 4 and sons 6 times, p=.28. Daughters and sons never actively shared with fathers, and daughters shared with mothers only 5 times, p=.35. Passive Share by Parents and Offspring. Daughters and sons solicited passive shares from fathers 253 and 351 times, p=.05. They did so from mothers 466 and 419 times, p=.16. While sons solicited passive shares from fathers more than did daughters, the data grand totals show that daughters solicited shares from mothers more than did sons. In response, fathers passive shared with daughters 211 and sons 296 times, p=.04. Mothers shared with daughters 416 and sons 341 times, p=.40. While fathers passive shared with sons more than daughters, the data grand totals show that mothers shared with daughters more than sons. Fathers solicited passive shares from daughters 14 and sons 22 times, p=.16. Mothers solicited shares from daughters 121 and sons 64 times, p=.41. The data grand totals show that fathers solicited shares from sons more than daughters and mothers solicited shares from daughters more than sons. Daughters and sons passive shared with fathers 13 and 18 times, p=.25. They did so with mothers 115 and 59 times, p=.41. The data grand totals show that sons passive shared with fathers slightly more than did 156 daughters and daughters shared with mothers more than did sons. Reluctant Share by Parents and Offspring. Daughters and sons solicited reluctant shares from fathers 43 and 87 times, p=.15. They solicited shares from mothers 93 and 125 times, p=.31. The data grand totals show that sons solicited reluctant shares from both parents more than did daughters. Fathers reluctant shared with daughters 4 and sons 12 times, p=.06. Mothers reluctant shared with daughters 13 and sons 10 times, p=.43. Fathers reluctant shared with sons more than daughters, and the data grand totals show that mothers shared slightly more with daughters than sons. Fathers solicited reluctant shares from daughters 10 and sons 9 times, p=.38. Mothers did so from daughters 46 and sons 33 times, p=.48. The data grand totals suggest that fathers showed no sex preference when soliciting offspring and mothers interacted with daughters slightly more than with sons. Daughters and sons reluctant shared with fathers 3 and 2 times, p=.38. They did so with mothers 34 and 13 times, p=.46. The data grand totals show that offspring shared about equally with fathers, and daughters interacted with mothers more than did sons. 157 Parent-offspring interactions are influenced by the sex of the actors (Table 5). Five parent-offspring socialization categories were examined: (1) infant carry, (2) offspring solicit and parents groom, (3) parents solicit and offspring groom, (4) offspring approach and sit-by parents and parents approach and sit-by offspring, and (5) offspring hop-over parents and parents hop-over offspring. Fathers initiated interactions with daughters (cf carry infant 9, cf solicit young 9 to groom, cf approach and sit-by young 9, and cf hop-over young 9) more than sons (cf groom young cf) . Mothers also initiated interactions with daughters (9 carry infant 9, 9 approach and sit-by young 9, and 9 hop-over young 9 ) more than sons (9 groom young cf and 9 solicit young cf to groom). Daughters and sons interacted more often with fathers and mothers, respectively. Daughters initiated interactions with fathers (young 9 groom cf, young 9 approach and sit-by cf, and young 9 hop-over cf) more than mothers (young 9 approach and sit- by 9 ) . Sons initiated interactions with mothers (young cf solicit 9 to groom, young cf groom 9, and young cf hop-over 9) more than fathers (young cf solicit cf to groom) . Five major categories of food sharing were examined: (1) offspring active share with parent and parent active share with offspring, (2) offspring solicit passive share from parent and parent share with offspring, (3) parent 158 solicit passive share from offspring and offspring passive share with parent, (4) offspring solicit reluctant share from parent and parent reluctant share with offspring, and (5) parent solicit reluctant share from offspring and offspring reluctant share with parent. Food sharing behaviors seem to be associated along same sex lines. Fathers initiated interactions more with sons in four food sharing categories (1,2,3,4), and with daughters in only one category (5). Mothers also distributed food stuffs along same sex lines as they initiated interactions more with daughters in four behavioral categories (2,3,4,5) and sons in one category (1). Offspring also shared food more with parents of the same sex. Daughters interacted with mothers more than fathers in four food sharing categories (1,2,3,4), and with fathers more in one category (5). Sons interacted with fathers more than mothers in three categories (2,3,4) and more with mothers in one category (5). The just discussed behavioral interactions that indicate a sexual preference bias between parents and offspring utilized 13 offspring birth and development cycles. Because there were eight 9 9 and five cr TABLE 5. Proportion of Occurrence Grand Totals in 10 Interactive Behavior Categories between Callimico Parents and Offspring by Sex of Actors. Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions and high interaction sequence ranking sex Fathers Carry daughters .642 (fathers) Fathers Carry sons .358 Mothers Carry daughters .574 (mothers) Mothers Carry sons .426 Daughters Solicit fathers to .46 groom Sons Solicit fathers to .54 (sons) groom Daughters Solicit mothers to .42 groom Sons Solicit mothers to .58 (daughters) groom Fathers Groom daughters .376 Fathers Groom sons .624 (fathers) Mothers Groom daughters .344 Mothers Groom sons .656 (mothers) Fathers Solicit daughters to .583 (fathers) groom Fathers Solicit sons to groom .417 Mothers Solicit daughters to .489 groom Mothers Solicit sons to groom .511 (mothers) Daughters Groom fathers .562 (daughters) Sons Groom fathers .438 Daughters Groom mothers .34 Sons Groom mothers .66 (sons) Daughters Approach/sit-by father .608 (daughters) Sons Approach/sit-by father .392 Daughters Approach/sit-by mother .51 [daughters) Sons Approach/sit-by mother .49 Fathers Approach/sit-by .832 (fathers) daughters Fathers Approach/sit-by sons .168 Mothers Approach/sit-by .631 (mothers) daughters Mothers Approach/sit-by sons .369 160 Table 5 (continued) Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions and high interaction sequence ranking sex Daughters Hop-over fathers .571 (daughters) Sons Hop-over fathers .429 Daughters Hop-over mothers .443 Sons Hop-over mothers .557 (sons) Fathers Hop-over daughters .568 (fathers Fathers Hop-over sons .432 Mothers Hop-over daughters .521 (mothers) Mothers Hop-over sons .479 Fathers Active share with .455 daughters Fathers Active share with sons .545 (fathers) Mothers Active share with .4 daughters Mothers Active share with sons .6 (mothers) Daughters Active share with No incidence of fathers behavior Sons Active share with No incidence of fathers behavior Daughters Active share with 1.0 (daughters) mothers Sons Active share with .00 mothers Daughters Solicit passive share .419 from fathers Sons Solicit passive share .581 (sons) from fathers Daughters Solicit passive share .527 (daughters) from mothers Sons Solicit passive share .473 from mothers Fathers Passive share with .416 daughters Fathers Passive share with .584 (fathers) sons Mothers Passive share with .55 (mothers) daughters Mothers Passive share with .45 sons 161 Table 5 (continued) Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions and high interaction sequence ranking sex Fathers Solicit passive share .389 from daughters Fathers Solicit passive share .611 (fathers) from sons Mothers Solicit passive share .654 (mothers) from daughters Mothers Solicit passive share .346 from sons Daughters Passive share with .419 fathers Sons Passive share with .581 (sons) fathers Daughters Passive share with .661 (daughters) mothers Sons Passive share with .339 mothers Daughters Solicit reluctant .331 share from fathers Sons Solicit reluctant .669 (Sons) share from fathers Daughters Solicit reluctant .427 share from mothers Sons Solicit reluctant .573 (Sons) share from mothers Fathers Reluctant share with .25 daughters Fathers Reluctant share with .75 (fathers) sons Mothers Reluctant share with .565 (mothers) daughters Mothers Reluctant share with .435 sons 162 Table 5 (continued) Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions and high interaction sequence ranking sex Fathers Solicit reluctant .526 (fathers) share from daughters Fathers Solicit reluctant .474 share from sons Mothers Solicit reluctant .582 (mothers) share from daughters Mothers Solicit reluctant .418 share from sons Daughters Reluctant share with .60 (daughters) fathers Sons Reluctant share with .40 fathers Daughters Reluctant share with .723 (daughters) mothers Sons Reluctant share with .277 mothers daughters than sons, and daughters socialized more with parents than did sons. In single birth groups (1, 6, and 7) three 9? were born, but in multiple birth groups (2-5) there was an equal number of 9 and d' offspring, five each. Succeeding births by group were, Group 2 9-*9, Group 3 d,->9-*9-*cP, Group 4 and Group 5 9-+cf. The equal sex ratio between parents and offspring in these four groups allowed for equal opportunities to interact preferentially with one sex during social encounters. Comparison of such sex differentials in behavioral preferences during parent- offspring interactions in the groups with equal numbers of 9 and cf offspring are different from those of sex 163 preference interaction grand totals. One behavior sequence found in the "equal sex of offspring groups" alters the parent-offspring sex preference grand totals suggesting that mothers associate with sons more than daughters (boldface type). Fathers in the "equal sex of offspring groups" initiated interactions with daughters more than sons (cf carry infant 9, solicit young 9 to groom, There is only one difference in food sharing behaviors initiated by parents in the equal sex multiple offspring groups. Fathers solicited more reluctant shares from daughters than sons. Still, this did not change the sex preference food sharing grand totals between parents and all offspring. Mothers reluctant shared with daughters more than sons. That fathers solicited more reluctant shares from daughters does not alter the general pattern that food sharing between parents and offspring are commonly between the same sex. 164 The only difference in offspring initiated social interactions in the equal sex multiple offspring groups is that daughters approached and sat-by fathers more than mothers. Two changes occurred in food sharing behaviors initiated by offspring. Daughters solicited passive shares from fathers more than from mothers, although this did not alter the all offspring sex preference food sharing grand totals. Second, sons solicited passive shares from mothers more than fathers, thus mothers passive shared with sons more than daughters. In response to the three questions that opened this section concerning Callimico parent-offspring care, the sex of the parents and offspring appears to affect the performance frequency of parent-offspring interactions. Analysis of a suite of socialization behaviors indicates that, in both parents and all offspring grand totals and parents and equal sex number offspring groups, fathers initiate more social interactions with daughters than with sons. Mothers, in the sex preference grand totals, also initiate more social interactions with daughters than with sons. This is not the case in the "equal sex of offspring groups," where mothers initiate more interactions with sons. For offspring-initiated interactions in the all offspring grand totals and "equal sex of offspring groups," 165 daughters initiate more interactions with fathers than with mothers, while sons initiate more interactions with mothers than with fathers. These parent-offspring sex preferences are less obvious in the food sharing behaviors, which seem to arrange themselves according to same sex interactions (tfcf associate with For a species that quickly matures and is capable of early reproductive behavior, a young Callimico ¥ that socializes more with her father may be better prepared to adjust to her first-time adult pair-bonding. Because mothers socialize more with daughters, although to a lesser degree than fathers, this supports an argument that young ¥¥ need additional social skill preparation to be successful in reproductive relationships. Enhanced compatibility of young adult Callimico pairs may result from such short-term intersexual social relationships. This behavior could also enhance future reproductive success. Reproductively successful primiparous parents would, in turn, produce more reared offspring. A result that not only enhances individual reproductive success, but also bodes well for the survival of this geographically spread, low population density species. 166 Conclusions Darwin (1859) argued that sexual dimorphism is a consequence of sexual selection. Furthermore, he saw sexual dimorphism as resulting in diverse and specialized roles for each sex during reproductive behavior and infant care. Small-bodied monomorphic primate species that practice at least partial monogamy often include fathers in infant care- giving behaviors. Whitten (1987) defined the male's role in regard to extensive infant care-giving behaviors as spending the better part of each day taking care of infant(s). The more dimorphic large-bodied species engage in reproductive strategies which include multiple reproductively active tfcT and/or ?? in each social group. Males not only help defend territory and subsistence resources, but also must assert themselves to defend mating rights to individual ¥¥. Consequently, they spend much less time with postpartum ¥? and their offspring. Callimico is small-bodied and monogamous, at least in captivity, and fathers practice intensive infant care-giving. Results from this analysis indicate greater variation than characterizes other species committed to this same reproductive strategy. Aotus, Callicebus, and the callitrichid fathers care for newborns on their day of birth. Males engage in an assemblage of 167 infant care-giving behaviors until offspring locomote independently, generally between 8-12 weeks of age. This is not the case for Callimico fathers. Callimico fathers do not begin to actively practice infant care-giving behaviors until the offspring is about three weeks old. From then until the infant is locomoting independently, fathers variably carry, groom, sit-by, and share food with their offspring. Fathers appear to take a more active role in socializing young daughters. The father's directed behavior might be seen as a tactic to help insure future reproductive success for his daughter. His behaviors, if similar to those of a young adult cf, could help prepare the young 9 for the eventual difficult social transition she must make when locating a mate and becoming reproductively active. If a young adult 9, who just dispersed from her natal group is knowledgeable regarding the behaviors of an adult (her father), she might more quickly and easily adapt to a social and sexual relationship with an unfamiliar adult OLDER SIBLINGS AND INFANT CARE Introduction In Aotus, Callicebus, and the callitrichids older siblings care for newborns. These infant care-giving behavior studies have not utilized large samples making it difficult to evaluate the relationship between sustained reproductive success and the number of nonreproductive helpers in a family group (Price, 1992). Although long-term reproductively successful, the Callimico colony at Brookfield Zoo also did not generate a large sample of nonreproductive helpers (older siblings) per family group. But, because there are virtually no data examining intensive infant care-giving behaviors by sibling Callimico and the effect of such behavior on future reproductive success, the results of this analysis could provide an argument substantiating the merits of infant care experience (ICE) by juveniles and subadults in an early maturing reproductively active species. 168 169 Methods During the study period there were seven first births, four second births, one third birth, and one fourth birth in seven unchanged nuclear family groups at Brookfield (see Table 2). Examined first is the juvenile's role in infant carrying and its association with the same behavior in parents. Infant carrying by juveniles is minimal and does not accurately reflect their interest in newborn brothers or sisters. Thus, it was necessary to compare close proximity and contact behaviors between fathers and mothers carrying newborns, and first-born juveniles. Close proximity and contact behaviors, i.e., solicit groom, allogroom, and approach and sit-by are used to examine interest in newborns shown by juvenile Callimico. Comparisons between parent- juvenile interactions are made to examine how first-born offspring are influenced by birth of another sibling. Specifically, do juveniles interact more with their mothers who are carrying newborns or with their fathers? These close proximity and contact behaviors are also analyzed to determine how sex of first-born siblings influences attentive behaviors toward mothers carrying newborns. Four first-born juveniles were present when subsequent offspring were born. The number of cf and 9 six-month-old juvenile siblings was equal; first-born offspring in Groups 170 3 and 4 were d'd', and in Groups 2 and 5 were ??. Because these four first-born offspring included equal numbers of each sex, results should be equivalent regarding interactions between juvenile dd and ¥?, and fathers and mothers carrying newborns. Data are presented as grand totals for close proximity and contact interactions occurring between first-born offspring and parents during the second-born offsprings' infant dependence cycle. Complete locomotor independence of second-born offspring occurred as early as 12 weeks (Group 4) and as late as 17 weeks (Group 3) postpartum. As a result, the four second-birth infant dependence cycles are measured through an interval of 17 weeks (n=17). MONTE CARLO is used to determine whether there are statistically significant differences in the occurrence of interactions between juvenile siblings, and fathers and mothers carrying newborns. Differentials in behavior indicate whether or not juvenile siblings were attempting to interact with newborns. Differences in care-giving behaviors will also be examined for a d as a juvenile and subadult. The first-born offspring from Callimico Group 3 (Lew) is the focus animal for this analysis. Differences in infant care-giving between a subadult o* and juvenile 9 will be examined following birth of a third sibling. Lew and his younger 171 sibling Kris will be the focus animals for this comparison. Lew's infant carrying behavior as a juvenile and subadult will also be used to validate the necessity of ICE by older siblings. Juvenile Siblings and Infant Care Six-month-old first-born Callimico juvenile siblings minimally carried their second-born siblings (Figure 7). During weeks when first-born offspring carried newborns, they did so less than 2% of the total carrying time (Figure 8). Mothers apparently were more affected by juvenile help, carrying newborns 12% less when juveniles were available to carry newborns. Juveniles carried newborns more than 2% of total weekly carrying time only when they first carried during week three (Figure 9). They carried somewhat less, but consistently during the middle stage of infant dependence (weeks 6-8). Overall, it is difficult to determine which adult profited more from carrying by juveniles, but it is unlikely either parent benefited much from juvenile infant carrying. Because infant carrying by juveniles was limited another methodology was used to examine whether birth of a second offspring affected behavior of a first-born. Three major categories of close proximity and contact behaviors 172 were examined: solicit groom, allogroom, and approach and sit-by. These dyadic interactions were summed by week while the newborn was still dependent on others for transportation (n=17). Comparative frequencies of occurrence per age-sex group are displayed as grand totals. Fathers solicited juveniles to groom 375 times, while mothers carrying newborns did so 266 times, p=.03. In response, juveniles groomed fathers 405 and mothers carrying newborns 467 times, p=.22. While fathers solicited juveniles to groom more than did mothers, the data grand totals show that juveniles groomed mothers more than fathers. It is appropriate to note that juveniles groomed mothers 176% as often as mothers solicited juveniles, while fathers were groomed only 108% as often. Juvenile offspring displayed a clear grooming preference for mothers carrying newborns. Juvenile offspring solicited fathers to groom 779 times, but only solicited mothers 634 times, p=.18. In response, fathers groomed juveniles 400 times, while mothers did so 304 times, p=.13. The data grand totals show that juveniles solicited fathers to groom more than they did mothers carrying newborns. In response, fathers groomed juveniles more than did mothers. Fathers approached and sat-by first-born offspring 73 times, mothers carrying newborns did so 7 6 times, p=.50. 173 Juveniles approached and sat-by fathers 559 and mothers 913 times, p=.01. The data grand totals show that mothers carrying newborns and fathers approached and sat-by juveniles almost equally, but juveniles approached and sat- by mothers carrying newborns more than fathers. Juveniles showed partiality toward fathers and mothers carrying newborns in close proximity and contact behaviors (Table 6). Out of six interactive sequences, juveniles favored or were favored by mothers and fathers three times each. These results suggest that juveniles show some interest in newborns. Because results were mixed, close proximity and contact behaviors were used to determine if sex of juveniles influenced interactions between parents and first-born offspring. The same three interactive categories were examined. Data are summed by week. Because sex of juveniles is included in this analysis, there are eight behavior sequences in each category. The infant dependence •cycles comparing interactions between juvenile daughters and parents, and sons and parents are 16 and 17 weeks, respectively (n=16, n=17). Fathers solicited juvenile daughters to groom 194 times, they solicited sons 180 times, p=.29. Mothers, solicited daughters to groom 116 times, they solicited sons 150 times p=.19. The data grand totals show that fathers solicited juvenile daughters to groom slightly more than 174 TABLE 6. Proportion of Occurrence Grand Totals of Close Proximity and Contact -Behaviors among First-born Juveniles, Fathers, and Mothers carrying Newborns. Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence Fathers Solicit juvenile .585 progeny to groom Mothers Solicit juvenile .415 progeny to groom All juvenile progeny Groom fathers .464 All juvenile progeny Groom mothers .535 All juvenile progeny Solicit fathers to .551 groom All juvenile progeny Solicit mothers to .449 groom Fathers Groom juvenile progeny .568 Mothers Groom juvenile progeny .432 Fathers Approach and sit/by .49 juvenile progeny Mothers Approach and sit/by .51 juvenile progeny All juvenile progeny Approach and sit/by .38 fathers All juvenile progeny Approach and sit/by .62 mothers 175 sons, and mothers solicited juvenile sons more than daughters. In response, juvenile daughters groomed fathers 231 times and juvenile sons did so 173 times, p=.04. Daughters groomed mothers 188 times and sons did so 279 times, p=.04. Juvenile daughters and sons were more attentive to fathers and mothers, respectively. Again it is obvious that grooming frequency by offspring exceeds solicitation by parents. This increased activity by juveniles may indicate ongoing socialization by parents. Patterns of performance of these behaviors seems to support the hypothesis that socialization occurs by parents of the opposite sex to juvenile offspring. Juvenile daughters solicited fathers to groom 567, but juvenile sons did so only 214 times, pc.001. In contrast, daughters and sons solicited mothers carrying newborns to groom almost equally, 314 and 336 times, p=.50. Fathers appear to provide security and stability for juvenile daughters when mothers direct their attention to newborns. Why juvenile sons do not focus on fathers for assurance during this time may relate to the ongoing process of socialization by mothers. Juvenile sons soliciting mothers to groom more than juvenile daughters supports this view. Juvenile daughters solicited fathers to groom more than did sons and fathers groomed daughters 280 times, but only 176 groomed sons 115 times, p=.004. Mothers groomed daughters 140 times, but groomed sons 167 times p=.37. Fathers are more attentive to juvenile daughters, and the data grand totals show that mothers are somewhat more attentive to sons. These data show that, whereas fathers socialize daughters, juvenile daughters are interested in mothers carrying newborns. Fathers approached and sat-by daughters 47 times, and sons 25 times, p=.06. Mothers carrying newborns approached and sat-by daughters 57 and sons 20 times, pc.OOl. These results show that fathers and mothers were more attentive to daughters. Juvenile daughters approached and sat-by fathers 393 times, sons did so 166 times, p<.001. This result shows that fathers are a focal point for daughters during periods of change, such as the birth of a sibling. Juvenile daughters and sons approached and sat-by mothers carrying newborns 521 and 390 times, p=.04, showing that juvenile daughters were more attentive to mothers carrying newborns. Since daughters consistently out-performed sons in this behavior, this supports the suggestion that they were interested in the newborns and may have been initiating the process of learning infant care-giving behaviors. Although fathers interact with juvenile daughters more than sons and mothers carrying newborns interact with sons more than daughters, there is one exception (Table 8). 177 Mothers carrying newborns approached and sat-by daughters more than they did sons. The more frequent performance of this behavior by mothers toward daughters suggests that mothers may be providing juvenile daughters opportunities to interact with newborns. Thereby, mothers begin the process of learned infant care by rapidly maturing juvenile ??. Even though first-born juvenile offspring are being socialized by parents, postpartum estrus cycling by mothers often results in pregnancy and birth of subsequent siblings. Since juvenile sons socialize more with their mothers, they are in a position to immediately learn infant care-giving behaviors. Juvenile daughters socialize more with their fathers than with their mothers. To initiate the process of learned infant care-giving behaviors by juvenile daughters, mothers carrying newborns often seek out their daughters. Performance of this behavior by mothers gives juvenile daughters additional opportunities to view, be near, and perhaps interact with newborns. Weighted performance of this behavior by mothers in favor of daughters also gives juvenile 9? more opportunities to observe infant care- giving behaviors performed by reproductively active 99. TABLE 7. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors among Callimico First-born Juvenile Females and Males, Fathers, and Mothers carrying Newborns. Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence Fathers Solicit juvenile .519 daughters to groom Fathers Solicit juvenile .418 sons to groom Mothers Solicit juvenile .436 daughters to groom Mothers Solicit juvenile .564 sons to groom Juvenile daughters Groom fathers .572 Juvenile sons Groom fathers .428 Juvenile daughters Groom mothers .403 Juvenile sons Groom mothers .597 Juvenile daughters Solicit fathers to .726 groom Juvenile sons Solicit fathers to .274 groom Juvenile daughters Solicit mothers to .483 groom Juvenile sons Solicit mothers to .517 groom Fathers Groom juvenile .709 daughters Fathers Groom juvenile sons .291 Mothers Groom juvenile .456 daughters Mothers Groom juvenile sons .544 179 Table 7 (continued) Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence Fathers Approach and sit-by .658 juvenile daughters Fathers Approach and sit-by .347 juvenile sons Mothers Approach and sit-by .74 juvenile daughters Mothers Approach and sit-by .26 juvenile sons Juvenile daughters Approach and sit-by .703 fathers Juvenile sons Approach and sit-by .297 fathers Juvenile daughters Approach and sit-by .572 mothers Juvenile sons Approach and sit-by .428 mothers Subadult Siblings and Infant Care Only one unchanged family group of Callimico at Brookfield Zoo experienced three consecutive births. Group 3 originated from the founding population and initially consisted of the male/female pair, Jos6 and Tina (see Table 3). The third newborn born in this group joined an older brother and sister. At the time of birth of the third offspring, the first-born, a cf named Lew, was 323 days old, and the second-born, a ? named Kris, was 161 days old (see Table 3). The day Kris was born Lew was 162 days old, only one day older than Kris when the third offspring (Minnie) was born. 180 This section compares the infant care-giving behaviors of Lew during the infant development cycles of the second- (Kris) and third-born (Minnie) offspring. The analysis and discussion focus on Lew's infant carrying behavior and the complex of close proximity and contact behaviors between Lew, and his father and mother while she carried two subsequent newborns. Infant carrying behavior and close proximity and contact behaviors between Lew's juvenile sister, Kris, and her parents following the birth of Minnie are examined and discussed. Differences in interactive behavior frequencies between first and second-born offspring, and their father and mother carrying a newborn should provide data on which sibling interacts more with the newborn. Close proximity and contact behaviors are again used to determine which members of the group interacted most frequently during Minnie's 16 week dependence cycle. Passive food sharing between Lew and Minnie, and Kris and Minnie during Minnie's infancy are also examined to determine if the newborn interacted more often with Lew or Kris. These data are summed weekly. During Lew's first experience with infant care, he intermittently performed infant transport. Lew first carried Kris when he was 188 days old, she was 26 days. He carried Kris during weeks 4-11, but logged more than two percent of the total carrying time per week only during 181 weeks 7-8 (Figure 10). Lew is slightly above average for all first-born offspring (n=4) who carried newborns during this time frame (see Figure 9). Lew's brief carrying of Kris did not appear to affect weekly carrying times for either parent. Lew and his parents' frequency of close proximity and contact during Kris' infancy suggests that Lew was attentive to the presence of the newborn. Lew's father, Jos6, solicited Lew to groom 169 and his mother, Tina, did so 117 times, p=.04. Lew groomed his father 118 and his mother 146 times, p=.16. Although Jose solicited Lew to groom more than did Tina, the data grand totals show that Lew groomed his mother more than his father. Lew groomed his father 69% of the time he was solicited. Lew groomed his mother 124% more often than she solicited him. Lew's spontaneous grooming of his mother while she carried a newborn suggests that Lew was attentive to the newborn's presence. Lew solicited Jose to groom 86 and Tina 255 times, pc.OOl. Lew's father groomed his juvenile son 19 and his mother did so 86 times, p=.002. Lew solicited his mother to groom more than his father while she carried a newborn. Tina groomed Lew more than did Jose, thus providing Lew with more opportunities to observe, be near, and interact with his infant sibling. 182 Jose approached and sat-by Lew 22 times, while Tina did so 11 times, p=.07. Lew approached and sat-by his father 102 and mother 261 times, pc.OOl. Although Tina did not approach and sit-by her son more than did Jose, Lew did so with his mother more than father. Results of the analysis of close proximity and contact behaviors between Lew and his parents are mixed (Table 8). Still, it appears that Lew showed increased interest in his mother while she carried a newborn. Tina groomed Lew in response to Lew's solicit to groom behavior more than did his father. By acting so, Tina may have reduced her son's uncertainty toward the newborn while keeping Lew close to interact with his infant sister. Lew's behavior toward newborns was considerably different as a subadult. Lew's carrying of his first sister, Kris, was minimal. Still, Lew interacted with his mother more than his father while she carried Kris. Following the birth of Minnie, his second sister, Lew appeared to practice more infant carrying and care-giving. Lew first carried Minnie when he was 353 days old, Minnie was only 38 days old. During weeks 7-9, following Minnie's birth, Lew carried her more than did her parents (Figure 11). Lew's mother, Tina, benefited most from Lew's increased infant carrying behavior during this time-frame. Tina carried Minnie only 1.5%, 2.9%, and 19.7% of the total TABLE 8. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Group 3's First-born Offspring (Lew) and Parents following Birth of Subsequent Infant. Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence Father (Jos6) Solicit first-born H .591 progeny (Lew) to groom H Mother (Tina) Solicit Lew to groom I .409 Lew Grooms Jos6 H .447 Lew Grooms Tina H .553 Lew Solicit Jos6 to groom H .252 Lew Solicit Tina to groom H .748 Jos6 Grooms Lew H .181 Tina Grooms Lew H .819 Jos6 Approach and sit-by H .667 Lew II Tina Approach and sit-by H .333 Lew H Lew Approach and sit-by H .281 Jos6 A Lew Approach and sit-by H Tina H H 719 I 184 carrying time during weeks 7-9 of Minnie's life. Interestingly, Kris carried her infant sister 2.7%-4.8% of total carrying time during weeks 10-13 (Figure 11). These totals are considerably more than when Lew, as a juvenile, carried Kris. Lew's diligent helping may have motivated Kris to be more active in carrying Minnie. Lew's participation in close proximity and contact behaviors with his parents following Minnie's birth was different from his participation following the birth of Kris. Jose solicited his son to groom 6 times, and Tina solicited Lew 33 times, p=.003. Lew groomed his father 5 and his mother 32 times, p=.002. Tina, while carrying a newborn, solicited her son more than did his father. Lew responded by grooming his mother more than his father. Lew solicited his father to groom 7 and his mother 86 times, pc.OOl. In turn, Jose and Tina groomed Lew 4 and 25 times, p=.003. While Tina carried Minnie, Lew solicited his mother to groom more than he did his father. Tina responded by grooming her son more than did his father. Jose approached and sat-by Lew 1 time, while Tina did so 3 times, p=.31. Lew approached and sat-by his father 8 and his mother 30 times, p=.001. While the data grand totals show that Tina approached and sat-by her son slightly more than did Jose, Lew did so with his mother more than his father. 185 Lew interacted with his mother much more than with his father (Table 9). While carrying a newborn, Tina interacted with her son more than did his father (Table 9). In only one interactive sequence (parent approach and sit-by first born) , did Lew not interact with his mother significantly more than his father. This may be related to the infrequent occurrence of this behavior. Lew's behavior during Minnie's infancy can better be established by comparing it with his performance during Kris' infant dependence. Lew and his mother interacted more with one another in four of six behavioral sequences during Kris' infancy (see Table 8). Following Minnie's birth Lew and his mother interacted more with one another in all six behavioral sequences. Although generalizations are limited because of small sample size, these data show that Lew participated in intensive infant care-giving more with Minnie than with Kris. Lew interacted with his mother more than his father while she carried Minnie. Kris interacted with her father more than her mother during this time. Jose solicited Kris to groom 19 times, while Tina solicited Kris 11 times, p=.23. Kris groomed her father 21 and her mother 17 times, p=39. Kris solicited her father 58 and her mother 46 times, p=.31. Kris' father groomed her 11 times, while her mother groomed her 12 times, p=.50. 186 Table 9. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Group 3's First-born Offspring (Lew) and Parents following Birth of Second Infant. Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence Father (Jos6) Solicit first-born .154 progeny (Lew) to groom Mother (Tina) Solicit Lew to groom . 846 Lew Grooms Jos6 .135 Lew Grooms Tina . 865 Lew Solicit Jos6 to groom .075 Lew Solicit Tina to groom . 925 Jos6 Grooms Lew .138 Tina Grooms Lew .862 Jos6 Approach and sit-by .25 Lew Tina Approach and sit-by .75 Lew .211 Lew Approach and sit-by Jos6 .789 Lew Approach and sit-by Tina 187 Jose and Tina each approached and sat-by Kris twice, ,p=.68. Kris did so with her father 63 and her mother 54 times, p=.33. Kris carried Minnie for brief periods. Still, Kris interacted with her father more than her mother during Minnie's infancy (Table 10). Jose seems to have assumed responsibility for socializing Kris more than did Tina during Minnie's dependency. The interactions between Kris and Lew during Minnie's infancy provide insight into how juvenile offspring learn infant care in multiple offspring groups. When Lew was most responsible for Minnie's transport, weeks 7-9 postpartum (see Figure 11), Kris interacted more with Lew. She approached and sat-by Lew more often after he assumed primary responsibility for carrying Minnie (Figure 12). Shortly thereafter, weeks 10-13, Kris performed the majority of her newborn transport as Lew and she shared carrying Minnie (see Figure 11). Because Kris' infant carrying immediately followed Lew's behavior in weeks 7-9 following Minnie's birth, her behavior is possibly a catalytic extension of Lew's infant carrying experience. Records on who was carrying the newborn during each interaction sequence between Lew and Kris were not kept. Still, it appears that Kris became more comfortable with the newborn and more readily accepted infant transfer as she 188 TABLE 10. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Group 3's Second-born Offspring (Kris) and Parents following Birth of Subsequent Infant. Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence Father (Jos6) Solicit second-born .633 progeny (Kris) to groom Mother (Tina) Solicit Kris to groom .367 Kris Grooms Jos6 .533 Kris Grooms Tina .447 Kris Solicit Jos6 to groom .558 Kris Solicit Tina to groom .442 Jos6 Grooms Kris .478 Tina Grooms Kris .522 Jos6 Approach and sit-by .50 Kris Tina Approach and sit-by .50 Kris Kris Approach and sit-by .538 Jos6 Kris Approach and sit-by .462 Tina e b b s 189 interacted more closely with Lew while he had primary responsibility for carrying Minnie. Lew's infant care behavior appears to have been the stimulus for Kris' helping behaviors. Food sharing between siblings was not regularly practiced during neonatal development. Still, when Lew carried Minnie he passively shared food with her more often than at any other time (Figure 13). During weeks 7-12 following Minnie's birth, Lew passively shared with his newborn sister more than did any other group member. In all cases, with the exception of Kris in week 7, Minnie received 100% of the passive shares she solicited from family members. These results suggest that newborns may solicit more shares from older siblings than from parents and, in return, receive more shares from older siblings. Conclusions Data on infant care-giving behaviors by the four first born juveniles indicate they minimally assisted their parents in rearing second-born offspring. They carried newborns for brief periods of time and did most of their carrying while newborns were in the middle stage, weeks 4-7 postpartum, of infant development. This carrying time, although well into the infant development cycle, provided 190 juveniles additional opportunities to interact with younger siblings. Close proximity and contact behaviors indicate that juvenile Callimico 9 9 and cfcf are interested in newborn siblings. Juvenile offspring groomed mothers carrying newborns more often than they did fathers, even though mothers solicited juveniles less. Mothers carrying newborns approached and sat-by juveniles more than did fathers. Juveniles also approached and sat-by mothers with newborns more than they did fathers. Being in close proximity to newborns likely gives juveniles more opportunities to closely observe, if not participate, in infant care-giving behaviors. Data are available from only one group that record juvenile and subadult infant care-giving behaviors. Still, results clearly indicate that this individual (Lew) was more active in infant care-giving as a subadult than as a juvenile. Lew's additional helping behavior during Minnie's infancy demonstrate that, as Lew neared sexual maturity and adult status, he was more active in infant care. This suggests that behaviors learned as a juvenile and subadult may better prepare Callimico to succeed as first-time parents. CHAPTER VIII PREVIOUS INFANT CARE EXPERIENCE IN PRIMI PAROUS PARENTS Introduction Anthropoid behavior is largely based on learned experiences (Baldwin & Baldwin, 1979; Rowell, 1975). In many species, successful reproductive behavior is tied closely to learned parenting skills. Primiparous parents without prior experience seem to be less successful at rearing their offspring. This may be particularly true for those primates that develop rapidly and mature early. Still, learned parenting behaviors by one generation from the previous have been little studied. This chapter addresses learned parenting skills among primiparous parents and their reproductive success. Methods Data were available on two Fj captive-born Brookfield ?? and one cf who later had offspring in the colony. Prima, the first-born Fj female, was paired with Antonio, the first-born Fx male. Judy, the second-born Fx female, was 191 192 paired with Pepe, the youngest cf from the founding population. Infant care experience of both ?? was comparable. However, Antonio had ICE through only one succeeding infant's infancy. Pepe's learned infant carrying and care- giving skills were unknown. However, his infant carrying was similar to that of the first-born Infant carrying was minimal for Prima and Judy and completely lacking for Antonio, F: captive-born primiparous parents. Therefore, the close proximity and contact behaviors were used to examine ICE by these parents. This was done to determine whether as juveniles these individuals interacted more with their fathers or mothers carrying newborns. If interactions with mothers were greater, this would suggest greater opportunities to learn infant care- giving skills. This would also suggest the juveniles were seeking to interact with newborn siblings. As a primiparous parent, Antonio did not carry his offspring. Therefore, a different method is used to examine the quality of his infant care skills. This is still based on the suite of close proximity and contact behaviors, but also includes passive and reluctant food sharing. If 193 Antonio and Prima interact equally with their infant, Antonio was likely an adequate first-time parent. MONTE CARLO is used to test for significant differences in interaction frequencies between parents and offspring through four infant dependence cycles, 12-16 weeks long (n=12,13,14,16). The data are summed and computed by week. The data displayed in the text are grand totals for each interaction. Primiparous Mothers and Previous Infant Care-aivina Experience ICE for the two 99 was of short duration. As juveniles, they carried infant siblings less than one percent of family group total carrying time (Figure 14). They did so during weeks 3 and 10 postpartum (Figure 15). Given these low totals, close proximity and contact interactions between these two 9 9 and their parents during their siblings' infancy were used to examine whether they showed a preference for mothers carrying newborns. If mothers carrying newborns socialized more with daughters and daughters did so with mothers carrying newborns, this would suggest a preference by juvenile 99. Such a preference would suggest that the two 9 9 were observing infant care- giving and interacting with their infant siblings. 194 Fathers solicited juvenile daughters to groom 194 times, and mothers carrying newborns did so 116 times, p=.04. Juvenile daughters groomed fathers 231 and mothers 188 times, p=.16. Fathers solicited juvenile daughters to groom more than did mothers, and the data grand totals show that daughters groomed fathers somewhat more than mothers. Juvenile daughters solicited fathers to groom 567 and mothers carrying infants 314 times, p=.001. Fathers groomed daughters 280 times, mothers did so 140 times p=.007. Not only did juvenile daughters solicit fathers to groom more than mothers, but fathers responded by grooming juvenile daughters more than did mothers. Fathers and mothers approached and sat-by juvenile daughters 47 and 57 times, p=.30. Juvenile daughters approached and sat-by fathers 393 and by mothers 521 times, p=.07. While the data grand totals show that mothers carrying newborns approached and sat-by juvenile daughters slightly more than did fathers, daughters approached and sat-by mothers more than fathers. Close proximity and contact data on the juvenile ?? show that these individuals interacted more with fathers and less with mothers carrying newborns (Table 11). Individual family interaction totals are different from these combined totals for both young 9?. Data from Group 2, Judy, are presented first, and those for Group 5, Prima, last. 195 TABLE 11. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Juvenile Daughters and Parents during Infancy of Second-born Offspring. Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence Fathers Solicited juvenile .626 daughters to groom Mothers Solicited juvenile .384 daughters to groom Juvenile daughters Groom fathers .551 Juvenile daughters Groom mothers .449 Juvenile daughters Solicit fathers to .644 groom Juvenile daughters Solicit mothers to .356 groom Fathers Groom juvenile .667 daughters Mothers Groom juvenile .333 daughters Fathers Approach and sit-by .452 juvenile daughters Mothers Approach and sit-by .548 juvenile daughters .43 Juvenile daughters Approach and sit-by fathers .57 Juvenile daughters Approach and sit-by mothers 196 Judy was the first offspring born in Group 2. She was 166 days old when her infant sister, Vicki, was born. Judy was 175 days old when she first carried nine-day-old Vicki. She did not carry Vicki again until the newborn was 25 days old. Following which, Judy carried her newborn sister occasionally for the next seven weeks (Figure 16). Although Judy did not carry Vicki very long, she did acquire more infant carry experience as a juvenile than any other first born offspring in the Brookfield colony. Close proximity and contact behaviors between Judy and her parents during Vicki's infancy are different from the combined totals just presented. Will, Judy's father, solicited his daughter to groom 3 times, while Eunice, Judy's mother, did so 26 times, p=.001. Judy groomed her father 72 and mother 76 times, p=.46. Although Judy's mother solicited her daughter to groom more than did her father, the data grand totals show that Judy groomed her mother only slightly more than her father. Judy solicited her father and mother to groom 117 and 186 times, p=.02. Will groomed his daughter 24 and Eunice did so 87 times, p<.001. During Vicki's infancy, Judy solicited her mother to groom more than she solicited her father. Eunice responded to Judy's solicitations grooming her daughter more than did her father. 197 Will approached and sat-by Judy 39 and Eunice did so 19 times, p=.06. Judy approached and sat-by her father 260 and mother 278 times, p=.38. Judy's father approached and sat- by his daughter more than did her mother. Judy did so with her mother carrying a newborn slightly more than with her father. Callimico fathers generally interact with daughters more than sons. However, when Judy's mother Eunice was carrying Vicki, Judy interacted with her mother more than her father (Table 12). Judy's interactions with her parents were apparently influenced by the presence of an infant sibling. Judy's high infant carry totals (for juveniles) may have been a direct result of interactions with her mother and infant sister. During the interactions between Judy and Eunice, the newborn (Vicki) could have transferred to Judy with ease. Behavioral interactions of Eunice and Judy are different from those of the Group 5 reproductive ? and her first-born daughter after the birth of a second infant. Prima was the first-born in Group 5. She was also the first Fj Callimico born at Brookfield Zoo. Prima was 167 days old when her brother Ken was born. Prima first carried Ken when she was 193 days old, Ken was 26 days. Prima's infant 198 TABLE 12. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Group 2's First-born Offspring (Judy) and Parents during Infancy of Second-born Offspring. Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence Will (Father) Solicit first-born . 103 progeny (Judy) to groom Eunice (Mother) Solicit Judy to groom .897 Judy Grooms Will .486 Judy Grooms Eunice .514 Judy Solicit Will to . groom .386 Judy Solicit Eunice to .614 groom Will Grooms Judy .216 Eunice Grooms Judy .784 Will Approach and sit-by .672 Judy Eunice Approach and sit-by .328 Judy Judy Approach and sit-by .483 Will Judy Approach and sit-by .517 Eunice transport experience was quite limited. She carried her brother only during weeks 4, 8, and 10 following his birth, and only briefly (Figure 17). Prima's father, Scruffy, also hardly carried Ken during his infancy, during weeks 5 and 7-10 (Figure 17). Overall, Scruffy contributed minimally to infant carrying (Figure 18). Prima's periods of carrying Ken coincided with weeks when Scruffy also carried the newborn. Callimico fathers may motivate and precipitate infant carrying by juveniles. Perhaps Scruffy's infrequent carrying of Ken failed to encourage Prima to carry her infant brother. Scruffy's lack of carrying may have been the result of his own limited experience. As will be described, one Brookfield primiparous father without infant carry experience did not carry his first-born offspring. Since Prima barely carried her infant brother, close proximity and contact interactions between Prima and her parents, during Ken's infancy, were examined to determine if she gained ICE from close association with her mother (Betty) and infant brother. Scruffy solicited Prima to groom 191 times, Betty did so 90 times, p=.01. Prima groomed her father 162 and her mother 112 times, p=.08. Prima's father solicited her to groom more than did her mother, and Prima groomed her father more than she groomed her mother. 200 Prima solicited her father to groom 450 times, but only solicited her mother 128 times, pc.OOl. Scruffy groomed his daughter 257, while Betty groomed Prima 53 times pc.OOl. Not only did Prima solicit her father to groom more than she did her mother, but Scruffy groomed Prima more than did Betty. Scruffy approached and sat-by Prima 8 times, while Betty did so 39 times, pc.OOl. Prima approached and sat-by her father 133 and her mother 243 times, p=.007. During Ken's infancy, Betty approached and sat-by Prima more than did Scruffy. Prima, in turn, approached and sat-by her mother more than her father. Scruffy and Prima solicited and groomed each other more often than Betty and Prima (Table 13). Prima's mother approached and sat-by her daughter more than did her father (Table 13). Prima responded by approaching and sitting-by her mother more than her father (Table 13). Since Betty carried Ken more than 98% of the time during his infancy (see Figure 18), Prima was in close proximity to her infant brother much of the time. Not only did Prima's mother place her daughter in a position to interact with her infant brother, Prima also placed herself in such positions allowing her to observe her mother perform infant care- giving behaviors and perhaps to practice these behaviors herself. Although Scruffy undertook the primary 201 TABLE 13. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Group 5's First-born Offspring (Prima) and Parents during Infancy of Second-born Offspring. Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence Scruffy (Father) Solicit first-born .68 progeny (Prima) to groom Betty (Mother) Solicit Prima to groom .32 Prima Grooms Scruffy .591 Prima Grooms Betty .409 Prima Solicit Scruffy to .779 groom Prima Solicit Betty to groom .221 Scruffy Grooms Prima .829 Betty Grooms Prima .171 Scruffy Approach and sit-by .17 Prima Betty Approach and sit-by .83 Prima Prima Approach and sit-by .354 Scruffy Prima Approach and sit-by .646 Betty 202 responsibility for socializing his juvenile daughter, Prima maintained an interest in her mother, as Betty carried infant Ken. Primiparous Fathers and Previous Infant Care-aivino Experience Antonio was the first Fa Callimico cf born at Brookfield. When his younger brother Juan was born, Antonio was 195 days old. Antonio never carried his newborn brother (Figure 19). Antonio and Juan's father (Rob) carried Juan about 31% of the time (Figure 20). Thus, when Antonio interacted with his father and mother (Marie), he was in close proximity to his infant brother. It might be expected, from his father's active infant carrying, that continued close proximity to Juan would have encouraged an infant transfer to Antonio. However, this did not occur. Close proximity and contact interactions between Antonio, and Rob and Marie, as both parents carried Juan, suggests that Antonio had access to his infant brother. Rob solicited Antonio to groom 12 times, Marie did so 33 times, p=.005. Antonio groomed his father 55 and his mother 133 times, pc.OOl. Marie solicited Antonio to groom more than did his father. Antonio groomed his mother more than his father. Antonio solicited his father to groom 128 203 and his mother 81 times, p=.06. Rob groomed Antonio 96 and Marie did so 81 times, p=.31. Antonio solicited his father to groom more than his mother and Rob groomed him more than did Marie. Still, Marie groomed Antonio 100% of the time he solicited her, while Rob did so about 75% of the time. Rob approached and sat-by Antonio 3 times, while Marie did so 9 times, p=.06. Antonio approached and sat-by his father 64 and his mother 129 times, p=.004. During Juan's infancy, Marie approached and sat-by Antonio more than did his father, and Antonio did so with his mother more than his father. Antonio interacted with his mother more than his father (Table 14). His mother carried Juan almost 70% of the time. These interactions probably gave Antonio many opportunities to be close to and interact with Juan. Why Antonio never even briefly carried Juan cannot be determined. Whatever caused this inconsistency, it was not because Antonio was not in close proximity to or did not have opportunities to carry his brother. Judy, Prima, and Antonio were the only known primiparous parents in the Brookfield Callimico colony during this study. Pep§'s, Judy's mate, degree of ICE and reproductive success were questioned. Since he was a colony founder, he had no documented early life-history. One piece 204 TABLE 14. Proportion of Occurrence Grand Totals of Close Proximity and Contact Behaviors between Callimico Group 4's First-born Offspring (Antonio) and Parents during Infancy of Second-born Offspring. Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence Rob (Father) Solicit first-born .25T...... progeny (Antonio) to groom Marie (Mother) Solicit Antonio to .733 groom Antonio Grooms Rob .293 Antonio Grooms Marie .707 Antonio Solicit Rob to groom . en... Antonio Solicit Marie to groom .388 Rob Grooms Antonio .542 Marie Grooms Antonio .458 Rob Approach and sit-by .25 Antonio Marie Approach and sit-by .75 Antonio Antonio Approach and sit-by .332 Rob Antonio Approach and sit-by .668 Marie 205 of evidence indicates that Pepe may not have been reproductively active prior to his captivity. When first introduced to an adult ¥ (Tango) from the founding population, Pep6 was dominated by and became subordinate to Tango. As a result, there was no sexual behavior between the two individuals. His subordinate behavior in the face of an adult ¥ suggested that he had no prior reproductive experience. Perhaps Pepe was a subadult or very young adult when he arrived at Brookfield Zoo. When Pep§ and Judy's infant was born, Judy carried the newborn without Pepe's assistance for the first six weeks. During week seven, Judy attempted to force the infant from her back by rubbing the newborn against external enclosure features and pulling or biting at its limbs and tail. Pepe made himself available for infant transfer and began to carry the infant. Following that, Pepe and Prima alternated carrying their infant daughter until she was 14 weeks old and locomoting independently (Figure 21). Pep6's infant carry behavior appears quite similar to Lew's (the first born cf from Group 3) as a subadult, when he carried his infant sister, Minnie (see Figure 11). This similarity suggests that Pepe was a young adult when he arrived at Brookfield Zoo. In contrast, Antonio did not carry the infant he fathered with Prima. Prima, as had Judy, began to attempt 206 to force the infant from her back during its seventh week of life. She, like Judy, attempted to dislodge the newborn by rubbing it against external enclosure features and/or pulling and biting at its limbs and tail. Antonio, unlike Pepe, did not make himself available for infant transfer. The absence of infant carry behavior by Antonio as a parent appears to result from his lack of infant carry experience as a juvenile. Was Antonio's poor infant carrying behavior an example of his general skills as a first-time parent? An examination of the interaction frequency differences between primiparous fathers and mothers, and their newborns might provide an answer to this question. The close proximity and contact, and passive and reluctant food share behaviors were analyzed to discover if there was a significant difference in the number of interactions between tf or ¥ primiparous parents and their infants. The data were compiled by week following the first incidence of a scored behavior (other than carrying) between parent and infant. The data set begins during the Group 6 (Antonio and Prima) infant's fourth week of life as Antonio first interacted (groomed) with the newborn during that week. The data set ends during the Group 7 (Pepe and Judy) infant's 17th week of life when data collection ended. Because there were few interactions between each group's parents and the newborn, the data sequences were pooled. 207 During this 14 week cycle, fathers solicited their two infant daughters to groom 5 times, while mothers only solicited their infants to groom 2 times, p=.24. Infants twice groomed their fathers, but never groomed their mothers, p=.26. Infants solicited fathers to groom 13 times, while they solicited mothers 9 times, p=.36. Both fathers and mothers groomed their daughters 16 times, p=.56. Fathers approached and sat-by their infants 12 times, mothers did so 16 times, p=.32. Infants approached and sat- by fathers 66 and mothers 94 times p=.19. Infants solicited passive shares from fathers 38 and mothers 85 times, p=.02. Fathers passive shared with their offspring 37 times, mothers did so 83 times, p=.02. Infants solicited reluctant shares from fathers 13 and mothers 29 times, p=.06. Both fathers and mothers reluctant shared with their infants once, p=.75. Fathers and mothers did not interact equally with their newborns (Table 15). Still, the only significant differences in behavioral interaction frequencies between fathers and infants and mothers and infants are in the food sharing behaviors. Because mothers shared food with infants more than did fathers in the parent-offspring interaction grand totals (Chapter VI), the results of this examination are not atypical. These results suggest that the absence of infant carrying behavior by Antonio did not lead to a 208 TABLE 15. Proportion of Occurrence Grand Totals of Close Proximity and Contact and Passive and Reluctant Share Behaviors between Primiparous Callimico Parents and Offspring during Infancy. Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence Fathers Solicit newborn .714 offspring to groom Mothers Solicit newborn offspring to groom .286 Offspring Groom fathers 1.0 Offspring Groom mothers .00 Offspring Solicit fathers to .59 groom Offspring Solicit mothers to .41 groom Fathers Groom offspring .50 Mothers Groom offspring .50 Fathers Approach and sit-by .429 offspring Mothers Approach and sit-by .571 offspring Offspring Approach and sit-by .412 fathers Offspring Approach and sit-by .588 mothers Offspring Solicit passive share .309 from fathers Offspring Solicit passive share .691 from mothers Fathers Passive share with .308 offspring Mothers Passive share with .692 offspring 209 Table 15 (continued) Individual(s) that Behaviors Behavior occurrence initiated the behavior proportions interaction sequence Offspring Solicit reluctant .31 share from fathers Offspring Solicit reluctant .69 share from mothers Fathers Reluctant share with .50 offspring Mothers Reluctant share with .50 offspring generalized deficiency in performance of parent-infant care- giving behaviors. Conclusions Several investigations report that older siblings from two cebid (Aotus and Callicebus) and the callitrichid genera practice intensive infant care-giving behaviors (Box, 1975, 1977; Cebul & Epple, 1984; Cleveland & Snowdon, 1984; Engel, 1985; Epple, 1975b; Hoage, 1978; Ingram, 1978; Rothe, et al., 1993; Tardif, et al., 1993; Vogt et al., 1978; Wright, 1984). A limited number of investigators suggest that ICE by primiparous parents is essential to successful reproductive behavior (Epple, 1975b, 1978; Hoage, 1978; Tardif et al., 1984). One investigation suggests that ICE by d'd' in at least one callitrichid species is not essential to survival of infant offspring (Tardif et al., 1984). Results of this analysis demonstrate that in Callimico some previous learned infant care by primiparous parents is necessary to rear offspring. Two primiparous 9 9 with limited ICE became adequate mothers of first-born offspring. One of the two young adult fathers, who had probable infant transport experience, began to carry his newborn following its mother's efforts to remove the infant from her. The other young father, with no infant carrying experience, never carried his first-born offspring. But, in an analysis of father-mother-infant interactive behaviors, this primiparous father performed other parental behaviors at normal rates. Although the results of the interactive behaviors analysis show that infants socialized more with their mothers, as they should because reproductive 9? are primarily responsible for newborns' survival, both sexes of both sets of primiparous parents more or less equally socialized with their offspring. Some learned ICE is essential for primiparous mothers to adequately rear first-born offspring. The same cannot be said for primiparous fathers. A father without infant carrying experience did not carry his first-born offspring, while a father with experience did supplement the mother's infant carrying behavior. This does not mean that the young father who did not carry his first infant will not carry 211 other, later born offspring. As carrying behavior by fathers appears to be learned from one generation to the next, young adult fathers without experience could learn the behavior as they attempt to limit the cost to mothers of carrying infants. CHAPTER IX CALLIMICO IN CAPTIVITY Introduction Systematic studies of Callimico behavior in a natural environment will produce the most accurate results, but for numerous reasons this has been a difficult endeavor. Publications on wild Callimico have often been vague and contradictory. In contrast, studies of captive populations have resulted in several publications recording intragroup behaviors. A criticism of captive studies is that a spatially limited environment results in increased rates of social behavior. Although there may be increased behavioral frequencies per individual, the proportion of interactions among group members should provide an accurate account of which age-sex groups socialize more with one another. None of the captive investigations have examined the socialization of offspring by parents, or the effect of such socialization on older siblings and infant care of subsequent offspring, or the impact of ICE by older siblings on their later reproductive success as first-time parents. 213 The current research addressed these issues as they affect intragroup behaviors. Impact of Physical and Behavioral Development on Intragroup Behaviors in Callimico This dissertation shows that Callimico physically develop and reach sexual maturity more quickly than callitrichids, but behaviorally they mature more slowly than callitrichids. Callimico remain infants longer than callitrichids resulting in an abbreviated adolescent cycle. Infant development and dependence cycles of Callimico newborns (until infants locomote independently) range from about 12- 17 weeks postpartum. Following infancy, the adolescent period (juvenile and subadult status) is only about 38-50 weeks. This segment of the Callimico life cycle for females seems to coincide with the time between locomotor independence of the first-born offspring and the second consecutive birth of subsequent offspring in the natal group (38 weeks). Males do not reach sexual maturity for at least another 12 weeks. The argument used here to validate the abbreviated adolescent period in Callimico centers around its reproductive strategy. 214 Callimico mothers exhibit a postpartum estrus cycle that can result in parturition twice annually, but with only one offspring each time (as opposed to twins in callitrichids). Because the costs to the parents are less when rearing only one newborn, there appears to be less need for older siblings as infant care-giving helpers. Callimico females become sexually mature and possibly disperse from their natal group at about one year of age. Thus, they only obtain ICE from one subsequent sibling birth and dependence cycle. This research examined whether learned but limited ICE by juvenile females, as a result of a short adolescent period and the birth of a single subsequent sibling, affect the quality of care these females provide their first-born offspring. Data presented here show that primiparous females with ICE from one subsequent sibling birth go on to become skilled, successful first-time mothers. The same cannot be said for primiparous fathers. It appears that males do not become sexually mature until they are about 15 months old. If delayed sexual maturation in males is consistent in Callimico, subadult males can experience a second subsequent infant birth and development cycle. Do primiparous fathers require this additional experience to fulfill their responsibilities as 215 skillful first-time parents? Data presented here show that a primiparous father without experience from two succeeding sibling infancies still interacted with his first-born. However, he did not reduce the infant care-giving costs to the mother by carrying the infant. Because this father's first-born survived, he is classified as reproductively successful, but he was not a skilled first-time parent. Males seem to need additional experience over two subsequent infancies in their natal group to receive sufficient ICE. Does limited time for socialization of offspring by parents have an effect on the initial pair bonding relationship of young adults and their later success as first-time parents? Callimico is more cebid-and cercopithecid-like in its parenting behaviors than the true monkeys Aotus and Callicebus, and the callitrichids. Mothers carry offspring almost 75% of the time throughout each infancy. Callimico fathers do practice considerable infant care-giving behaviors. However, they do so much less than Aotus, Callicebus, and callitrichid fathers. It appears that Callimico offspring are reared principally by their mothers. It turns out that this assumption is only partially true in terms of socialization of offspring by Callimico parents. Data in this dissertation show that fathers and daughters, and mothers and sons socialize more with one another than do fathers and sons, and mothers and daughters. Socialization of daughters by Callimico fathers appears to be unique to primates. An examination of the literature has not disclosed this parent-infant socialization strategy by any other primate. Although the owl monkey (Aotus trivirgatus), Barbary macaque (Macaca sylvanus), and siamang (Hylobates syndactylus) give birth to single infants and fathers carry infants for appreciable lengths of time, the data is unclear as to whether fathers spend more time with infant daughters or sons (Chivers et al., 1975; Dixson & Fleming, 1981; Taub, 1984). This opposite sex parent-progeny socialization tactic effected by mothers toward sons, and fathers toward daughters could better prepare young adult Callimico for a first-time pair bonding relationship leading to early reproductive success. In a rapidly maturing and short-lived primate such as Callimico, early and consistently successful reproduction is essential to species survival. Rapid physical development and early sexual maturation in concert with limited adolescent learning results in successful birthing of single infants and a successful life history strategy for Callimico. What does this strategy imply for 217 learned versus biological foundations of social behaviors that could be pivotal to the survival of a species? Callimico and Sociobioloav E. 0. Wilson (1975:4) defined sociobiology as, "the systematic study of the biological basis of all social behavior." Sociobiology strives to apply evolutionary theory to understanding social behavior by asserting that genetic variability resulting from natural selection controls animal social behavior. Sociobiology assumes that certain aspects of social behaviors are influenced genetically and that behaviors evolve because of selection for genotypes that are associated with reproductive success, i.e., fitness. Since sociobiology claims that, "natural selection is the agent that molds virtually all of the characteristics of a species" (Wilson, 1975:67), little attention has been paid to learned and environmental definitions of behavior. Wilson (1975:22) claims that, "behavior and social structure, like all other biological phenomena, can be studied as 'organs,' extensions of the genes that exist because of their superior adaptive value." Baldwin and Baldwin (1981), in a review and evaluation of sociobiological theory, present several nonhuman primate 218 behavior studies that cast doubt on the concept of a genetic foundation as the basis for all behaviors. The results of their analysis, "make it clear that past experience, local traditions, the local economics of resource utilization, and other nongenetic factors have a significant effect on primate behavior" (1981:10). Although some primate studies fit the sociobiological model, Baldwin and Baldwin (1981:11) argue that, "others do not . . . in addition, studies on other mammals and on birds reveal that the evolutionary model is not always appropriate for explaining the behavior of many advanced species." Baldwin and Baldwin conclude that, "there is an increasing awareness that direct environmental influences on behavior must be studied in order to account for the enormous variability in behavior" (1981:11). This appears to be the case for Callimico. Some Callimico social and reproductive behaviors are undoubtably under genetic control. The prohibitive costs of these behaviors to mothers created selection for partial participation in infant care-giving behaviors by fathers. But paternal care appears to vary greatly from male to male, suggesting that learning plays some role in the ontogeny of infant care-giving behaviors. This investigation has shown that primiparous fathers without previous experience carrying younger siblings in 219 their natal group do not carry their first-born offspring. They do interact with each infant as it reaches locomotor independence, and in this respect become successful parents. Although these young adult males do not carry their first offspring, they may later learn to carry future offspring. Variability of paternal care-giving behaviors seen in many human cultures is also common in the two South American cebid genera, Aotus and Callicebus, the callitrichids, and Callimico. The degree to which infant care-giving behavior manifests itself on an intraspecific level among these Neotropical primates (i.e., the monogamous/polyandrous mating species) appears to revolve around the number of available males and other infant care-giving helpers in the family group. There are analogies in paternal care between the mating systems of these nonhuman primates and humans (monogamy and polygyny) in which there are high levels of paternity certainty within a family structure with few adult males and other individuals (related nonreproductive care givers) (Taub & Mehlman, 1991). Several preindustrial human societies with monogamous or slightly polygynous mating systems exhibit high levels of paternal investment. In extended families (with nonreproductive care-givers in the group), there are associations between a high certainty of paternity and 220 marriage types (monogamy or polygyny), and high degrees of paternalism (Katz & Konner, 1981). One type of measurement that is common to both human and nonhuman primate paternal behavior studies is the amount of time adult males spend in close proximity to offspring. Katz and Konner (1981) did a cross-cultural survey of 80 preindustrial human societies looking for correlates between family structure, marriage styles, economic subsistence, and patterns of parenting. In 59% of these societies, fathers are rarely in close proximity to their offspring. Furthermore, only 4% of societies were characterized as showing close father-infant relationships (the highest percentage of father-infant close proximity and contact). In these societies (e.g., the South African SKung San), fathers account for no more than 6% of the direct parental care given to infants. Additionally, they spend only about 14% of their time directly interacting with infants. The data •from this dissertation show that in four of the 13 infant birth and development cycles, Callimico fathers carried newborn infants 0%-17% of the time (see Table 4). The infant carrying time by these four fathers is comparable to direct father-infant interactions in humans, as infant carrying can be seen as directly interacting with infants. Where Callimico and human fathers appear to differ most 221 regarding behavioral investment in offspring, is that Callimico fathers invest notably in the socialization of daughters. This directed behavior by Callimico fathers seems to be related to the reproductive success of young adult Callimico mothers. Because early reproductive success in short-lived organisms would seem to be essential, the directed performance of a fathers's behaviors toward his daughter appear directly related to the phylogeny of Callimico. Taub and Mehlman (1991) used the results of the Katz and Konner (1981) study to rank human males along Whitten's (1987) continuum of paternal investment in offspring by nonhuman primates. Taub and Mehlman think human fathers fall somewhere in the middle of Whitten's (1987) father- infant care-giving classifications ranking. The paternal investment seen in these preindustrial human societies is less than the father-infant intensive care-giving behaviors found in Aotus and Callicebus, the callitrichids, and Callimico, and is ranked on a level equivalent to mountain gorillas (Gorilla gorilla beringei). The mountain gorilla male does not usually practice comprehensive infant care- giving behaviors, but Whitten (1987:346) classifies the father-infant relationship as, "involving strong and enduring relationships." 222 The results of the Katz and Konner (1981) study, and to a limited degree the data from this dissertation, indicate that a certain level of father-infant care-giving behaviors in a small number of human societies positively covary with some of the father and infant behavioral interaction variables that operate in the monogamous/polyandrous Neotropical nonhuman primate species. Although these small bodied South American primates are distant phylogenetic relatives of humans, analogies can be drawn in regard to the quantity and quality of paternal care by these distantly related primates (Nicholson, 1991; Taub & Mehlman, 1991). Conclusions Callimico is a little studied primate in its natural habitat, which encompasses the upper Amazon basin of north- central South America. A small number of field investigations resulted in an equally small number of publications recording Callimico intragroup social behavior interactions. The primary difficulty of close study of Callimico in the wild results from the species' small size, cryptic coloration, and propensity for inhabiting a nearly impenetrable microhabitat. It is easier to study Callimico intragroup social behaviors in captivity. Publications have documented the pair bonding behaviors of adults, compared 223 the adult iviteractive behaviors of Callimico and the callitrichids, and compared the parenting behaviors of Callimico with the callitrichids (Carroll, 1985; Omedes & Carroll, 1980; Pook, 1978). No studies have looked at the dissimilar parenting behaviors of Callimico fathers and mothers and the results that differential performance of these behaviors have on the offspring after they reach sexual maturity and adulthood. Three hypotheses stated in Chapter I have a direct bearing on the reproductive success and resultant species survival of Callimico. The first hypothesis stated that accelerated physical and delayed behavioral maturation resulting in limited infant care experience, and single births are a successful reproductive strategy for young adult Callimico. The data show that Callimico physically develops and matures more rapidly than the callitrichids, but behaviorally matures more slowly than the callitrichids. This results in a lengthened infant but shortened adolescent life-history cycle for the species. Because Callimico gives birth to single infants as opposed to twinning in the callitrichids, there appears to be less need for nonreproductive infant care-giving helpers (adolescent siblings). Less need for juvenile and subadult siblings to supplement the cost of infant care-giving behaviors to 224 parents appears to have resulted in the shortened adolescent cycle of Callimico. The shortened adolescent cycle results in animals that are sexually mature at 12-15 months of age. An obvious cost of early maturity and dispersal from the natal group for young adult Callimico is less ICE that is apparently necessary for successfully rearing first-born infants. The second hypothesis specified that infant care-giving behavior experience is essential to skillful parenting in young adult Callimico. The data show that this is the case. Although of brief duration, young Callimico mothers require ICE from at least one subsequent sibling infancy to become skilled primiparous parents themselves. Fathers, on the other hand, seem to require ICE from two subsequent sibling infant development cycles to become skilled first-time parents. A primiparous father with experience from only one subsequent sibling infant development cycle did not carry his first-born offspring. Although the infant survived resulting in the father becoming reproductively successful, he did not carry the infant and thus reduce the costs to the mother who possibly just ended a postpartum estrus cycle and was again pregnant. Conversely, a young adult father with probable ICE from two subsequent sibling infancies did reduce the costs to his mate by carrying their first 225 offspring through the middle and end of its infancy. Although, he did not begin to carry the infant until the seventh week following birth, between weeks 7-12, he carried the infant 53% of the time. The third hypothesis stated that learned infant care- giving behaviors by yearling subadult Callimico are markedly different from a similar suite of behaviors in juvenile six- month-old siblings. The data show that a juvenile son is still being socialized by his mother following the birth of a subsequent neonate. Because mothers are interacting more with their sons than with their daughters and sons are interacting more with their mothers than with their fathers, juvenile males consistently find themselves in close proximity to the neonate. They, like juvenile females, are able to closely observe the newborn and the mother's infant care-giving behaviors, and perhaps interact with the neonate. As a subadult, following the birth of a second sibling, the behaviors of a Callimico male become noticeably different. Not only does he carry the newborn much more than juveniles, there is a profound difference in the number of behavioral interactions between the subadult male, and his father and mother carrying a newborn. 226 As a juvenile, the male interacted with his mother more than with his father in four of six close proximity and contact behavioral sequences. He significantly interacted with her more in three behavioral sequences; juvenile solicits parent to groom, parent grooms juvenile cf, and juvenile cf approach and sit-by parent. As a subadult, the male interacted with his mother more than his father in all six behavioral sequences. He significantly interacted with his mother more in five of the behavioral sequences; parent solicits subadult cf to groom, subadult cf grooms parent, subadult Mothers are the primary care-givers to newborn infants as they carry their offspring almost 75% of the time. This 227 behavior is less like Neotropical Aotus, Callicebus, and the callitrichids, and more like most New World cebids and Old World cercopithecids. However, following locomotor independence of offspring, fathers take a more active role in socializing their progeny. Fathers socialize more with daughters than do mothers, and mothers socialize more with sons than do fathers. These parent-offspring behavioral interaction preferences seem to be unique to Callimicor as no other primate fathers have been observed to principally socialize daughters. The results of socialization of offspring by opposite- sex parents could have a direct bearing on the later first pair-bonding and reproductive success of Callimico offspring after they become young adults. In an early maturing and relatively short-lived species such as Callimico, early and consistent successful reproduction is crucial to species survival. Several predictions can be made concerning the social and reproductive behaviors of this species that can only be verified by other long-term captive studies, or future comprehensive field studies. 1. Callimico mothers are more cebid-and cercopithecid- like (New and Old World monkeys) in their performance of infant care-giving behaviors than either Aotus and Callicebus, or the callitrichids. Following locomotor independence of offspring, Callimico fathers play a more active role in the socialization of their progeny. Fathers socialize more with daughters than with sons, and mothers socialize more with sons than with daughters. Socialization of offspring by opposite-sex parents prepares young Callimico to better adapt to a first time adult pair-bonding relationship with an unfamiliar partner. This social tactic is essential to expedite first-time reproductive success. Young adult Callimico females with ICE limited to one subsequent sibling infant birth and development cycle make successful first-time parents. Young adult Callimico males with ICE limited to one subsequent sibling infant birth and development cycle do not fulfill their responsibilities as skilled first-time parents by carrying their newborn offspring. Although previous infant carrying inexperienced primiparous fathers do not assist mothers in carrying the first-born during its development and dependence cycle, they become successful parents because mothers assume the primary responsibility for successfully rearing the newborn. 229 7. Following locomotor independence of their first-born offspring, primiparous fathers with limited ICE will interact with their offspring thus insuring the probability of successful socialization of young Callimico. As these predictions suggest, comprehensive long-term captive and/or field studies of Callimico are necessary to add to the body of knowledge concerning this little known, enigmatic primate. Although this dissertation has identified several mechanisms that are perhaps responsible for reproductive strategies and long-term survival of Callimico, several questions concerning Callimico morphology and behavior remain to be answered. 1. Why are newborn Callimico infants so similar in appearance to adults? Is the paedomorphism shown by young Callimico the result of the evolution of an efficient strategy for early attainment of adult morphology, which sees a rapidly maturing primate reaching adult mass more quickly if less morphological change is necessary to achieve adult status? Or, is the close resemblance of infants and adults related to some unknown behavioral artifact that is stimulated by the acute visual similarity of progeny and parents? 230 2. As close contact socialization of young females by Callimico fathers appears to be a social tactic meant to simplify an early and successful pair bonding relationship between a young adult female and an unfamiliar adult male, why isn't this strategy practiced by other monomorphic primate species that exhibit a similar social group structure? 3. Why are Callimico fathers so variable in their parenting behaviors? Are their behaviors idiosyncratic or do males require more learned ICE than females to skillfully supplement the infant carrying and care-giving costs to mothers? Until future investigations concerning behaviors of Callimico are completed, these questions will remain unanswered. At present, data in this dissertation describe the reproductive and parenting behaviors of a diminutive primate exhibiting the general morphology of a small-bodied callitrichid. However, it also demonstrates at least one parenting behavior that is unique to primates (fathers socialize daughters), and others that are more closely related to the parenting behaviors of larger-bodied cebids and cercopithecids. APPENDIX A GOELDI'S DATA SHEET GP#:______Date:______Time In:______Time Out:______Obs:_____ Behaviors (A) (B) (C) (D) Male Female Infant-1 Infant-2 Solicit groom A l l o g r o o m A u t o g r o o m Approach S Sit Pilo/Display Hopping Over Tail Over Ventral Tail Genital Mark Active Share Passive Share Reluctant Share Long Call Carrying Time COMMENTS: 231 APPENDIX B FIGURES The percentage of time by week infants independently locomote week 5 week 6 week 7 infants (0 27%) - infants (1 62%) infants (9 30%) mothers (43 58%) mothers (77.21%) ~ mothers (47 24%) fathers (54 80%) fathers (43 46%) fathers (I 52%) " | week 8 week 10 infants (7.11%)- infants (9.03%) infants (27 32%) mothers (47.47%) - mothers (51 38%) mothers (46 52%) fathers (45.42%) ~ fathers (39 59%) fathers (2616%) j week 11 week 12 week 13 infants (59.32%) ~ infants (64 47%) “ infants (66 36%) mothers (23.02%) “ mothers (24 97%) mothers (30 81%) fathers (17.67%)- 0 fathers (10.57%) a fathers (2 83%) 2 week 14 week 15 week 16 infants (65 07%) “ infants (92 98%) infants (96 48%) mothers (14.28%) - mothers (6.99%) 0 fathers (0 66 % )- mothers (3 54%) 0 fathers (0.04% J fathers i( (000%) Figure 1. Development of locomotor independence in Callimico infants. Average % of time by week following birth that 13 infants became independent of parents, and % of time parents carried infants during that time. First incidence of independent locomotion occurred in week 5. 232 233 Percentage of time all fathers and mothers carried all 13 neonates ill fathers carry 13 infants (25.46%) all mothers cany 13 infants (74.54%; Figure 2. Grand Totals: Infant Carry by Callimico Parents. Percent time fathers and mothers carried 13 infants. 234 Total infant carry time by week for 13 births: % time parents earned infants week 4 week 5 week 6 mothers (44.36%) mothers (87 67%) mothers (90 28%) fathers (55 64%) fathers (32 33%) fathers (9 72%) 4 J 4 week 7 weekB week9 mothers (53 34%) mothers (51.59%) mothers (60.01%) fathers (46 06%) I fathers (48 41%) 4 fathers (39.99%) 4 week 11 week 12 mothers (56 03%) mothers (05 73%) mothers (70 26%) fathers (43 97%) fathers (34 27%) - 4 4 fathers (29 74%) 4 week 13 mothers (85 49%) ~ fathers (14 51%) - 4 Figure 3. Grand Totals by Week: Infant Carry by Callimico Parents. Percent time by week following birth that fathers and mothers carried 13 infants. Father begins to carry in Week 4. 235 Infant carry by week for Group 1: % of time the parents carried the neonate week 1 week 2 week 3 mother (100 00%) mother (100.00%) mother (100.00%) father (0 00%) I father (0 00%) J father (0 00%) J week 5 week 6 week 7 mother (0.00%) mother (9.71%) mother (55 36%) father (100 00%) father (90 29%) fattier (44.64%) I 1 1 week10 week 11 mother (4 37%)* mother (12 48%) mother (31.48%) father (05 63%) - father (87 52%) father (68 54%) 1 1 1 week 12 week 13 mother (0.31%)' mother (6.08%) father (00 00%) - father (00 62%) 1 1 Figure 4. Infant Carry by Callimico Parents Group 1 by Week. Percent time by week following birth that each parent carried infant. No data was collected in weeks 4 and 8. 236 Infant carry by week 2nd birth, Group 5: % of time family carried 2nd infant unillf 4 HMIftlf H i u j w i Ij 45 WWJR e VrUwn w VrUUK w )uv. fatter (1.14%) mother (08 66%) — mother (97.68%) mother (100 00%) r(2.12% ) uiBalr 7 iiuuilf fl mftolr O TTWm « WUUK O VWUH 9 l e i s t e r (0 69%) mrfhor (95 07%) ^ B B mother (W 47%) father (4 04%) week 10 V * «fefar(0 41%) mother (95 06%) father (3 61%) Figure 5. Infant Carry by Week of Second-born Infant by Callimico Group 5 Parents and Juvenile Sister. Percent time by week following birth that parents and juvenile sister carried second-born infant. Juvenile sister first carries during Week 4, and only carries during weeks 4, 8, and 10. 237 Infant cany by week 1st birth, Group 5: % time parents carried 1st infant week 4 week 5 week 6 mother (90 00%) mother (75 09%) j mother (84.11%) ______father (50.00%) tether (24 91%) lather (15 69%) week 7 week 8 week 9 mother (97.19%)— mother (100 00%)- mother (100 00%) lather (2 81%) - week 10 week 11 mother (50 00%) mother (100 00%) father (50 00%) Figure 6. Infant Carry by Week of First-born Infant by Callimico Group 5 Parents. Percent time by week following birth that each parent carried infant. Father begins to carry infant during week 4 following birth. 238 Infant cany totals for all 2nd births % of time family carried 2nd infant juvenile siblings carry 2nd infants (0.53%)-| lathers carry 2nd infants (20.23%) mothers carry 2nd infants (79.24%; Figure 7. Infant Carry Grand Totals by all Callimico Parents and juvenile offspring. Percent time average that each set of parents and a juvenile carried 4 second-born infants. 239 Weekly infant cany percentage for the weeks when juveniles carried infants juvenile siblings cany 2nd infants 'athers carry 2nd infants (33.80%) mothers cany 2nd infants (64.81 % Figure 8. Infant Carry Weekly Average by all Callimico Parents and Juvenile Offspring. Percent time each week that each set of parents and a juvenile sibling carried 4 second-born infants. 240 Second-bom infant carry totals by week for all family group members *eek 4 Juveniles (2 60%) juveniles (1.36%) juveniles (1.18%) mothers (43 46%) mothers (97.40%) mothers (94 58%) fathers (55 36%) fathers (0 00%) fathers (4 06%) week 6 juveniles (1.65%) Juveniles (1 75%) Juveniles (1 63%) mothers (14.11%) mothers (46 43%) mothers (66.31%) fathers (M 24%) fathers (5182%) fathers (32 06%) Juveniles (0 43%) Juveniles (0 17%) juveniles (0 87%) mothers (61 16%) mothers (83.05%) mothers (91 66%) fathers (37.97%) fathers (16 52%) fathers (8 18%) Figure 9. Infant Carry Totals by Week for all Callimico Parents and Juvenile Offspring. Average percent time by week following birth that each set of parents and a juvenile sibling carried 4 second-born infants. Juveniles began to carry during week 3 following birth, and did not carry past Week 11. 241 Group 3, second-bom infant cany by father, mother, juv. male (Lew) week 4 week 5 week 6 Lew (1 44%) Lew (0 07%) Lew (0 58%) — mother (19 85%) — mother (56 97%) mother (9315%) father (79 57%) father (42.96%) father (5 41%) week 7 w eeks w eek9 Lew (3 61%) Lew (2 62%) Lew (018%) mother (25 30%) mother (47.15%) mother (60 76%) father (74 51%) father (50 23%) father (35.63%) week 10 week 11 Lew (0 87%) mother (71 35%) mother (61 42%) father (28 65%) father (37,71%) Figure 10. Infant Carry Totals by Week for Callimico Group 3 Parents and Juvenile Son (Lew). Percent time by week following birth that parents and juvenile son carried second-born infant. Lew did not begin to carry infant until week 4, and did not carry after week 11. 242 Group 3, 3rd-bom infant cany by father, mother, and subadutt (Lew) week 6 week 7 week 8 Lew (915%) motner (46 57%) Lew (57 90%)- Lew (75 97%) mother(1.55%) - father (44 28%) father (40 47%) - mother (2 91%) father (21 11%) week 9 week 10 week 11 Kfts (1.71%) Krti (2 87%) — Krto (2 70%) Lew (14 60%) — Lew (17.27%) mother (0 80%) Lew (44.33%) mother (21.90%) mother (1917%) father (79 24%) father (60 64%) father (34 80%) week 12 week 13 Kfts (2.69%; Kris (4 75%] Lew Lew mother mother father (60.58%) father (85 35%) Figure 11. Infant Carry Totals by Week for Callimico Group 3 Parents and Subadult Son (Lew). Percent time by week following birth that parents, subadult (Lew) and juvenile (Kris) siblings carried third-born infant. Lew did not begin to carry infant until week 6. 243 Group 3, juvenile (Kris) app/sit-toy subadult (Lew) when he carried infant week 6 week 7 K /feappt at~by lew (00 67%) M « l i * - b y L«w(83 33%) Lew app 0 el-by Km (1313%) Lew app 0 el-by Km (0.07%) w e e k 8 Km app 0 «t-by le w (91.30%) Km app 0 el-by le w (100.00%) lew app 1 H-by Km (0 70%) lew app & et-by Km (0 00%) week 10 week 11 Km app * el-by le w (00 00%) Km app & el-by lew (100 00%) lew app 4 el-by Km (20.00%) Lew app & el-by Km (0.00%) Figure 12. Callimico Group 3 Juvenile and Subadult Siblings Approach and Sit-by One Another while Subadult carried Infant. Percent time by week following birth that juvenile (Kris) approach and sit-by subadult (Lew) while he carried infant. Lew did not begin to carry infant until week 6. 244 The number of times by week that Group 3 passive shares with infant (Minnie) ■ 1 1 weekh 7 week 8 J week 9 V week 10 week 11 week i 12 week 13 m Minnie sol sh from Lew | | Lew share w/ Minnie Minnie sol sh from Jose m Jose share w/ Minnie m Minnie sol sh from Tina m Tina share w/ Minnie m Minnie sol sh from Kris Kris share w/ Minnie Figure 13. Callimico Group 3 Parents and Juvenile and Subadult Siblings Passive Share with Infant. Number of times per week that infant (Minnie) solicits passive shares from parents (Jose) and (Tina) and juvenile (Kris) and subadult (Lew) siblings, and number of times Jose, Tina, Kris, and Lew share with infant (Minnie). 245 Second-bom infant carry totals for fathers, mothers, juvenile daughters juvenile daughters (0.63%; mothers (84.21%; Figure 14. Infant Carry Grand Totals of Second-born Infants by Callimico Parents and Juvenile Daughters. Percent time average that each set of parents and a juvenile daughter carried 2 second-born infants. 246 The percentage of time by week that juv. females carried 2nd-bom infants week 3 week 4 week 5 tomato (1.53%) |uv tomato (0 34%) juv tomato (1.15%) mothart (59.70%) mathart (90 47%) mothart (99 00%) tothart (39 00%) w e e k 6 week 7 weekS jUV tomato (1 44%) juv tomato (0.30%) juv tomato (1.3t%) (51 02%) mothart (59 02%) mothart (72 40%) tothart (47 54%) (3907%) tothart (26.21%) week 10 juv tomato (0.27%) juv femalai ( 0 .22%) mothart (99 49%) mothart (90.28%) (1.50%) Figure 15. Infant Carry Totals by Week of Second-born Infants by Callimico Parents and Juvenile Daughters. Percent time by week that each set of parents and juvenile daughters carried 2 second-born infants during weeks when juveniles carried infants. Juveniles did not begin to carry until week 3 following birth, and did not carry past week 10. 247 The percentage of time the juv. female (Judy) carried the 2nd-bom infant Wujm W l \L oO week 4 week 5 Judy (2 60%) Judy (0 00%) Judy (1.92%) mother (34.46%) mother (97 40%) mother (100 00%) father (63 02%) father (0 00%) father (0 00%) week 6 week 7 week 8 Judy (2 69%) Judy (0 52%) Judy (1.47%) mother (8 58%) mother (37 03%) mother (64 00%) father (66 73%) father (62 44%) father (34 53%) week 9 week 10 Judy (0 50%) Judy (0 08%) mother (99 50%) mother (99 92%) father (0 00%) father (0.00%) Figure 16. Infant Carry Totals by Week Callimico Group 2 Parents and Juvenile Daughter (Judy). Percent time by week following birth that each parent and juvenile daughter (Judy) carried second- born infant during the weeks when juvenile carried infant. Juvenile did not begin to carry until week 3 and did not carry past week 10. 248 The percentage of time the juv. female (Prima) carried the 2nd-bom infant week 1 week 2 week 3 week 4 M m (1.14%) —j •L -m o lfw (100 OOX) • mathwOOOOOXI • ikO m t (100.00%) •<— mother l l t m i weeks week6 week 7 week 8 r— W h«r(312% ) r - « f » r (8 58%) P it™ (088% ) —i i— W h w (4 04%) ma8»r (87 M%>• —1 • ■- moDmOOOOOTHmothwiei.44%) • mothar (85 07%) • —1 week 9 week 10 week 11 week 12 r - M h w 10 S IX ) Pnm» (0 41%) —. M har (3 8 1 *) mother (00 47%)• - J mother (OS 06%) • - 1 • mother (100 00%) • mother (100.00%) week 13 week 14 week 15 week 16 +1— mothor (100 00%) m L- mathor (100 00%) m m ath* (100 00%) m •— moth«r(100 00%) Figure 17. Infant Carry Totals by Week: Callimico Group 5 Parents and Juvenile Daughter (Prima). Percent time by week following birth that each parent and a juvenile daughter carried second-born infant. 249 The percentage of time Group 5 family members carried the 2nd-bom infant Prima (0.14% H rfather (1.36%) mother (98.51 %] Figure 18. Infant Carry Grand Totals: Callimico Group 5 Parents and Juvenile Daughter (Prima). Percent time that parents and juvenile daughter carried second-born infant. 250 The percentage of time the Group 4 juv male (Antonio) carried 2nd-bom infant week 1 week 2 week 3 M o n lo (0 00%) Antonio (000%) Antonio (0 00%) mother (100 00%) 1 mother (100 00%) 1 mother (100 00%) 1 week 4 week 5 week 6 Antonio (0 00%) frtfortfo (0 00%) Antonio (0 00%) mother (SO 01%) mother (64 00%) mother (100 00%) father (40 00%) 1 r (15.64%) 1 1 week 7 weeks week 9 Antonio (0 00%) M o n o (0 00%) Antonio (0.00%) mother (20 80%) * (42,74%) mother (02 30%) lather (70.14%) father (57.26%) 1 1 father (37.70%) 1 week 10 week 11 week 12 Antonio (0 00%) M o n o (0 00%) Antonio (0 00%) mother (25 00%) father (100.00%) father (100 0 0 % ) ----- r(74.04%) 1 1 1 Figure 19. Infant Carry Totals by Week: Callimico Group 4 Parents and Juvenile Son (Antonio). Percent time by week following birth that each parent and juvenile son carried second-born infant. 251 The percentage of time the Group 4 father & mother carry 2nd-bom infant mother (Marie) (68.84%; Figure 20. Infant Carry Grand Totals of Second-born Infant by Callimico Group 4 Parents. Percent time father (Rob) and mother (Marie) carried second infant. 252 The percentage of time by week the Group 7 father (Pepe) carried infant week 7 weeks week 9 mother (17 33%) m other (51 05% ) mother (7500%) father (82 67%) lather (48 95%) father (25.00%) week 10 week 11 week 12 mother (28 59%) mother (44 73%) mother (63 87%) father (71 41%) father (55.27%) father (36 13%) week 13 mother (100 00%) Figure 21. Infant Carry Totals by Week: Callimico Group 7 Primiparous Parents. Percent time by week following birth that father (Pepe) and mother (Prima) carried first infant. Father did not begin to carry until week 7 following birth. 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