Laboratory Primate Newsletter

Interaction with Infants in a Captive Troop of Cebus Apella, by K. A. Leighty, G. Byrne, & S. J. Suomi...... 1

Optimizing the Laboratory Environment for Studying Animal Cognition, by A. R. Dickinson...... 4

The Monkey Cave: The Dark Lower-Row Cage, by V. & A. Reinhardt...... 8

Collaboration Between Field Primatologists and Biomedical Researchers, by J. E. Phillips-Conroy & C. J. Jolly...... 10

Forming a Bachelor Group of Long-tailed Macaques (Macaca fascicularis), by C. Asvestas & Michelle Reininger...... 14

Awards Granted...... 4
Primate Center Scientists Win Pediatric AIDS Award; Sabin Heroes of Science

Resources Wanted and Available...... 11
. . . Chimpanzee Breeding Colony; Reminder: WRPRC Audiovisual Archives; More Photos on CD-ROM; ABS Media Library; Gall Bladders and Bile; Hominidae Prostate Tissue or RNA

New Films on Macaques...... 13

Budongo Forest Project...... 15

Grants Available...... 16
. . . High Impact Research: Feasibility Studies; NIA Pilot Research Grant Program; NIAMS Small Grant Program for New Investigators; Vaccine Immunology Basic Research Centers; Research Supplements: Underrepresented Minorities; Reentry into Research Careers

Editors� Notes...... 18
. . . Mailing, E-mailing, and the Web; Five More Years!

Primates de las Américas...La Página...... 19

Information Requested or Available...... 20
. . . Knowing How to Practice Safe Science; Primates-Online Gets New Web Home; Live Primate Chat; WHO Library Digest for Africa; LOCATORplus; More Interesting Web Sites

Workshop Announcements...... 21
. . . Information Requirements of the Animal Welfare Act; Case Reports � Association of Primate Veterinarians

Research and Educational Opportunities...... 24
. . . Postdoc in Behavioral Psychopharmacology; Lincoln Park Zoo Funds Support Field Research; Bushbabies in Kenya; Animal Behavior

Meeting Announcements...... 25

Latin American Society of Animal Welfare...... 25

News Briefs...... 26
. . . 3.6 Million-Year-Old Hominid Find in South Africa; Souvenir Trade Threatens Rare Monkeys; Supreme Court Denies Review of Challenge; Multipurpose Retirement Home for Aged Primates; Monkeys Spread Terror in Abkhazia; Chimpanzee Biomedical Research Program; Gorilla Haven Hires Peter Halliday; Bayne Appointed to AVMA Committee; L.A. Monkeys To Get Paternity Tests; Ribbon Cutting at Retirement Reserve; Proposed Baboon Abbatoir, South Africa

Risk for Ebola Virus Infection in Côte d�Ivoire...... 36

Address Changes...... 13

Positions Available...... 22
. . . Animal Facility Supervisors, Georgia; Predoctoral Intramural Research Training Award; Postdoctoral Training in Comparative Medicine, MIT; Wildlife Waystation, California; Laboratory Animal Veterinarian, Minnesota; Animal Research Facility Manager, Washington, DC; Training and Development Officer, Georgia; Clinical Laboratory Animal Veterinarian, Duke

Recent Books and Articles...... 29

Interaction with Infants in a Captive Troop of Cebus Apella

Katherine A. Leighty, Gayle Byrne, and Stephen J. Suomi
Laboratory of Comparative Ethology, National Institute of Child Health and Human Development, NIH

For years researchers have examined the social relationships present in nonhuman primate species in order to provide insight into the origins of human social behavior. Past research has shown that many nonhuman primate species, including Cebus apella, a New World monkey, engage in a significant level of allomaternal care of their infants (Fragaszy, Baer & Adams-Curtis, 1991; Robinson & Janson, 1987). In addition, investigators have also begun to examine more closely the specific relationships that different troop members develop with infants.

Method

Animals: At the onset of this study in 1997, the social group of Cebus apella observed consisted of 20 animals (two adult males, four adult females, seven juvenile males, three juvenile females, two infant males, two infant females). By the completion of data collection in 1998, the troop contained a total of 22 members (two adult males, four adult females, nine juvenile males, three juvenile females, two infant males, and two infant females; see Table I). This troop was obtained by the National Institutes of Health�s Laboratory of Comparative Ethology in June of 1990 and was reported to have been formed 15 years previously. Two infants were observed in this study: Lyla, the female infant of Lee, was observed from birth to five weeks and 52 to 57 weeks of age; and Luther, the male infant of Lucy, was observed from five to 10 weeks of age.

-Othello - alpha male                     -Hamlet - adult male
-Lucy - adult female                      -Creepshow - juvenile male
   -Lee - adult female                    -Shinade - adult female
       -Lyla  infant female                -Shasta - juvenile male
               for Luther 5-10               -Squeak - juvenile male
   -Little Ricky � juvenile male             -Sagan - infant female
   -Liddy - juvenile male                 -Isabella - adult female
   -Lorena - juvenile female                 -Iko - juvenile male
   -Lexis - infant male for Lyla 0-5         -Ito - infant male for Lyla 0-5
            juvenile for Luther 5-10                juvenile for Luther 5-10
            and Lyla 52-57                          and Lyla 52-57 
   -Luther - infant male for                 -Isuzu - juvenile male
             Lyla 52-57                      -Ian - infant male for Luther 5-10
                                          -Mocha - juvenile female
                                          -Magic - juvenile female 

Social proximity               Animal is within the social space of the infant.
                               "Social space" is approximately 15 cm, or an arm�s
                               length of the animal.
Grooming Mother                Animal is grooming the focal infant�s mother 
                               while the infant is present.
Grooming Infant                Animal is grooming the infant.
Observing Infant               Animal is within the social space of the infant
                               and is peering at the infant.
Reaching for the Infant        Animal is within the social space of the infant
                               and is attempting to touch or grab the infant.
Touching the Infant            Animal is in physical contact with the infant,
                               but is not grooming, carrying, or engaging in 
                               playing behaviors.
Lip-smacking                   Animal is within the infant�s social space and
                               has its face within the infant�s line of sight,
                               but not in direct contact, and engages in a 
                               "kissing" behavior.
Carrying Infant                Animal is carrying the infant.  
Playing with the Infant        Animal is within the infant�s social space and is
                               engaging in species-typical play behavior (mock
                               fighting, wrestling, chasing, tumbling).

Byrne, G., & Suomi, S. (1995). Development of activity patterns, social interactions, and exploratory behavior in infant tufted capuchins (Cebus apella). American Journal of Primatology, 35, 255-270.

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Awards Granted

R. Paul Johnson and Julie Overbaugh, affiliate scientists at, respectively, Harvard Medical School and the University of Washington, were among four recipients of the 1999 Elizabeth Glaser Scientist Award, which recognizes outstanding, cutting-edge studies of pediatric HIV/AIDS.

On January 14, over 120 people braved an ice storm in Washington, D.C., to attend the presentation of the 1999 Albert B. Sabin Heroes of Science Awards by Americans for Medical Progress (AMP). The reception, held in the historic Cosmos Club, was attended by many public officials and entertainers as well as representatives of health advocacy organizations, the research and medical communities, and the pharmaceutical industry. Among the 1999 Albert B. Sabin Heroes of Science is Thomas B. Clarkson, DVM, Wake Forest University Bowman-Gray School of Medicine. For further information about the Albert B. Sabin Heroes of Science Awards, please contact AMP [703 836-9595; e-mail: [email protected]].

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Optimizing the Laboratory Environment for Studying Animal Cognition

At the XVIIth Congress of the International Primatological Society (1998) held in Antananarivo, Madagascar, a paper reporting the very first extended classification and control of extended serial order productions in brown capuchin monkeys (Cebus apella) was given in a session concerned with laboratory primate learning and cognition (McGonigle & Dickinson, 1998). During that presentation, we claimed that any cognitive program of research would require a novel long-term study environment conducive to the production of rich, individual monkey behavior graphs extending over long periods of time (years rather than months). Results to date have shown the first consistent and unambiguous demonstrations with nine-item size-seriation (akin to the standard Piagetian task in which the human child is required to arrange items of a random array in order of increasing size). These demonstrations not only reflect the success of Brendan McGonigle�s experimental research paradigm, but are also the result of the husbandry protocols and experimental procedures used in our laboratory. Indeed, the present paper claims that the colony management and husbandry procedures which have been used in the Laboratory for Cognitive Neuroscience have contributed greatly to an environment made optimal for demonstrating consistently high levels of cognitive functioning of a kind never before recorded for the nonhuman primate (Dickinson, 1997; McGonigle & Dickinson, 1994, 1998).

The Laboratory for Cognitive Neuroscience and Intelligent Systems is situated in the University of Edinburgh, Scotland, under the supervision of its founder and director, Dr. Brendan McGonigle. The Laboratory features converging comparative, developmental, and robotics approaches, with the specific objective of understanding the core design features of complex intelligent systems. Based on extended learning-to-learn episodes spanning many years, our program has radically extended the pioneering work of Harlow (1949). Eschewing the blitzkrieg studies which Harlow so rightly criticized, our experiments have tracked nonhuman primate subjects for over seven years with a series of tasks which are progressive in difficulty, enabling us to assess the cumulative effects of learning in novel ways. In doing so, we have had to develop entirely new methods of experimentation, first adapting paradigms from human cognition (McGonigle & Chalmers, 1977; McGonigle, 1987). Currently, in concert with Herb Terrace and his group at Columbia University, we have evolved touch-screen-based procedures, which enable us to devise explicit ordering tasks of a sort which have been previously impossible to implement using standard discrimination learning methods. Just as crucially, we have been able to provide an objective metric of task difficulty � based on the length of the sequence which subjects must learn. In short, the longer the sequence, the harder the task (although this is non-linear: see McGonigle & Chalmers, 1996).

Our Cebus apella colony derives from an initial group of six feral-born sub-adults (two male and four female), estimated from body weight, color, and dentition to have been between three and four years of age upon their arrival at the Laboratory. They were transported directly here from the south-east littoral of Brazil in 1988, specifically for the purpose of establishing an in-house breeding facility for longitudinal research work in comparative and developmental cognition. Following six months of strict veterinary quarantine, the females were quick to conceive, and have so far produced fifteen healthy youngsters, all of whom have survived. One advantage of establishing a colony in this way was that many of the environmental variables, which might otherwise confuse the interpretation of any behavior changes observed during the animal�s later development would be known. Such a personal history is rarely compiled for individual laboratory primates, and often the detailed hereditary, social, and circumstantial background of individual subjects remains unknown in many institutions. Health records are widely and routinely kept, but these do not offer enough detail to explain the occasional performance change which might be unrelated to difficulty of the experimental task. Such detailed information is especially important when interpreting failure with a given task. As might be the case with human developmental studies, such knowledge may reveal issues associated with social and family politics which might otherwise be missed and, indeed, prove to be of much explanatory value.

As long ago as the 1930s, Heinrich Kluver often attributed his experimental (and somewhat unusual breeding) successes with New World primates to his day-to-day husbandry and dietary practices (Kluver, 1933). Again, as with the human child, one should not expect isolated subjects living in sterile, featureless environments to be capable of demonstrating any normal developmental processes. Indeed, the ideal situation would be one in which observed changes in cognitive growth were solely the result of some experimental variable as determined in advance by the research design. For these reasons, among many others, every member of the monkey colony resident in our Laboratory enjoys what we suggest are the optimal conditions for high levels of individual physical and mental health, collective social welfare, and comfort. Such attention to the husbandry environment has, I believe, paid dividends, as seen by the high degree of co-operation seen with our monkeys: their voluntarily presenting for work daily (monkeys are not caught in nets or "crush-cages") and their consistent attention and orientation to tasks of increasing difficulty and complexity. Most important of all, changes reflecting the effect of traumas (e.g., deteriorating health, social withdrawal, lack of motivation or stimulation) will not go undetected. Such factors might otherwise confound our explanations of performance changes during the monkeys� behavioral development. This is especially relevant in cases which might involve the interpretation of experimental performance stability or sudden failure with a novel task. This latter scenario is typically interpreted as an animal�s reaching a "ceiling limit" of performance and has resulted in fewer subjects being reported upon than were actually used from the outset of many animal learning programs.

For their daily transfer to the experimental test-room (and for weekly weighing), the monkeys voluntarily enter a wheeled transit-enclosure directly from their adjacent home colony room. In keeping with our Laboratory philosophy of optimizing performance, the monkeys work at their tasks simultaneously in pairs, side by side, in an attempt to simulate their natural social foraging habits. As seen by the absence of the tics and stereotypies so often seen in singly housed monkeys, the social aspect of our working environment during testing appears to enhance the monkeys� comfort. As is typical of the experimental environments set up for working with the human child, this arrangement provides a supportive environment which promotes continued motivation and engagement with the increasing cognitive challenges of the experimental tasks. The female monkeys will typically work with their nursing offspring when they have them, and auditory contact with their family group is maintained throughout the experimental session. After each animal�s experimental session has ended (a maximum of one hour per day), attention may be given to the needs of any individual monkey before its otherwise immediate return to its colony room. Indeed, apart from voluntary attendance at the daily experimental session, a monkey very rarely leaves its family environment.

So far, the program has had an interesting yield. First, we have been able to study ordering and seriation behavior in prelinguistic primates. In the past, such capabilities have only been expressed via the use of language (in the case of human subjects), or by lifting and rearranging objects and placing them in a series, using the Wisconsin General Test Apparatus (Dickinson, 1997; Dickinson & McGonigle, 1996; McGonigle & Dickinson, 1996, 1998; McGonigle et. al., 1994). Second, this has revealed seriation capabilities which converge on those shown by children aged 6 or more (McGonigle and Chalmers, 1996, 1998; McGonigle, 1999). However, as with children, such ordering capabilities are not learned overnight; instead, the course of their emergence is very similar in the years of learning required (4 to 5 years). Third, the strong forms of relationally based "learning to learn" which we can now evaluate (see McGonigle and Chalmers, 1998, p. 522, fig. 22.9) suggest that there is no "glass ceiling" on the Cebus monkeys� ability to learn yet more complex tasks. Instead, the more experienced the subject, the quicker the learning of tasks of greatly increased complexity. This accelerating "learning to learn" process is the most powerful indicator yet that learning studied in the primate laboratory may reveal some of the core inductive mechanisms which signal both a distinctive shift in learning mechanisms in evolution, and provide the basis for both language learning and high level cognitive adaptive capabilities in man (McGonigle, 1999).

* * *

The Monkey Cave: The Dark Lower-Row Cage

Introduction

Small and medium-sized primates are commonly kept in double-tier cages to minimize the space necessary for their housing. The financial benefits of this caging system are very attractive, but are counterbalanced by serious shortcomings for the caged monkey.

* * *

Collaboration Between Field Primatologists and Biomedical Researchers

The recent report that HIV-1 can be traced to a particular subspecies of chimpanzee (Pan troglodytes troglodytes) has prompted a call for closer communication between biomedical scientists and field-workers in primatology. The call for fundamental epidemiological research on retroviruses in natural populations of nonhuman primates resonates with us. As primatologists, our research focus has been long-term study of two primate populations which live sympatrically in central Ethiopia: hybridizing olive and hamadryas baboons and grivet monkeys. We have been following these populations intermittently for more than 25 years. Each year when we conduct our fieldwork, we capture the animals and routinely take blood, body measurements and weights, dental casts, fecal samples and other useful biomedical and genetic information.

Jin, M. J., Rogers, J., Phillips-Conroy, J. E., Allan, J. S., Desrosiers, R. C., Shaw, G. M., Sharp, P. M., & Hahn, B. H. (1994). Infection of a yellow baboon with SIV from African green monkeys: Evidence for cross-species transmission in the wild. Journal of Virology, 68, 8454-8460.

* * *

Resources Wanted and Available

* * *

New Films on Macaques

* * *

Address Changes

* * *

Forming a Bachelor Group of Long-tailed Macaques (Macaca fascicularis)

* * *

Budongo Forest Project

* * *

Grants Available

* * *

Editors� Notes

* * *

Primates de las Américas...La Página

                           promedio         mínimo      máximo

Hemoglobina (g/dl)           14.29           11.7       17.9
Hematocrito (g/dl)           43.52           35         55
CMHB (g/dl en eritrocitos)   32.84           31.96      33.86
Reticulocitos (%)             1.32            0          2.4
Plaquetas (/m)          396,391         298,000    535,000
Leucocitos (/m)            8776.08        4200     13,600
Lifocitos (%)                27.60           12         58
Monocitos (%)                 0.17            0          3
Eosinofilos (%)               0.95            0          7
Basofilos (%)                 3.47            0         68
Segmentados (%)              67.47            0         88
Banda (%)                     0.21            0          2
Metamielocitos (%)            0.08            0          1
Mielocitos (%)                0               0          0
Promielocitos (%)             0               0          0
Blastos (%)                   0               0          0

G/dl - gramos por decilitro; /m - número por microlitro; % - porcentaje en la muestra

* * *

Information Requested or Available

· AALAS resource for IACUC members and staff: www.iacuc.org

· AWIC�s Selected Web Sites for Biomedical, Pharmaceutical, Veterinary, and Animal Sciences: www.nal.usda.gov/awic/pubs/awic9802.htm

· AWIC�s Selected Databases for Biomedical, Pharmaceutical, Veterinary and Animal Science Resources: www.nal.usda.gov/awic/pubs/selectdata/preface.htm

· Infectious Disease Web-link: pages.prodigy.net/pdeziel

· Swiss Tropical Institute: www.sti.unibas.ch/

* * *

Workshop Announcements

* * *

Positions Available

* * *

Research and Educational Opportunities

* * *

Meeting Announcements

* * *

Latin American Society of Animal Welfare

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News Briefs

Recent Books and Articles

Mitochondrial pseudogenes and phyletic relationships of Cebuella and Callithrix (Platyrrhini, Primates). Moreira, M. A. M., & Seuánez, H. N. (Genetics Section, Serv. de Pesquisa Básica, Inst. Nac. de Câncer, Praça da Cruz Vermelha 23, 20230-130, Rio de Janeiro, RJ, Brasil). Primates, 1999, 40, 353-364.
. . . Two cytochrome b pseudogenes were isolated from PCR-amplified products of Cebuella pygmaea DNA. These sequences showed insertions and deletions when compared to paralogous mitochondrial sequence regions of several primates. Phylogenetic analyses indicated that an ancestral pseudogene originated sometime before the divergence of Cebuella and Callithrix and that this sequence was later duplicated some 5.6 million years ago. Parsimony and distance analyses indicated that C. pygmaea and Callithrix species of the argentata group were more closely related to one another than any of them was to Callithrix species of the jacchus group, in agreement with previous analyses based on nuclear genes and karyotypic data. These findings also indicated that Callithrix is a paraphyletic genus, in agreement with previous propositions that Cebuella should be included within the genus Callithrix.

· Paternity determination in two groups of Eulemur fulvus mayottensis: Implications for understanding mating strategies. Gachot-Neveu, H., Petit, M., & Roeder, J. J. (J. J. R., Lab. d�Ethologie et Neurobiologie, URA/CNRS 1295, 7 rue de l�Université, 67000 Strasbourg, France). International Journal of Primatology, 1999, 20, 107-119.
. . . Random amplified polymorphic DNA was used to determine paternity in two groups of brown lemurs. The results were analyzed in relation to behavioral data on observed copulations, dominance relationships among adult males, and female behavior. The association between paternity determination and behavioral sampling shows that paternity determination is a crucial tool for understanding mating strategies and reproductive success in the studied species. In brown lemurs, dominance relationships between males are correlated with reproductive success, but male social dominance could be altered by female choice, as suggested by the ability of subordinate males to sire offspring in the presence of a dominant male.

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Risk for Ebola Virus Infection in Côte d�Ivoire

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All correspondence concerning the Newsletter should be addressed to:
Judith E. Schrier, Psychology Department, Box 1853, Brown University
Providence, Rhode Island 02912. [401-863-2511; FAX: 401-863-1300]
e-mail address: Judith_Schrier@brown.edu

Current and back issues of the Newsletter are available on the World Wide Web at
http://www.brown.edu/Research/Primate

ACKNOWLEDGMENTS

The Newsletter is supported by U. S. Public Health Service Grant RR-00419 from the Comparative Medicine Program, National Center for Research Resources, N.I.H.

Cover illustration of a slow loris (Nycticebus coucang bengalensis) by John Henry Drake (LABS of Virginia)

Copyright (c) 1999 by Brown University

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Last updated: June 19, 1999