Laboratory Primate Newsletter

VOLUME 23 NUMBER 4 OCTOBER 1984

CONTENTS

Articles and Notes

Do Monkeys Prefer to Give Birth on Weekends? by W. C. McGrew & E. C. McLuckie........1

On the Taub Case, by A. R. Morrison & P. J. Hand........4

Ethical Principles & Guidelines for Scientific Experiments on Animals in Switzerland........ 5

Trends in Primate Imports into the U.S.: 1983 and Comments on World Trade, by L. Gray-Schofeld & J. L. Chandler........9

News, Information, and Announcements

Research Opportunities in Chimpanzee Behavioral Studies at Vilab II, Liberia........8

Cartoon: Terrible Pun

Cartoon: Worse Pun

Departments

Recent Books and Articles ........14

* * *

Do Monkeys Prefer to Give Birth on Weekends?

W. C. McGrew and E. C. McLuckie
University of Stirling

Introduction

Birth in primates, both human and nonhuman, does not occur randomly but rather at regular intervals. Circadian periodicity is the rule, with those species active by day giving birth at night, and vice versa (Jolly, 1973). Annual periodicity is common, especially in habitats which undergo marked seasonal changes over the yearly cycle (Lancaster & Lee, 1965). Finally, there is some evidence, at least for prosimian primates, that reproduction may show lunar cyclicity related to levels of moonlight (Cowgill et al., 1962). All of these are natural cycles, and it is not hard to put forward adaptive reasons for births being timed accordingly.

The main aim of this article is to report another kind of periodicity in births, which though unnatural may be widespread. The finding was serendipitous and we are not aware of its being reported before. It is circum-weekly periodicity, i.e., differences over days of the seven-day week. A secondary aim is to encourage others working with primates in captivity to check their records for evidence of similar cyclicity.

Methods

The Primate Unit, Department of Psychology, University of Stirling, houses a breeding colony of two species of Callitrichidae, Callithrix j. jacchus and Saguinus o. oedipus. There are 3 families of the former and 4 families of the latter. These monkeys have lived here since June, 1982, and research is restricted to non-invasive, observational studies of intact nuclear families, under the direction of the senior author. Prior to that, from 1972-1982, the Unit housed a large colony of Macaca arctoides, with which both experimental and observational studies were done, under the direction of A. S. Chamove (Chamove, 1981). Experimental procedures included separation of infants from their mothers shortly after birth, hand-rearing, and upbringing in varying degrees of social restriction. For all 3 species, however, breeding was or has been highly successful, in terms of high rates of prenatal, perinatal, and neonatal survival.

Husbandry procedures over the week have been much the same throughout the existence of the Unit, with different routines for the working week and the weekend. On Monday through Friday, there are technical and research staff present over most of the day from 09.00 to 17.00 hrs. Most research and all cleaning and maintenance are done during these hours. Three meals are given, at morning, mid-day, and afternoon. On weekends, only feeding takes place, in one large meal given in the morning by one technician. (The exception to this occurred when neonatal macaques were being hand-reared, and a technician made short, regular visits to bottle-feed infants in the nursery). Research done on weekends is rare and sporadic. Heating and lighting schedules, on the other hand, remain constant. In summary, whereas routines during non-working hours do not vary over the week, there are notable differences between weekdays and weekends during working hours. On weekdays the Unit is busy and human-monkey interactions occur throughout the day; on week-ends the Unit is quiet and the monkeys are largely left alone.

To test the staff's impression that births occurred more often at weekends, the week was divided into weekends, i.e., 17.00 hrs on Friday to 09.00 hrs on the following Monday, versus the remainder of the week. All births so far in the Unit have occurred outside of working hours, i.e., overnight with newborns being found the following morning. This means that newborns found on Saturday, Sunday and Monday mornings were weekend births, and those found on Tuesday through Friday mornings were not. The expected probabilities of births are 3/7 for weekends and 4/7 for weekdays. Observed frequencies were tested against these using one-sample chi-squared tests. Callitrichids typically bear twins, but for the calculations, it was the event of birth rather than number of offspring which was used. Only naturally-timed births which resulted in at least one surviving offspring were included.

Results

Table 1 gives the results for the marmosets and tamarins born in the Unit. Each species shows the same pattern of births being concentrated at weekends: 69% of Saguinus o. oedipus and 73% of Callithrix j. jacchus. Given the similarity in cyclicity, the two sets of data were lumped and the result is a statistically significant difference: x2 = 8.40, df = 1, p < .0l. There is also an indication that within the weekend, births tend to be concentrated at the end, on Sunday nights: A third of newborns were found on Monday mornings.

-----------------------------------------------------------
                    Day of the Week
Species    Sat  Sun  Mon  Tues  Wed  Thurs  Fri  Total
-----------------------------------------------------------
Stirling
  C.j.j.    2    2    4    1     1     1     0    11
  S.o.o.    2    3    4    2     0     0     2    13
  Total     4    5    8    3     1     1     2    24
-----------------------------------------------------------
Aberystwyth
  C.J.J.   22   19   20   24    17    15    12   129
  S.o.o.    0    2    4    1     2     1     0    10
  Total    22   21   24   25    19    16    12   139
-----------------------------------------------------------
Stirling
  M.a.     11   16   15   12    16    14    11    95
-----------------------------------------------------------

Table I: Distribution of Births of Callithrix j. jacchus (C.j.j.), Saguin o. oedipus (S.o.o.), and Macaca arctoides (M.a.) Over the Week.

In order to pursue the apparent cyclicity in the Callitrichidae, we sought another, larger set of data from elsewhere. Sian Evans kindly supplied records of Callitrichid births over 10 years in the Department of Zoology, University College of Wales, Aberystwyth. Results for 129 Callithrix j. jacchus and 10 Saguinus o. oedipus births are given in Table 1. There is a suggestive trend toward births at weekends, but it does not reach statistical significance ( x2 = 1.44, df = 1, p < .25). Also, there is no skewing of births within the weekends, but the number of births seems to decline over weekdays.

Table 1 gives the results for the 95 stumptailed macaques born in the Unit. Contrary to the two species of Callitrichidae, it is obvious from inspection that there are no differences across days of the week ( x2 = 0.04, df = 1, p < .85). Only 44% of births occurred at weekends which is near chance level.

Discussion

No firm conclusions can be drawn from these data except that the phenomenon seems to deserve further study. We know of no other published findings on weekly periodicity of any sort in nonhuman primates, but preschool-aged children show day-to-day differences in free play over the working week (McGrew, 1972, pp. 210-211).

We believe that the following hypotheses are worth testing elsewhere, on larger samples:

a) The greater the difference between weekdays and weekends in the routine of a captive colony, the more births will be concentrated at weekends.

This can be falsified if the effect fails to occur under such conditions, or if it persists in colonies where routines do not vary over the week. In the (unlikely?) event of a colony being busier at weekends than during weekdays, a converse pattern is predicted.

b) The more "nervous", "sensitive" or "difficult" the species, the more likely the effect is to emerge.

If peace and quiet is the key, then the relief from disturbance should have the greatest effect on births in highly-strung forms. This would be falsified, for example, if Macaca mulatta showed a weekend effect, but Cacajao rubicundus did not.

c) The greater the difference between the routines of weekdays and weekend, and the more "nervous" the taxon, the greater the skew of births toward the end of the weekends; and the greater the skew toward the beginning of the working week.

If the onset of labor is to some extent psychosomatic then it should be most likely to occur when the animals are calmest. They should become more calm as the weekend progresses, and be most calm over Sunday night-Monday evening. If stress accumulates over the working week, monkeys will be most tense by Friday morning.

d) The more normal the rearing and housing conditions of the monkeys, the more likely the weekend effect is to emerge.

Given that reproductive failure (e.g., abortion, stillbirth) is more common in captive-born than wild-born females, the absence of normal conditions may also lead to onset of labor occurring at less than optimal times.

We look forward to hearing of the results of similar analyses from other colonies. If monkeys do prefer to give birth on weekends, this presents obvious inconveniences for perinatal and neonatal studies.

Acknowledgements

We thank Sian Evans for advice and additional data and Ian Rodgerson for his careful husbandry of the monkeys, and Arnold Chamove for critical comments on the manuscript.

References

Chamove, A. A. Establishment of a breeding colony of Stumptailed monkeys (Macaca arctoides). Laboratory Animals, 1981, 15, 251-259.

Cowgill, U. M., Bishop, A., Andrew, R. J., & Hutchinson, G. E. An apparent lunar periodicity in the sexual cycle of certain prosimians. Proceedings of the National Academy of Sciences, 1962, 48, 238-241.

Jolly, A. Primate birth hour. International Zoo Yearbook, 1973, 13, 391-397.

Lancaster, J. B., & Lee, R. B. The annual reproductive cycle in monkeys and apes. In I. DeVore (Ed.), Primate Behavior. New York: Holt, Rinehart & Winston, 1965.

McGrew, W. C. An Ethological Study of Children's Behavior. New York: Academic Press, 1972.

---------------------------------------------------

Authors' address: Department of Psychology, University of Stirling, Stirling FK9 4LA Scotland.

---------------------------------------------------

* * *

On the Taub Case

Adrian R. Morrison and Peter J. Hand
University of Pennsylvania

In the article by Jeffrey L. Fox "Animal rights bill defeated in California" (Science, News and Comment, 29 June, p. 1414), a misleading subheadline states, "meanwhile HHS upholds NIH halting Taub's grant because of animal misuse." The fact is that the Department of Health and Human Services (HHS) board found that the animals had not suffered misuse and that their condition was not due to inadequate veterinary care, but was a consequence of the experimental procedure, as stated later in the article. The board faulted Edward Taub's institute, IBR, for not ensuring regular visits by an attending veterinarian. Because there had been no problems in his small, stable colony, Taub had not found such assistance necessary. Taub's belief that he was providing adequate care was reinforced by the generally positive reviews given his laboratory by the U. S. Department of Agriculture veterinarian who inspected his laboratory 15 times during the period in question.

Also, Fox states that "The narrowly based HHS decision sidesteps the question of whether Taub's research is worth continuing..." The importance of his research was simply not an issue. In fact, the decision explicitly states that "both NIH and the scientific experts who testified on behalf of the PI {principle investigator, Taub} at the hearing agreed that the studies were important and had valuable clinical implications."

On the basis of knowledge we have gained as expert witnesses for the defense in two court trials--in an appeal before a Public Health Service board and in the HHS hearing--we can make one thing immediately clear. The harshness with which the National Institutes of Health dealt with Taub depended in large measure on their belief that his monkeys had, indeed, suffered maltreatment at his hands. This opinion stemmed from the results of physical examinations made by two zoo veterinarians flown in by People for the Ethical Treatment of Animals. These veterinarians interpreted the conditions seen in some of the deafferented limbs as if they were present in physiologically normal limbs.

Unfortunately, NIH officials did not include someone with the expert opinion necessary to evaluate the conditions of the monkeys' limbs on the review committee that voted to suspend Taub's grant in 1981. In future cases, it is imperative that NIH be assured that it has benefited from the same degree of expert opinion in arriving at a decision to suspend or terminate a grant as it did when awarding a grant. We remain convinced that, had this been done in Taub's case at the outset of the proceedings, he would not have received such harsh treatment at NIH's hands and would have had NIH's support rather than its opposition at his court trials.

---------------------------------------------------

Authors' address: Department of Anatomy, School of Veterinary Medicine, University of Pennsylvania, 3800 Spruce St., Philadelphia, PA 19104.

From the "Letters" section of Science, 1984, 225.

---------------------------------------------------

* * *

Ethical Principles and Guidelines for Scientific Experiments on Animals in Switzerland

Preamble

These present guide-lines issue from the recognition that man, in his need to solve the problems of his existence, cannot dispense with experimentation on animals, while on the other hand the ethical principle of reverence for life lays upon him the charge of protecting animals.

They reflect the conviction that scientists, as responsible members of the community, should of their own accord devise, implement, and ensure the observance of the measures necessary to achieve the optimal resolution of this conflict.

The Swiss Academy of Medical Sciences and the Swiss Academy of Sciences have therefore jointly formulated the following Ethical Principles and Guide-Lines for Scientific Experiments on Animals, which were adopted at the meetings of their Senates in the spring of l983 and are to serve as a code of conduct for all scientists and members of allied professions practicing in Switzerland.

I. Legal Bases

1.1 The Swiss Animal Protection Act of March 9th, 1978 lays down principles (Article 2) for the treatment of vertebrate animals, according to which: no person may, without justification, inflict pain, suffering, or injury upon an animal, or cause it fear.

In Section Six, conditions governing experiments on vertebrates are set forth; according to Article 12, "experiments on animals" are to be construed as: any procedures in which live animals are used for the purpose of testing a scientific theory, acquiring knowledge, obtaining or testing a substance, or determining the effect of a particular procedure on the animal, as well as any use of animals in experimental behavioral research.

Articles 13 and 14 contain statutory regulations according to which: experiments which cause the animal pain may not be performed without permission from the authorities and must be limited to the essential minimum.

1.2 Scientists are under obligation to conduct experiments on animals in conformity with the Act and the appurtenant Statutory Regulations of May 27th, 1981. These legal provisions, however, admit of considerable latitude in their interpretation, which has to be narrowed, on the one hand by the authorizing bodies and the organs of jurisdiction and, on the other hand, by scientists themselves within their own responsibility.

II. Ethical Principles

2.1 Being endowed with the faculties of reason and reflection, man is answerable for his actions. In these actions, it is his duty to seek the greatest good of all concerned. Life confronts man with ineluctable problems, to solve which, failing ready resources, he must contrive to augment the range and the fullness of his knowledge. At the same time, it is also man's duty to respect, to preserve, and to care for the gifts of nature, and the ethical principles of reverence for life demands that man should protect his fellow-creatures, the animals.

2.2 Experimental investigations in animals are often of decisive importance for the understanding of vital phenomena. They represent a particular form of man's age-long practice of using animals for the sake of his own self-preservation and welfare. Knowledge acquired through experimentation on animals is of service to man in protecting life, in alleviating suffering, and in ensuring his survival. The right claimed by man to use animals is, however, inseparable from the duty to avoid abuse of that right.

2.3 The ethical problems of experimentation on animals arise from the conflict between the endeavor to realize the above-mentioned human values, on the one hand, and ethical principles such as reverence for life and abstinence from acts inflicting pain and suffering, on the other hand. This conflict is unavoidable: it can only be responsibly settled by weighing the mutually opposing values.

2.4 The ethical principle of reverence for life of man and animals demands, in particular, that experiments on animals should be restricted as far as possible, without, however, denying man the fulfillment of his own claims to security.

III. Ethical Requirements for the Legitimation of Experiments on Animals

3.1 The requirement that experiments on animals must be justifiable on the grounds of greater good imposes upon scientists the duty of adducing proof of the necessity and the suitability of each experiment to be performed.

3.2 The more essential is the knowledge to be gained from experiments on animals and the greater its import for the upholding of human values, the more plainly justifiable are such experiments: to protect human life and to mitigate severe suffering are not merely prerogatives that man may exercise, but obligations he must fulfil.

3.3 The greater the suffering an experiment is apt to inflict upon an animal, the more acute becomes the question of its justifiability.

3.4 Experimentation on animals must conform to the established principles and precepts of science. In particular, the results sought must extend clearly beyond the confines of present knowledge, the assumption to be tested must be reasonable, and the procedure chosen must be likely to achieve success and be consistent with the existing state of research.

3.5 Experiments on animals which are of direct and readily perceptible benefit to the life and health of man and animals are ethically legitimate. These include experiments directed towards prophylactic, diagnostic and therapeutic ends in medicine, or serving the interests of safeguarding against dangers. Experimental investigations in human beings can, in many fields, only be performed if they are warranted by the results of experiments on animals. *.

3.6 Experiments on animals are ethically legitimate if--even without being of immediately appreciable benefit to life and health--they serve the end of acquiring new knowledge, for instance if they can in all probability be expected to contribute significantly to our knowledge of the make-up, function, and behavior of living creatures.

3.7 Experiments on animals which under the Animal Protection Act require official authorization are ethically legitimate as part of the curricula of universities and other institutes of higher learning for students of medicine, dental surgery, veterinary medicine, pharmacy, and biology, and in the vocational training of laboratory technicians and paramedical staff, provided that no alternative possibilities exist for them to acquire the necessary, more profound understanding of vital phenomena, or be trained in the skills needed for the performance of experiments.

3.8 Experiments on animals are not ethically legitimate if sufficiently conclusive alternative methods exist of acquiring the knowledge sought. Experiments on animals which have already been competently performed may not be repeated without adequate grounds.

IV. Ethical Requirements for the Conduct of Experiments on Animals

4.1 The ethical principle of reverence for life demands that the greatest possible gain in knowledge should be achieved at the cost of the fewest possible experiments and animals, and the least possible suffering of the latter.

4.2 It is the duty of all persons participating in experiments on animals to be heedful to the well-being and assure the least possible suffering of the experimental animals. The decisive criterion on which the fulfillment of this duty depends is their professional competence and express acceptance of their responsibility towards the animal.

4.3 Experiments apt to inflict pain must be performed under general or local anesthesia, unless anesthesia is precluded by the purpose of the experiment.**

4.4 If pain, suffering, or fear are inevitable accompaniments of an experiment, all possible measures must be taken to limit their duration and intensity to the essential minimum. The animal must be able to give expression to its sensations and, whenever possible, able to avoid painful stimuli. For this reason, the use of paralysant substances without narcosis is forbidden.

4.5 In all experiments which lead to chronic suffering or necessitate repeated interventions, every possible measure must be taken to mitigate suffering and to dispel anxiety. It is particularly important in such cases that the animal should be carefully accustomed to the experimental conditions and cared for in the proper fashion before, during and after the experiment.

4.6 Experiments apt to cause the animal severe suffering must be avoided by modifying the hypothesis to be tested in such a way that other criteria of the successful conclusion of the experiment can be applied, or by forgoing the anticipated gain of knowledge. Severe suffering is to be construed as any state which in man would be qualified as unbearable without palliative measures.

4.7 Continued physical restraint must only be resorted to after other procedures have been considered and found wanting. All possible measures must be taken to alleviate anxiety, including in particular careful and gentle accustoming of the animal to the experimental conditions.

4.8 Animals on which experiments are to be performed should, as a rule, originate from special laboratory-animal breeding units. Animals of unknown origin must not be used. Particular reservation is called for in the case of species living in the wild. Experiments on species threatened with extinction are only justifiable if they contribute towards the preservation of those species.

V. Responsibilities

5.1 The scientific, moral, and legal responsibility for the legitimation, planning, and performance of experiments on animals is borne by the scientist-in-charge. All other persons participating in the experiment share the moral responsibility; they must therefore have complete freedom to voice their opinions and, if need be, refuse their cooperation.

5.2 In consequence of his insight and within the bounds of his knowledge, each individual scientist is responsible for ensuring that, within his own sphere of influence, the Animal Protection Act and the present guide-lines are duly observed.

5.3 It is the duty of all scientists to take and to support all conceivable measures towards the restriction of experiments on animals, in particular through the development of alternative methods and the constant improvement of test systems in order to augment the relevance and validity of experiments on animals. It is their further duty to contribute towards the avoidance of unnecessary experiments on animals by promoting the development and operation of information systems and data banks as well as appropriate means for the communication of the results of experiments on animals, including those of experiments with a negative inconclusive outcome.

5.4 Scientists are duty-bound to subject to constant, critical scrutiny the relevance and validity of experiments on animals stipulated by existing legal provisions enacted to protect mankind from danger, and, whenever necessary, to use their best resources to bring about amendments to these regulations.

5.5 Scientists are urged to exploit the findings of behavioral research in order to hasten the development of new experimental strategies which, in experiments causing pain and anxiety, could diminish or eliminate the animal's perception of pain.

5.6 It is the duty of scientists and of institutions for the advancement of science constantly to promote the training of persons participating in experiments on animals, to oversee their knowledge and capabilities in an appropriate manner, and to instill, during their tuition, into students of the disciplines entitled to conduct experiments on animals a sense of their ethical responsibility.

5.7 It is the duty of the institutions for the advancement of science to deny their support to experiments on animals which contravene the ethical principles and the present guide-lines. Scientific journals are urged not to accept the results of such experiments for publication.

5.8 The Swiss Academy of Medical Sciences and the Swiss Academy of Sciences consider it, in particular, their permanent duty to review the adequacy and validity of legal texts and provisions, as well as of their own ethical principles and guide-lines in the light of the existing state of science and to foster among the general public the assumption of a more critical attitude towards the claims for welfare and security of which experiments on animals are a consequence

---------------------------------------------------

From the ICLAS Bulletin, No. 53, December 1983.

* Cf Article II.3 of "Richtlien für Forschungsuntersuchungen am Menschen", published by the Swiss Academy of Medical Sciences, December 1st, 1970.

** Animal Protection Act, Article 16.2.

---------------------------------------------------

* * *

Research Opportunities in Chimpanzee Behavioral Studies at Vilab II, Liberia

Vilab II, the Liberian Institute for Biomedical Research, Robertsfield, Liberia, a field laboratory of the New York Blood Center, is engaged in an experimental program concerned with rehabilitation, and release to the wild, of chimpanzees which have participated in hepatitis B vaccine studies. Animals which are in good health and free of recognizable infections are resocialized into large groups within our colony, and then for a period of a few years on large islands. Groups of about 20 such animals will then be released into National Park areas having low existing chimpanzee populations. The success of the program will be assessed by aerial and on the ground telemetry and direct on the ground observation.

This program offers research opportunities for graduate students, or research fellows, interested in various aspects of chimpanzee behavior.

Applications from those interested should be addressed to Dr. Alfred M. Prince, The Lindsley F. Kimball Research Institute of the New York Blood Center, 310 East 67th Street, New York, N.Y. 10021. Please send C. V. and outline of research interest and plans. Funding or fellowship support to cover travel and subsistence in the field must be provided.

* * *

Trends in Primate Imports into the United States: 1983 and Comments on World Trade

Lynn Gray-Schofield and Jeri Lynn Chandler
TRAFFIC (U.S.A.), Washington, DC

The decline in primate imports into the United States reported in previous years (Mack, 1982, 1983) is still occurring; imports during 1983 decreased by 21 percent, from 16,651 animals in 1982 to 13,148 in 1983. Trade bans and restrictions implemented by several major supplying countries over past years appear to have affected both the number and species of primates imported by the United States and other importing countries. At the same time captive-breeding and placement programs have increased, helping to ensure adequate supplies of primates for research.

U.S. Trade

Figures from the U. S. Department of Commerce show that from 1980 through 1982, the United States imported a total of 62,132 primates; 23,024 in 1980; 22,457 in 1981; and 16,651 in 1982 (Mack, 1981, 1982, 1983). Of these, 60 percent were imported from Asia.

Data from annual reports filed by the Fish and Wildlife Service under the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES Annual Reports, 1980, 1981, 1982) show that the long-tailed macaque (Macaca fascicularis) from Asia was by far the most commonly imported species between 1980 and 1982, accounting for 62 percent of total U. S. primate imports. The United States increased its imports of long-tailed macaques from the Philippines, Indonesia, and Malaysia following India's export ban of rhesus macaques (Macaca mulatta) in 1978 (Mack, 1982). During the early 1970s the rhesus macaque was the species second most commonly imported into the United States, averaging 22,870 animals per year; the squirrel monkey, imported primarily for the pet trade, was the most commonly imported species, averaging 26,980 animals per year (Paradiso & Fisher, 1972; Clapp & Paradiso, 1973; Clapp, 1974).

Other species imported into the United States in large numbers between 1980 and 1982 included the squirrel monkey (Saimiri sciureus), 9 percent of total primate imports; green monkey (Ceropithecus aethiops), 9 percent of imports; red-bellied tamarin (Saguinus labiatus), 6 percent of imports; baboon (Papio spp.), 3 percent of imports; and rhesus macaques (Macaca mulatta), 2 percent of imports.

Placement and Captive-Breeding Programs

With fewer numbers of wild primates available for importation, researchers are relying more often on captive-bred and "recycled" animals (Mack, 1983). The increase in recycling of primates is demonstrated by figures from the Primate Supply Information Clearinghouse (PSIC) at the University of Washington, Seattle, which provides a placement service for surplus primates held by U. S. research facilities.

The number of primates placed by the PSIC has increased steadily since its first year of operation in 1978, when 2,649 primates were placed. In 1983 the PSIC placed 7,135 live primates, representing a 29 percent increase in placements over the previous year. During 1982 and 1983 rhesus macaques were placed most frequently, followed by squirrel monkeys, marmosets and tamarins (Callitrichidae), and African green monkeys.

In addition to efforts by the PSIC, U. S. captive-breeding programs have helped offset the decreased availability of wild primates. The primate export ban implemented by India in 1978 created an immediate shortage of rhesus macaques in the United States (Mack & Eudey, in press). Since then, breeding programs have emphasized the production of this species over others still available from wild sources (Mack, 1982).

In 1978, 5,093 primates were produced in U. S. captive-breeding programs, including 3,518 rhesus macaques (Gerone, 1980). By 1983 captive breeding for all species, and for rhesus macaques in particular, increased by 78 and 96 percent, respectively. (The number of rhesus born in captivity in the U. S. in 1983 was 6,893). Other species produced in U. S. captive-breeding programs include squirrel monkeys, baboons, long-tailed macaques, and owl monkeys (Aotus trivirgatus).

Number of Primates Used in Experimentation

Although the availability of wild primates has decreased over the past several years, the number of primates reported to be used in experimentation has remained relatively stable since 1978, averaging over 55,000 animals per year. The percent of primates used compared to the total number of guinea pigs, hamsters, rabbit, dogs, and cats used in experimentation has also remained steady at an average of 3.3 percent per year.

World Trade

While the Unted States is the largest consumer of primates in the world, 13 other countries accounted for over 90 percent of the remaining primates used in biomedical and pharmaceutical research worldwide (Caldecott & Kavanagh, in press). Listed in order of decreasing usage they are: the United Kingdom, Taiwan, Japan, France, South Africa, Canda, the Federal Republic of Germany, the Soviet Union, Italy, the Netherlands, Sweden, India, and China. Outside the United States, an estimated 50,000 primates were used annually in biomedical and pharmaceutical research from 1977 through 1982 (Caldecott & Kavanagh, in press).

The predominant use of primates in these countries is in the production and testing of pharmaceuticals, a practice that requires constant replacement of animals, either from captive-bred or wild sources. Old World species, primarily green monkeys, long-tailed and rhesus macaques, patas monkeys (Erythrocebus patas), and baboons, account for most of the primates used by researchers outside the United States. The most commonly used New World species are common marmosets (Callithrix jacchus), cotton-top tamarins (Saguinus oedipus), and squirrel monkeys (Saimiri sciureus) (Caldecott & Kavanagh, in press).

The same trade bans that have apparently affected the U. S. primate trade could also be responsible for restricted supplies and inflated prices of wild primates for researchers worldwide, creating a similar need for captive-breeding programs. Although researchers continue to rely on wild populations to satisfy 80 to 90 percent of their demand, captive-breeding programs have been established in all major user countries except for South africa and Taiwan (Caldecott & Kavanagh, in press). In the later 1970s and early 1980s, approximately 4,000 to 5,000 primates were produced annually for research outside the United States (Caldecott & Kavanagh, in press). Species involved in foreign captive-breeding programs include common marmosets, macaques (Macaca mulatta, M. fascicularis, M. fuscata, and M. sylvanus), baboons (Papio spp.), green monkeys (Cercopithecus aethiops), saddle-back and cotton-top tamarins (Saguinus fuscicollis and S. oedipus), and chimpanzees (Pan troglodytes).

In 1975 the National Institutes of Health (NIH) entered into an agreement with the Pan American Health Organization (PAHO) that led to the establishment of a primate-breeding station in Iquitos, Peru (Eudey & Mack, in press). The goals of this program are to develop viable primate conservation programs in Peru and to increase captive-breeding efforts for several species. The program has been most successful in producing squirrel monkeys, and headway is now being made into the breeding of Aotus species (T. Wolfle, Interagency Primate Steering Committee, NIH, Bethesda, Maryland, personal communication, 1984). In 1983 the United States imported 358 primates (mostly squirrel monkeys) from Peru's management program (T. Wolfle, Interagency Primate Steering Committee, NIH, Bethesda, Maryland, personal communication, 1984), including both captive-bred and wild-caught primates. Population levels of primates taken from the wild are monitored regularly as part of the management program (R. Mittermeier, World Wildlife Fund--U. S., personal communication, 1984).

Trade Restrictions

Analysis of the primate trade shows that only a few countries supply the primates needed worldwide. In 1979, nine countries supplied 92 percent of all primates in trade (Table 1). The United States and the Netherlands, two of the major primate exporters, should not be considered primary sources since both countries re-export a large number of animals originating in Latin America, Africa, and Asia. Because only a small number of countries supply most of the wild primates in trade, trade bans or restrictions imposed by source countries can have significant effects on worldwide supplies of wild animals.

-------------------------------------------
Country of       Number of     Percentage
Export       Primates Exported  of Total
-------------------------------------------
Indonesia        17,907          27.6
Malaysia         12,199          18.8
Kenya             9,519          14.6
United States     5,229           8.0
Philippines       5,225           8.0
Bolivia           5,203           8.0
Ethiopia          1,848           2.8
Netherlands       1,405           2.2
Somalia           1,216           1.9
Other*            5,231           8.0
-------------------------------------------
TOTAL            64,982
-------------------------------------------
*Includes 50 countries each accounting for less than 2 percent of estimated world exports.
SOURCE: M. Kavanagh, in press.

TABLE 1. Estimated World Primate Exports, 1979

Beginning in the late 1960s, U. S. as well as world-wide trade was critically affected by several trade bans instituted by major supplying countries (Mack, 1983). Brazil banned all wildlife exports in 1967, which reduced trade in marmosets, tamarins, and squirrel monkeys. Bangladesh banned the export of primates in 1973 and India followed in 1978, severely limiting the number of wild rhesus macaques in trade. In 1974, a year after Peru restricted primate exports, Colombia suspended trade in live native wildlife. As a result, U. S. sources of New World species shifted from Peru and Colombia to Paraguay and Panama. However, these two countries subsequently banned exports in 1975 and 1979, respectively. Thailand banned exports of macaques in 1975 and of tree shrews in 1981, and trade in both species subsequently shifted to Malaysia.

As the last major source of New World species, Bolivia was an erratic supplier of primates in 1983. U. S. researchers report that it was difficult to obtain monkeys from Bolivia during most of 1983 (T. Wolfle, Interagency Primate Steering Committee, NIH, Bethesda, Maryland, personal communication, 1984). In fact, from 1982 to 1983 U. S. imports from that country decreased 48 percent, from 3,369 to 1,743 animals (Table 1). Effective May 1, 1984, Bolivian officials imposed a 1-year ban on the export of live wild animals (Ministerial Resolution No. 85/84, CITES Secretariat, Gland, Switzerland, Notification to the Parties No. 300, May 30, 1984).

Although U. S. primate imports from Kenya have declined over recent years, Kenya remains an important source for African primate species. Despite information reporting that in 1981 Kenya suspended all exports of primates, allowing only exports of stockpiled animals (Mack, 1983), the CITES Secretariat, Gland, Switzerland (personal communication, 1984), states that Kenya has never implemented a ban on trade in baboons, vervets, or bushbabies. Section 26 of Kenya's Wildlife (Conservation and Management) Act provides special authorization to hunt for scientific purposes. Consistent with this latter information, the United States continues to import baboons and green monkeys from Kenya, but the number imported has decreased significantly from 1,195 animals in 1981 to 393 in 1983 (Mack, 1982; Table 1).

In addition to Bolivia, Malaysia is the only other country that has imposed a trade ban since Mack (1983) published a list of countries banning primate exports. Effective June 15, 1984, Malaysia, a major primate exporter in 1979, discontinued exports of long-tailed and pig-tailed macaques (Macaca fascicularis and M. nemestrina) for a period of 5 years (CITES Secretariat, Gland, Switzerland, Notification to the Parties No. 294, May 18, 1984; Wildlife Trade Monitoring Unit, 1984). According to information that the CITES Secretariat received from Malaysian officials. Malaysia's ban does not include tree shrews. When Thailand banned the export of tree shrews in 1981, Malaysia became the primary source of tree shrews for U. S. researchers.

In addition to these trade restrictions and bans, other factors have contributed to the decrease in U. S. primate imports. These include the 1975 U. S. Public Health Service regulation banning the import of primates for the pet market, which affected U. S. trade in New World species, and implementation of the U. S. Endangered Species Act in 1973 and CITES in 1975, both of which limited trade in certain species.

Conclusion

Primate imports into the United States have declined steadily since the late 1960s. The number of primates imported in 1983 represented more than an 80 percent decrease since 1973. This decrease might continue, because more and more countries are implementing export restrictions and bans to protect their indigenous primate populations. These bans have not seriously hampered U. S. research efforts because the number of primates used in experimentation as remained fairly constant over the past 10 years and the increase in domestic breeding programs and recycling of experimental animals have offset the reduced availability of wild primates. The demonstrated increase in U. S. captive-breeding and placement programs should help ensure an adequate supply of primates for researchers.

References

APHIS (Animal and Plant Health Inspection Service), 1979-1984. Animal Welfare Enforcement, Reports for FY 1978 through FY 1983. Washington, DC: U. S. Department of Agriculture.

Caldecott, J., & Kavanagh, M. Captive breeding and the use of primates outside the United States. In D. Mack & R. Mittermeier, Eds., The International Primate Trade. Washington, DC: World Wildlife Fund--U.S., in press.

CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora) Annual Reports, 1980, 1981, 1982. Washington, DC: Fish and Wildlife Service, U. S. Department of the Interior.

Clapp, R. B. Mammals imported into the United States in 1972. U. S. Fish and Wildlife Service Special Scientific Report--Wildlife No. 181. Washington, DC: U. S. Department of the Interior, 1974.

Clapp, R. B., & Paradiso, J. L. Mammals imported into the United States in 1971. U. S. Fish and Wiildlife Service Special Scientific Report-- Wildlife No. 171. Washington, DC: U. S. Department of the Interior, 1973.

Eudey, A., & Mack, D. Use of primates and captive-breeding in the United States. In D. Mack and R. Mittermeier, Eds., The International Primate Trade. Washington, DC: World Wildlife Fund--U.S., in press.

Gerone, D. Domestic breeding of nonhuman primates, 1978. Unpublished manuscript prepared for the Conservation Committee, American Society of Primatologists, 1980.

Honackim J. H., Kinman, K. E., & Koeppl, J. W. Mammal species of the World. Lawrence, Kansas: Allen Press, Inc., and the Association of Systematics Collections, 1982.

Kavanagh, M. A review of the international primate trade. In D. Mack & R. Mittermeier, Eds., The International Primate Trade. Washington, DC: World Wildlife Fund--U.S., in press.

Mack, D. Trends in primate imports into the United States, 1980. ILAR News, 1981, 24{4}, 12-13.

Mack, D. Trends in primate imports into the United States, 1981. ILAR News, 1982, 25{4}, 10-13.

Mack, D. Trends in primate imports into the United States, 1982. ILAR News, 1983, 26{4}, 10-15.

Mack, D., & Eudey, A. A review of the U. S. primate trade. In D. Mack & R. Mittermeier, Eds. The International Primate Trade. Washington, DC: World Wildlife Fund--U.S., in press.

Paradiso, J. L., & Fisher, R. D. Mammals imported into the United States in 1970. U. S. Fish and Wildlife Service Special Scientific Report--Wildlife No. 161. Washington, DC: U. S. Department of the Interior, 1972.

Wildlife Trade Monitoring Unit. Malaysia bans monkey exports. TRAFFIC Bulletin, 1984, 5{5/6}, 51.

---------------------------------------------------

Reprinted with some editing from ILAR News, 1984, 27{4}, 6-12. In particular, refer to the original for extensive tables of data pertaining to the comments in the article.

---------------------------------------------------

* * *

Recent Books and Articles

(Addresses are those of first authors)

Bibliographies

Changes in hierarchy in nonhuman primates: A bibliography. Williams, J. B. Seattle: Primate Information Center, 1984. 17 pp. {Price: $7.00. ($6.00 prepaid). Send order to: Primate Information Center, Regional Primate Research Center SJ-50, University of Washington, Seattle, WA 98195}

Clinical blood pictures of nonhuman primates: A selected bibliography of major normative hemograms and chemistry. Caminiti, B. Seattle: Primate Information Center, 1984. 17 pp. {Price and ordering information same as above.}

Animal models of toxicant pharmacokinetics: Species differences of nonhuman to human primates or other animals. A bibliography, 1970-1983. Seattle: Primate Information Center, 1984. 11 pp. {Price and ordering information same as above.}

Endorphin and enkephalin studies in nonhuman primates: A bibliography. Williams, J. B. Seattle: Primate Information Center, 1984. 10 pp. {Price and ordering information same as above.}

Behavioral development in infant African monkeys: A bibliography. Williams, J. B. Seattle: Primate Information Center, 1984. 9 pp. {Price: $6.00. ($5.00 prepaid). Ordering information same as above.}

Disease

Transmission of B virus infection between monkeys especially in relation to breeding colonies. Zwartouw, H. T., MacArthur, J. A., Boulter, E. A., Seamer, J. H., Marston, J. H., & Chamove, A. S. (Chemical Defence Establishment, Porton Down, Salisbury, Wilts, SP4 OJG, England) Laboratory Animals, 1984, 18, 125-130.
. . .Studies of B virus (Herpesvirus simiae) antibody in several species of macaque lead to the following generalizations. Newborn monkeys are not infected with B virus, even when born of seropositive mothers. Young monkeys remain uninfected until they become adults. The majority of adults develop B virus antibody unless their physical contact with seropositive adults is restricted. These observations are consistent with sexual transmission of B virus and classification of the disease in monkeys as venereal. However, infection at oral and dermal sites also occurs and may play a part in monkey-to-monkey transmission. Epizootics of B virus occurred during early attempts to start B virus-free breeding colonies. They appeared to originate from reactivated latent B virus in adult monkeys which had only low titres of antibody. The stress produced when groups of adult strangers were assembled to form breeding colonies was the most effective known inducer of latent B virus. Total exclusion of animals with any trace of antibody has enabled the establishment of new breeding colonies which are free from B virus.

Treatment of pulmonary acariasis in rhesus macaques with ivermectin. Joseph, B. E., Wilson, D. W., Henrickson, R. V., Robinson, P. T., & Benirschke, K. (California Prim. Res. Ctr., Univ. of Calif., Davis, CA 95616) Laboratory Animal Science, 1984, 34, 360-364.
. . .Rhesus monkeys were treated for pulmonary acariasis with single injections of ivermectin (200 ug/kg). Monkeys were killed and complete necropsies performed. Control monkeys had numerous live mites, while treated monkeys had only dead, frequently fragmented mites. Histopathologically, inflammatory lesions were most severe in control monkeys and monkeys killed one week after treatment. Inflammatory changes progressively decreased with increasing time post treatment.

Physiology

Reference intervals for some clinical chemical parameters in the marmoset (Callithrix jacchus): Effect of age and sex. Davy, C. W., Jackson, M. R., & Walker, J. (Roche Products Ltd., Welwyn Garden City, Hertsfordshire, England) Laboratory Animals, 1984, 18, 135-142.
. . .The effects of age (250-300 days compared with 500-550 days) and sex on some clinical chemistry parameters in the marmoset was investigated. Alkaline phosphatase levels decreased with age, young males having higher plasma levels than young females, but no sex differences were discernible for older animals. Levels of gamma-glutamyl transpeptidase and sorbitol dehydrogenase were higher in older males than in younger females. Higher plasma iron levels were found in the males with increasing age. Age and sex effects for protein and albumin were interactive and further interpretation was therefore difficult. No significant age or sex effects were seen for cholinesterase, acetylcholinesterase, isocitrate dehydrogenase, malate dehydrogenase, lactate dehydrogenase, glutamate dehydrogenase, aspartate amino transferase, alanine aminotransferase or bilirubin.

The effect of hemolysis on some clinical chemistry parameters in the marmoset (Callithrix jacchus). Davy, C. W., Jackson, M. R., & Walker, J. (Roche Products Ltd., Welwyn Garden City, Hertfordshire, England) Laboratory Animals, 1984, 18, 161-168.
. . .The effect of hemolysis on the levels of commonly analyzed plasma constituents was investigated in the common marmoset. Results were divided into a) low levels of extra haemolysis (<2 g/l plasma hemoglobin) and b) high levels of extra hemolysis (>2 g/l plasma hemoglobin). Mean changes in plasma constituent levels were examined and the correlation with increased hemolysis measured. Large changes in malate dehydrogenase and lactate dehydrogenase were found at low levels of hemolysis. With higher levels of hemolysis there were statistically significant changes in the levels of alanine aminotransferase, isocitrate dehydrogenase, glutathione reductase, bilirubin, aspartate aminotransferase and sorbitol dehydrogenase. The significance of these findings is considered in relation to the interpretation of changes of plasma consituents as indicators of tissue/organ damage.

Breeding

Techniques for hand-raising neonatal ruffed lemurs (Varecia variegata) and (Varecia variegata rubra) and a comparison of hand-raised and maternally-raised animals. Meier, J. E., & William, M. S. (Jennings Ctr. for Zoological Med., Zoological Society of San Diego, PO Box 551, San Diego, CA 92112) Journal of Zoo Animal Medicine, 1984, 15{1}, 24-31.
. . .Techniques for hand-raising red ruffed and black and white ruffed lemurs have been highly successful. Success is dependent on early recognition of those neonates requiring hand-raising. Animals weighing less than 70 gm rarely survive. Hypothermia, trauma, and conjunctivitis are seen, but pneumonia is rare. Hand-raised ruffed lemurs do not initially gain weight as rapidly as maternally-raised animals; however, they both reach the same adult weight. Total formula intake in ruffed lemurs is high and frequent feedings are necessary for normal growth and development.

Problems and experiences in performing artificial insemination in bonobos Pan paniscus. Matern, B. (Zoologischer Garten, D-6000, Frankfurt/Main, Federal Republic of Germany) Zoo Biology, 1983, 2, 303-306.
. . .A report is given on the problems and the procedure of artificial insemination in (Pan paniscus). In addition, the different possibilities and methods of collecting sperm, its conservation, and determining the time of ovulation are discussed, as well as the various insemination techniques and their usage under practical conditions in zoological gardens.

Housing conditions and breeding success of chimpanzees at the Primate Center TNO. Goosen, C., Schrama, A., Brinkhof, H., Schonk, J., & van Hoek, L. A. (Primate Center TNO, PO Box 5815, 2280 HV Rijswijk, The Netherlands.) Zoo Biology, 1983, 2, 295-302.
. . .The colony was built up from 1964 to 1971 by the acquisition of mostly young chimpanzees; thereafter, it was increased by local breeding. The ages at which the animals became reproductive were between 6 and 11 years for the males and between 7 and 15 years for the females. Seventy-six percent of the pregnancies (N=132) were carried to full term and 87% of these were live births. Fifty-five percent of the babies were nursed by their mothers for 2-10 months. The next pregnancy after an abortion occurred on the average after 7 months; after a carriage to term, this occurred after 11.9 months. The difference was not influenced by the duration of the weaning period. Animals of 2 years or more that had been weaned within a month were more likely to show body rocking than animals weaned later. Cases of disturbed social or reproductive behavior were rare; the first locally bred animals have become reproductively active.

Breeding of the cotton-top tamarin Saguinus oedipus oedipus: A comparison with the common marmoset. Evans, S. (Dept. of Psychology, Univ. of Stirling, Stirling, Scotland FK94LA) Zoo Biology, 1983, 2, 47-54.
. . .A colony experienced in the successful breeding of the common marmoset acquired 15 cotton-top tamarins for breeding purposes over a period of 2 yrs. Data are presented on the breeding of the cotton-top and compared with the breeding of the common marmoset. The tamarins did not breed as successfully as the common marmosets. There were several reasons for this: Cotton-tops took longer to produce young on initial pairing, had a longer birth interval, and showed a high incidence of suspected infanticide and parental neglect. These factors are thought to be largely responsible for the relatively low reproductive potential of the cotton-top in captivity.

Timing of birth, female reproductive success and infant sex ratio in semifree-ranging Barbary macaques (Macaca sylvanus). Paul, A., & Thommen, D. (Affenberg Salem, D-777, Salem, Federal Republic of Germany) Folia Primatologica, 1984, 42, 2-16.
. . .Five years of data on the reproduction of a semifree-ranging population (starting H=164 animals) of Barbary macaques were examined. In this seasonally breeding species--birth season: mid-March to beginning of August--primiparous 4-year-old females gave birth significantly later in the year than older primiparous and multiparous females, respectively. Multiparous females without an infant from the preceding season gave birth significantly earlier than females who had raised an infant. 88.4% of birth intervals were approximately 1 year, 11.6% about 2 years. Infant loss did not influence the length of the interbirth interval, but after the birth of the next surviving infant the interval was significantly longer. The interval following the 1st infant was significantly longer than after subsequent infants. After the birth of daughters primiparous females had markedly longer birth intervals than after the birth of sons. Infant mortality was 9.1%. Neonatal mortality was influenced by rank and parity of the mother and sex of the infant. Allomothering and aggression by older group members are thought to be the main causes of infant mortality. Female reproduction rates were not dependent on rank. High-ranking females, however, bore their 1st infant significantly earlier than low-ranking females. Low-ranking females had more daughters than sons, in high-ranking females the reverse was found. Differences from findings of other species are discussed with regard to differences in social organization and the reproductive strategies resulting from them.

Field Studies

Chinese primates: Some real and one mythical(?). Poirier, F. E. (Dept. of Anthropology, Ohio State University, Columbus, OH 43210) Explorers Journal, 1983, 61, 124-130.
. . .An informal description of the author's trip to the People's Republic of China in 1982, for what was probably the first collaborative Sino-American primatological field research. The site was a remote mountain region of Hubei Province. The author's primary interest was in the rare golden monkey (Rhinopithecus roxellanae) and in rhesus monkeys (Macaca mulatta). The author also gathered information on the so-called hairy wildman. The author was unable to visit the largest population of golden monkeys in the Province (and in China) because the area they inhabit is being made into a nature reserve, but he was nevertheless able to gather considerable information about these monkeys, which he outlines in the article. The golden monkeys are so rare, in part because they have been hunted for their highly-prized hair, bones, and meat for almost 1,000 years. They are also sometimes killed because they are mistaken for the hairy wildman. The macaque population in the area is rapidly diminishing due to trapping, habitat destruction, and killing. Little can be expected to be done about this, since they raid crops, which, in turn, must be constantly guarded when they are ripening. Reports persist about the human-like or ape-like hairy wildman in this region, as well as other parts of China and other parts of the world. After reviewing the local and other evidence, the author concludes that the burden of proof of the existence of such creatures remains on those who claim they exist.

---------------------------------------------------

In many cases, the original source of reference in this section has been the Current Primate References prepared by The Primate Information Center, Regional Primate Research Center SJ-50, University of Washington, Seattle, WA 98l95. Because of this excellent source of references, the present section is devoted primarily to presentation of abstracts of articles of practical or of general interest. In most cases, abstracts are those of the authors.

---------------------------------------------------

* * *

* * *

NOTE: All printed back issues of the Laboratory Primate Newsletter are available at $3 each.

All correspondence concerning the Newsletter should be addressed to:
Judith E. Schrier, Psychology Department, Box 1853, Brown University
Providence, Rhode Island 02912. (Phone: 401-863-2511)
Judith_Schrier@brown.edu

ACKNOWLEDGMENTS

The Newsletter is supported by U. S. Public Health
Service Grant RR-00419 from the Animal Resources Program,
Division of Research Resources, N.I.H.

We are grateful to Linda Straw Coelho of San Antonio, Texas, for providing the cover drawing of a chimpanzee.

Copyright @1984 by Brown University

Editor: Allan M. Schrier
Consulting Editor: Morris L. Povar
Managing Editor Helen Janis Shuman