Table Of ContentCONTRIBUTORS
Delwood C. Collins David E. Martin
Charles Faiman Patrick R. McGinnis
Dian Fossey Paul I. Musey
Gene B. Fuller Ronald D. Nadler
Birute M. F. Galdikas John R. K. Preedy
Kenneth G. Gould Francisco L Reyes
Charles E. Graham R. V. Short
Alexander H. Harcourt Kelly ]. Stewart
William C. Hobson Caroline E.G. Putin
O. Ray Kling Jeremy S. D. Winter
Kristina Wright
Reproductive Biology
of the Great Apes
Comparative and Biomedical Perspectives
Edited by
CHARLES E. GRAHAM
Reproductive Biology Division
Primate Research Institute
New Mexico State University
Holloman Air Force Base, New Mexico
ACADEMIC PRESS
A Subsidiary of Harcourt Brace Jovanovich, Publishers
New York London Toronto Sydney San Francisco 1981
COPYRIGHT © 1981, BY ACADEMIC PRESS, INC.
ALL RIGHTS RESERVED.
NO PART OF THIS PUBLICATION MAY BE REPRODUCED OR
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ACADEMIC PRESS, INC.
Ill Fifth Avenue, New York, New York 10003
United Kingdom Edition published by
ACADEMIC PRESS, INC. (LONDON) LTD.
24/28 Oval Road, London NW1 7DX
Library of Congress Cataloging in Publication Data
Main entry under title:
Reproductive biology of the great apes.
Includes bibliographies and index.
1. Apes—Reproduction. 2. Mammals—Reproduction.
I. Graham, Charles E. [DNLM: 1. Pongidae—Phys-
iology. 2. Reproduction. WL 737.P96 G738r]
QL737.P96R45 599.88'40416 80-89417
ISBN 0-12-295020-8
PRINTED IN THE UNITED STATES OF AMERICA
81 82 83 84 9 8 7 6 5 4 3 2 1
CONTRIBUTORS
Numbers in parentheses indicate the pages on which the authors' contributions begin.
DELWOOD C. COLLINS (69,163), Departments of Medicine and Bio-
chemistry, Emory University School of Medicine, Atlanta, Georgia 30322
CHARLES FAIMAN (45,83), Department of Endocrinology and Me-
tabolism, University of Manitoba, Winnipeg, Manitoba R3E 0Z3, Canada
DIAN FOSSEY (265), Section of Neurobiology and Behavior, Lang-
muir Laboratory, Cornell University, Ithaca, New York 14850
GENE B. FULLER (83), Reproductive Biology Division, Primate Re-
search Institute, New Mexico State University, Holloman Air Force
Base, New Mexico 88330
BIRUTE M. F. GALDIKAS* (281), Orangutan Research and Conser-
vation Project, Pangkalan Bun, Kalimantan Tengah, Indonesia
KENNETH G. GOULD (105,127,375), Yerkes Regional Primate Re-
search Center, Emory University, Atlanta, Georgia 30322
CHARLES E. GRAHAM (1,69,407), Reproductive Biology Division,
Primate Research Institute, New Mexico State University, Holloman Air
Force Base, New Mexico 88330
ALEXANDER H. HARCOURT (265,301), Department of Applied Bi-
ology, University of Cambridge, Cambridge CB2 3DX, England
WILLIAM C. HOBSON (45,83), Reproductive Biology Division, Pri-
mate Research Institute, New Mexico State University, Holloman Air
Force Base, New Mexico 88330
O. RAY KLING (69), Department of Obstetrics, University of Okla-
homa, College of Medicine, Health Science Center, Oklahoma City,
Oklahoma 75190
*Present address: Department of Archaeology, Simon Fraser University, Burnaby, British
Columbia, Canada.
XI
Xll Contributors
DAVID E. MARTIN (105,127,343), College of Allied Health Sciences,
Georgia State University, Atlanta, Georgia 30303, and Yerkes Regional
Primate Research Center, Emory University, Atlanta, Georgia 30322
PATRICK R. McGINNIS (239), 102 Putnam Street, Watertown, Mas-
sachusetts 02172
PAUL I. MUSEY (163), Department of Medicine, Emory University
School of Medicine, Atlanta, Georgia 30322
RONALD D. NADLER (69,191), Yerkes Regional Primate Research
Center, Emory University, Atlanta, Georgia 30322
JOHN R. K. PREEDY (163), Department of Medicine, Emory Univer-
sity School of Medicine, Atlanta, Georgia 30322
FRANCISCO I. REYES5' (45,83), Departments of Obstetrics and Gy-
naecology and Physiology, University of Manitoba, Winnipeg, Mani-
toba, R3E 0Z3, Canada
R. V. SHORT (319), Medical Research Council Unit of Reproductive
Biology, Centre for Reproductive Biology, Edinburgh EH3 9EW, Scotland
KELLY J. STEWART (265), Sub Department of Animal Behavior,
University of Cambridge, Madingley, Cambridge CB3 8AA, England
CAROLINE E. G. TUTIN (239), Department of Psychology, University
of Stirling, Stirling FK9 4LA, Scotland
JEREMY S. D. WINTER (45,83), Department of Paediatrics, University
of Manitoba, Winnipeg, Manitoba, R3E 0Z3, Canada
KRISTINA WRIGHT (163), Department of Medicine, Emory Univer-
sity School of Medicine, Atlanta, Georgia 30322
^Present address: Department of Obstetrics and Gynecology, State University of New York,
Downstate Medical Center, Brooklyn, New York 11203.
FOREWORD
This valuable compilation of information concerning the reproductive
biology and sexual behavior of mankind's closest living relatives, the
great apes, is remindful of the heroic effort that was made to salvage
some of the archaeological treasures of Egypt from the rising waters
of the Aswan dam. Study of these rare and disappearing species rep-
resents exploration of a "last frontier" in reproductive biology that is
providing an exciting glimpse of the evolution of human reproduction
as well as insight into the specialized physiological mechanisms peculiar
to apes and humans.
From the study of numerous laboratory mammals much has been
learned over the past half century concerning both the basic principles
of reproductive physiology that are common to a wide variety of mam-
mals and the special mechanisms that apply to individual species. The
stimulatory action of estrogen on the female reproductive tract, the
follicle-stimulating action of FSH, the ovulation-inducing action of LH,
the masculinizing action of testosterone, and the obligatory role of
progesterone in the establishment of pregnancy are examples of basic
principles that could have been revealed by the study of any or all of
the common laboratory animals. On the other hand, we have learned
to our dismay that during evolution each species has developed features
that are peculiar to its own reproductive process, and that these spe-
cializations limit our ability to extrapolate findings from one species to
another.
Thus, all species exhibit minor to major differences in the anatomy
of their reproductive systems, in timing and control of hormone-
induced events, in alterations of peptide or protein hormone structure
that bestow immunologic specificity, and in the quantity and metab-
olism of hormones secreted. It is the details of this process that have
been most susceptible to evolutionary modification. As our knowledge
deepens, so has the need for detailed information concerning those
species most closely related to Homo sapiens. The elucidation of repro-
ductive functions has now progressed to the point that even the mon-
keys have limitations as a model for humans. Unquestionably the Day
Xlll
XIV Foreword
of the Ape has arrived! The effort and cost necessary to study these
difficult species are justified.
When I first learned that this volume on the reproductive biology of
the great apes was in preparation, it brought to mind an ancient parable
originally applied in a rather different context, 'The last shall be first
and the first last/' The apes, though last to be utilized as laboratory
subjects for reproductive studies, stand first as the animal of choice
when the ultimate objective is transference of the information gained
to humans. Although the old adage that "better late than never" also
holds true in this instance, there are other compensating aspects to this
long neglect of the apes. Most important is the fact that research on
these special species is now greatly facilitated by the revolutionary
improvements that have been made in the methods and equipment
available for basic biological research. Moreover, these modern labo-
ratory studies on captive apes benefit from the many preceding years
of close observation of the social organization, living habits, and sex
behavior of the great apes in their natural habitats and from the pi-
oneering experimental studies of Robert M. Yerkes and his colleagues.
The reasons for this long neglect of the apes as laboratory animals
for research on reproduction are not hard to find. If the principal criteria
for suitable laboratory animals—ease of handling, ready availablility in
large numbers, and low cost—are kept in mind, then the adult apes
rate rather low on all counts. Anyone who has ever observed these
powerful and forbidding adults in a zoo will appreciate that the nec-
essary serial sampling of blood and urine is not something for the faint
of heart. Although modern techniques have overcome some of these
difficulties, only a limited number of laboratories are properly equipped
for the conduct of basic biological research on reproduction in apes.
Likewise, the opportunities for testing in apes the unending stream of
ideas that flow from comparative studies in other species cannot be
fully accommodated. This book gives consideration to such limitations
in servicing the types of problems for which apes are suited.
The growing body of recently derived information about the repro-
ductive biology of the chimpanzee, gorilla, and orangutan has finally
reached a critical mass sufficient to generate a full review. The present
volume is a ground-breaking endeavor that will broaden and enhance
reproductive science. It will also contribute to the obliteration of a long-
standing gap in our knowledge of the reproductive process in the
nonhuman primates and will provide a preliminary measure of the apes
as model animals for their less brachiating and more depiliated human
counterparts who abound in the jungles of the world's cities. It is
certain that specialists concerned with the control of human fertility
Foreword XV
will find this material on the great apes of keen interest. A much larger
body of reproductive biologists and anthropologists will be eager to
learn in what ways ape reproductive phenomena agree with or differ
from those of other laboratory animals, or shed light on human
evolution.
Roy O. Greep
PREFACE
This volume is an up-to-date and thorough review of all aspects of
great ape reproduction, in a form that we expect will be of use to
human physiologists, comparative anatomists and zoologists, behav-
iorists, taxonomists, anthropologists, primatologists, and breeders of
apes. Particular thought has been given to the needs of biomedical
scientists working in the area of control of human fertility and gyne-
cological disease who may discover in these pages useful applications
of apes as research models for the human. The phylogenetic affinity
and obvious physical similarities of apes to man suggest the hypothesis
that apes resemble man more closely in the anatomy, physiology, and
behavior of reproduction than do monkeys and lower mammals. As
the reader will discover, this assumption has generally proved to be
correct.
To the extent that the apes share with man resemblances not pos-
sessed by other animals, they are of truly unique value for biomedical
studies. In drawing attention to the potential of chimpanzees as models
for man, Robert M. Yerkes pointed out that 'The greater the degree
of similarity (of structure and function), the safer the inference that
what is true for the one animal will apply also to the other." In no
field, with the possible exception of behavioral research, are apes of
more potential value than in the field of reproductive biology. This fact
is illustrated by the early appearance of papers on chimpanzee repro-
duction from 1930 to 1945, and a strong resurgence of activity during
the last decade which provided the main incentive for preparing the
present volume.
The availability of orangutans and gorillas for biomedical research is
severely limited. Comparative study of the reproduction of these great
apes, however, is of considerable academic interest, as well as of im-
portance to the conservation of apes in the natural state and in captivity.
Reproduction is a dominant factor in the daily physical and behavioral
activity of primates. Therefore it is necessary for every student of ape
biology to be cognizant of the impact of reproductive behavior or phys-
iology on his or her area of study. Reproduction also plays an important
role in species survival and evolution; investigation of the evolution of
xvn
XV111 Preface
reproductive patterns is therefore a proper anthropological endeavor.
Since the reproductive organs are composed of soft tissues not pre-
served in the fossil record, comparative study of living primates, in-
cluding the great apes, is the only pragmatic approach to this problem.
This book is intended not only as a reference work, but also as an
opportunity to identify new areas ripe for investigation. As with other
aspects of ape biology, there are many areas of reproduction that are
totally or incompletely studied, particularly in orangutans and gorillas.
Much new comparative data of significance to human sexual biology
therefore await discovery.
Although every effort has been made to make this volume as com-
prehensive as possible, I am aware that reproduction of the pigmy
chimpanzee has been almost ignored, except in the context of breeding.
This is not an accidental omission, but reflects the lack of opportunity
for study and acquisition of objective data on this species. This obscurity
of Pan paniscus has led most of us to refer to Pan troglodytes as "the
chimpanzee."
I was fortunate to have the opportunity to study reproductive biology
of the great apes during 13 years spent at Yerkes Regional Primate
Research Center under the sympathetic directorship of Geoffrey Bourne.
I also enjoyed the collaboration of a number of colleagues who con-
tributed their expertise to make those studies possible; many of them
are contributors to this volume. To all these colleagues I express my
special thanks.
I am no less grateful to those other contributors with whom I have
never previously worked, but who in every case have prepared excellent
and comprehensive reviews of their topics. All have been commendably
patient with me during the long process of editing. I especially want
to thank A. H. Harcourt, who helped me organize and edit the con-
tributions on field studies, in order to achieve a uniformity of pre-
sentation that would facilitate interspecies comparison.
Support from PHS Grant RR00165 to the Yerkes Regional Primate
Center is gratefully acknowledged. Also, the Ford Foundation gener-
ously and foresightedly underwrote much of the cost of my earlier
studies, in the days when chimpanzees were generally regarded as
exotic and impossible subjects. This book should help to change that
view, by showing that much data of theoretical and practical value are
obtainable from study of the great apes.
