Table Of ContentCHAPTERJ
Darwi·n.and friends
Cold cliffs, more beautiful the deeper you enter
Yet no one travels this road.
White clouds idle about the tall crags;
On the green peak a single monket; wails.
What other companions do I need?
I grow old doing as I please.
,-
Though face and form alter with the years,
I hold fast to the pearl of the mind.
I
j· (Han-Shan. Cold Mountain)
Sexology has never been a pursuit for the intellec Before entering deeper into the complexities of
tually faint-hearted. It might be argued that, now primate sexuality, it will be useful to consider, albeit
adays, attitudes towards the scientific study of sex briefly, some aspects of the history of research on
are much more enli~htened and more tolerant than sexual behaviour. This will serve as an introduction
was the case in the past. However, even now, the to the 14 chapters that follow. First, therefo"re,let us
subject is frequently undervalued, easily trivial return to the nineteenth century, 'a century of prud
ized and made the target of bigotry. People are. ery' (Hoenig 1977), and consider Darwin's funda
often conflicted by their own sexuality; indeed, in mental contributions to the theory of evolution.
many parts of the world, children are culturally In the years that followed the publication of the
conditioned from infancy to develop such con Origin of Species (Darwin 1859) acceptance was
flicts. An objective scientific approach, however, gained, albeit reluctantly in certain quarters, that
leads one to conclude that selective forces underly human beings must be closely related to the pri
ing successful reproduction, as well as survival, mates and especially to the great apes. The case for
are the engines which have driven the evolution of an evolutionary link between the ancestors of the
life on earth. For those organisms that engage in great apes and humans was cogently argued by
sexual reproduction the laws of sexual selectio_!l, Huxley (1863) in his essays on Man's Place in Nature.
as well as natural selection, have played essential Darwin's (1871) later treatise on The Descent of Man
roles in shaping behaviour, as well as anatomy and and Selection in Relation to Sex also contained com
physiology. Thus, no study of the reproductive parative material on the non-human primates.
biology of complex organisms, such as the pri Darwin emphasized the close relationship between
mates, can be complete without a consideration of humans and the African apes (gorilla and chimpan
their sexual behaviour. Although sexology may zee), positing that human beings had probably orig
still represent the scientific equivalent of Han inated in Africa. Although he made little reference
Shan' s Cold Mountain, yet it is full of important to sexual behaviour in his book, Darwin did discuss
and still poorly explored research questions. There the subject of sex differences in human morphology
is much in the scientific study of sexuality to and secondary sexual traits at some length, and
engage 'the pearl of the mind'. considered these in the light of the insights he had
2 PRIMATE SEXUALITY
gained from studies of other animals. Two principal Traditional Darwinian View
avenues of sexual selection were identified and
explored by Darwin; intra-sexual competition for
access to mates, and inter-sexual selection for sec
ondary sexual adornments and displays as enhanc
ers of sexual attractiveness. Both these processes Pre-copulatory
Sexual
were though(to act primarily upon the male sex
Selection
(Fig. 1.1). Thus, intra-sexual competition favoured
the evolution of greater aggressiveness, as well
as increased body size and weaponry in males of
various species. Inter-sexual selection, on the other
hand, accounted for the evolution of extravagant
secondary sexual characteristics, such as the bril
Modem Darwinian View
liant plumage of the peacock and the red and blue
pigmentation of the adult male mandrill.
Although Darwin was preoccupied with the
effects of sexual selection upon males there is, of
course, no reason to exclude the possibility that Pre-copulatory Copulatory
Sexual Sexual
females might compete among themselves for mat
Selection ·Selection
ing opportunities, as well as more indirectly for the
resources required to nurture their offspring.
Likewise, examples might exist of inter-sexual selec
tion for physical adornments or behavioural pat
CRYPTIC
terns that augment female sexual attractiveness FEMALE
CHOICE
(Fig. 1.1). Both these propositions are valid as far as
the Order Primates is concerned and examples will <==::J
·-·~ Intrasexual selection ,Intersexual selection
be described and discussed throughout the present
volume. Figure 1.1 Traditional and modern views of the processes
parwin considered that the primary genitalia of underlying sexual selection. The traditional Darwinian view
both sexes had been moulded by evolution in emphasized the importance of inter-male competition and female
response to natural selection, rather than as a result choice as pre-copulatory determinants of mating success. The modern
of sexual selection. ·He certainly recognized that Darwinian view acknowledges that intra-sexual competition might
sometimes involve females and that females can, in some
some structures, such as specialized prehensile
circumstances, produce extravagant adornments to attract males
organs in males of various invertebrate groups,
(e.g. sexual skin in some female Old World monkeys). Most important
might have been affected by sexual selection. Thus
has been the realization that sexual selection acts at the copulatory
'if the chief service rendered to the male by his pre
level and post-copulatory level, via sperm competition and cryptic
hensile organs is to prevent the escape of the female
female choice, to affect reproductive success (as indicated in lower
before the arrival of other males, or when assaulted
part of diagram, on the right hand side).
by them, these organs will have been perfected
through sexual selection'. Yet he lamented that 'in
most cases of this kind it is impossible to distinguish selection, embracing copulatory and post-copula
between the effects of natural and sexual selection'. tory processes in addition to pre-copulatory compe
Only in the last few decades has it become clear that tition and mate choice, is shown in schematic form
sexual selection operates at the level of the gonads on the right hand side of Fig. 1.1. Numerous exam
(via sperm competition: Parker 1970) and copulatory ples of such effects of sexual selection in primates
organs (via cryptic female choice: Eberhard 1985, 1996) will be dealt with in this book.
a~ well as influencing the evolution of patterns of Given Darwin's genius as a biologist, it might
copulatory behaviour. This modem view of sexual seem surprising that he failed to register the
DARWIN AND FRIENDS. 3
importance of sexual selection at the genitalic level. physiology or genetics in Darwin's time. Yet in the
His extensive taxonomic studies of barnacles, for fields of reproductive physiology, behaviour, and
example, should have alerted him to the possible genetics, contributions made by nineteenth century
effects of sexual selection upon masculine genital scientists have profoundly influenced the develop
morphology and behaviour (Darwin 1851, 1854). ment of sexology during the twentieth century.
Although barnacle species are usually hermaphro Mendel's experiments on inheritance in the garden
ditic, cross-fertilization between individuals is the pea provided the foundation for the science of
rule in this group. Being sessile, eachbamacle is genetics. His paper, publisbed in the Proceedings of
equipped with a greatly elongated penis; ~ose with the Natural History Society of Brunn in 1866 went
the longest penes gain a reproductive advantage, unnoticed by his contemporaries, but its impor
since they can reach and fertilize a larger number of tance was finally appreciated in 1900 when de Vries,
their neighbours (e.g., Semibalanus balanoides: Hoch Correns, and Tschermak each independently 'redis
2008). Each individual may be inseminated by a covered' it for science (Fisher 1965). In the field of
number of conspecifics, and barnacles often have reproductive physiology, the first proof of endo
large testes, presumably because sperm competi crine function is usually credited to Berthold (1849)
tion favours the production of larger numbers of who studied the effects of castration and testicular
gametes under such conditions. It is possible that implantation in the cockerel. Berthold's single
Darwin's reticence in dealing with the evolution of report was also a pioneering experiment in behav
copulatory behaviour and genital anatomy was a ioural endocrinology. He noted that three cockerels
result of the moral climate of his time. The nine that were castrated and implanted with a single tes
teenth century. was an era of prejudice regarding tis remained normal 'so far as voice, sexual urge,
sexual behaviour. Biographers have attested to belligerence, and growth of the comb and wattles
Darwin's retiring nature and his reluctance to par were concerned'. The three untreated castrates
ticipate in the heated public debates which greeted became caponized, however. Since the transplanted
the publication of his ideas concerning natural testes lacked their original innervation, Berthold
selection (Bowlby 1990; Desmond and Moore 1991). surmised that blood-born factors emanating from
One can only speculate as to what might have the transplants must be responsible, and that the
occurred if The Descent of Man had included a nervous system might also be a target for such fac
detailed exposition on. the evolution of the penis tors (Forbes 1949). In his survey of the history of
and testes or descriptions of the various copulatory behavioural endocrinology Beach (1981) notes that
postures and patterns employed by animals and 'during the half century that followed Berthold's
human beings. It is not unreasonable to suggest that discovery, physiologists in France, Italy, Germany,
Darwin concentrated on the pre-copulatory aspects and Russia undertook investigation of relationships
of sexual selection because they were less likely to between mating behaviour of various animals and
cause offence (Birkhead 1997). Even at the close of functions of the sex glands'. Steinach (1894, 1910),
the nineteenth century the great sexologist, Havelock for instance, conducted a variety of experiments
Ellis, records that his books had to be published in using amphibians, birds, and rodents. His view was
America, because their content was viewed as that gonadal secretions in some way stimulate, or
obscene in England (Havelock Ellis 1902). inhibit, specialized centres in the brain to produce
Setting aside the topic of sexual selection, it is their behavioural effects.
essential also to con5ider the many proximate Bayliss and Starling (1902) are often credited with
mechanisms that govern the expres~ion of sexual initiating the modem era of endocrinology; they
behaviour. How do sex differences in behaviour demonstrated that secretin released by the duode
develop during the lifetime of an individual and nal mucosa stimulates the flow of pancreatic juice
how do hormones and other physiological mecha (Turner 1960; Turner and Bagnara 1976). Starling
nisms influence sexual activities? In reviewing cur also coined the term 'hormone', deriving it from
rent knowledge of these fields it has been sobering the Greek word hormaein meaning to 'impel or
to reflect how little was known about reproductive arouse to activity' (Barrington 1963). Yet it was the
4 PRiMATE SEXUALITY
nineteenth century physiologists who had laid the (1872-1922). Forel was a psychiatrist and an ento
foundations upon which endocrinology is based, mologist of renown whose interest in sexual mat
and it is very much to their credit that behavioural ters was as an educator and campaigner for social
observations formed an integral part of their stud reform. Freud, the father of psychoanalytic theory,
ies of endocrine function. focused attention upon the phenomenon of infan
If the sexual activities of cockerels or fr.ogs were tile sexuality with the publication of Three Essays on
margiitally acceptable as subjects for scientific con the Theory of Sexuality (1905). ~ew today would sub
templation in Darwin's time, human sexuality was scribe uncritically to his views regarding phases of
quite another matter. As Hoenig (1977) says, 'the infant erato-sexual development (i.e. 'oral', 'anal',
19th century was a century of prudery, and to take and, 'phallic' phases) or the existence of oedipal or
up the study of sexual disorders and write about castration complexes in human infants. Indeed
them required great courage'. Rich¥"d von Krafft there is no evidence that homologues of such devel
Ebing (1840-1902) was one such courageous pio opmental processes exist among the non-human
neer who established the study of sexual disorders primates, as will be discussed in later chapters of
as a distinct branch of psychiatry. His Psychopathia this book. Hirschfeld was more specifically a 'sex
Sexual is: With special reference to the Antipathic Sexual researcher' who published a huge body of original
Instinct was published in 1886 and ran to 12 edi work, including his Die Transvestiten (Hirschfeld
tions. Despite criticisms of the book at the time, 1910) which provided the first scholarly treatment
and the fact that von Krafft-Ebing published other of what is now called 'transexualism' (Hoenig 1977).
major treatises on psychiatry, Psychopathia Sexualis Hirschfeld was a homosexual, and he campaigned
remains his most enduring contribution. His courageously for the rights of sexual minorities. His
detailed case histories and descriptions of ·para Centre for Sex Research, founded in 1919 and sub
philic behaviour are still valuable; the reader will sequently donated to the German nation, was closed
find them referred to in Chapter 5 of this book. and his books and collections were burned by the
Another, and less fortunate, student of human sex Nazis. Fortunately Hirschfeld was in France by that
uality was Albert Moll (1862-1939) a private practi time; he died there in 1935.
tioner who lived in Berlin. Despite an active career These early sexologists had little opportunity to
during which he founded an International Society compare their studies of human sexuality with
.for Sex Research and organized the first ever information on the non-human primates. Indeed,
International Congress on Sexology, Moll was to very little was known about the sexual lives of
die penniless and unmourned by the scientific monkeys and apes until the third and fourth dec
establishment. Havelock Ellis (1858-1939) who ades of the twentieth century, when important
wrote widely on sexual issues, wryly commented publications began to appear, both in the USA and
that 'the pioneer in this field may well count him in Great Britain. The realization that Old World
self happy if he meets with nothing worse than monkeys and apes have a menstrual cycle which is
indifference'. Havelock Ellis was not an experimen physiologically homologous with that of the human
tal scientist or collector of clinical histories; his con female, led to a number of studies to explore rela
tribution was made primarily by examining sexual tionships between the menstrual cycle and sexual
problems in the light of information derived from behaviour (in baboons: Zuckerman 1932; rhesus
studies in cultural anthropology. He referred occa monkeys: Ball and Hartman 1935; and chimpan
sionally to the sexual behaviour of animals, includ zees: Yerkes and Elder 1936; Young and Orbison
ing monkeys and apes (Havelock Ellis 1902), but 1944). In the USA, a special committee was formed,
there was insufficient information upon which to under the chairmanship of Robert Yerkes, to sup
base detailed comparisons. port research in the fields of sexual physiology and
Other pioneers in the field of sex research whose behaviour. Richard Harkness once defined a com
careers spanned the late nineteenth and early twen mittee as 'A group of the unwilling, picked from
tieth centuries include Forel (1848-1931), Freud the unfit, to do the unnecessary'. However, The
(1856-1939), Hirschfeld (1856-1935), and Bloch Committee for Research in Problems of Sex must have
DARWIN AND FRIENDS 5
been exceptional, as it was very effective in pro Altmann estimated that field research on primate
moting advances in s'exolqgy. . William Young, who ecology and behaviour was doubling every five
helped to lay the foundations of modem behav years. At that time, the majority of work involved
ioural endocrinology with his experiments on the the Old World monkeys and apes. However,
organization and activation of sexual behaviour by research interests have broadened over the years·
gonadal hormones, . received support from this and there has been a gratifying increase in field
Committee. The first large-scale surveysof human work both on the New World primates and on
sexual behaviour, carried out by Alfred Kinsey and prosimians, including some of the nocturnal forms
his colleagues at Indiana University (Kinsey et al. such as mouse lemurs, bushbabies, and pottos
1948, 1953), and the field researches of Clarence (Smuts et al. 1987; Campbell et al. 2007). Although
Ray Carpenter on primate behaviour (Carpenter the majority of reports are not specifically concerned
1934. 1935, 1940, 1942), also benefited from the sup with sexual behaviour, the primate field literature
port of Yerkes and The Committee for Research in as a whole constitutes an invaluable source of infor
Problems of Sex. mation on reproductive biology, mating systems,
Special mention must be made concerning mating tactics, and patterns of sexual·behaviour.
Carpenter's contributions to primatology, because Consider, as examples, the extraordinary breadth of
his comparative approach to studies of primate information now available on the social and sexual
social organization and sexual behaviour was lives of the African apes (Chimpanzee: Goodall
unique and well ahead of its time. Carpenter's 1986; Nishida 1990; Boesch and Boesch-Achermann
work led to the appreciation that primate mating 2000; Reynolds 2005; Bonobo: Susman 1984; Kano
systems are variable, and include monogamy (e.g. 1992; Gorilla: Schaller 1963; Harcourt and Stewart
in the gibbon) as well as multimale-multifemale 2007). These are just a few of the many books deal
groups (e.g. in howler and rhesus monkeys). He ing with the African apes; the number of specialized
obtained the first useful information on the perio research papers arising from field studies of the
dicity of sexual activity during ovarian cycles in non-human primates is truly formidable. One of the
female monkeys living under natural conditions. It tasks undertaken in preparing this book was to inte
J
became apparent that, although sexual receptivity grate information concerning sexual behaviour
is not limited to the peri-ovulatory period in species observed under natural conditions with observa
t
such as howlers and rhesus monkeys, there are, tions and experiments on the reproductive physiol
none the less, marked increases in sexual activity at ogy and behaviour of captive primates.
this time. Further, these increases are due in part to We are fortunate to have the opportunity to study
changes in the females' invitational behaviour to over 300 species of prosimians, monkeys, and apes;
males (what Beach (1976) would later call proceptiv a priceless resource upon which to base compara
ity in female mammals) and not simply to the tive and evolutionary arguments concerning the
males' greater willingness to copulate with females nature and origins of primate sexuality. Less fortu
at mid-cycle. nate are our non-human primate relatives, many of
Although a few scientists attempted to carry out which face extinction as the world's rainforests are
fieldwork on primate behaviour (e.g. Nissen (1931) destroyed. Fascinating creatures such as the aye
on· the chimpanzee and Bingham (1932) on the aye, woolly spider monkey, and mountain gorilla
gorilla), none achieved either the depth or compar may be numbered in their hundreds, whilst the
1 ative breadth displayed by Carpenter. A remarkable human population of our planet now exceeds
l, early pioneer in South Africa, Eugene Marais, seven billion. The delusion is still widely prevalent
should also be acknowledged, as his field observa that human population problems can be resolved
i tions on the behaviour of chacma baboons remained simply by the provision of better contraceptive
unpublished until long after his death in 1936 techniques. Yet, without acceptance of contracep
n (Marais 1973). Not until the 1950s and 1960s was tion as part of a healthy and happy sexual life, the
:e there a resurgence of interest in primate fieldwork miseries of overpopulation and disease increase
e which has continued until the present day. By 1967, with each P.assing year. If sexual intolerance and
6 PRIMATE SEXUALITY
bigotry were problems during Darwin's era, it must remarkable primate it is true, but in many ways no
be admitted that these attitudes still flourish and more remarkable than the aye-aye, woolly spider
impede the quest for sexual health in many parts of monkey, or mountain gorilla. However, in the final
the world. Recognition of humankind's sexual Chapter I attempt to place human sexuality in a
nature and our kinship with other primates as comparative context, and to summarize some
sexual beings is thus a matter of some import~ce. aspects of human sexuality, as illuminated by
Throughout this book, the human species is treated knowledge gained from studies of the prosimians,
as just one member of the Order Primates; a monkeys, and apes.
CHAPTER 2
Prim·ate classification and evolution
For those readers who are do not specialize in stud 1. The lemurs of Madagascar: Superfamily
ies of the primates, and who may be unfamiliar Lemuroidea
with their classification, this chapter provides some 2. The galagos and lorises of Africa and Asia:
background information relevant to the compara Superfamily Lorisoidea
tive accounts of primate sexuality that follow. 3. The Tarsiers of Southeast Asia: Superfamily
Members of the Order Primates differ from most Tarsioidea
other mammals in that there is no single diagnostic 4. The New World monkeys: Superfamily
trait that sets them apart and by which all of them Ceboidea
can be defined as belonging to the same taxonomic 5. The Old World monkeys: Superfamily
group. The rodents (Rodentia), for example, all pos Cercopithecoidea
sess specialized, continuously growing, gnawing 6. The apes and human beings: Superfamily
incisor teeth. Bats (Chiroptera) share the same dis Hominoidea.
tinctive wing anatomy, and the whales, dolphins,
and porpoises (Cetacea) all have a 'blow hole' and These six superfamilies comprise approximately 69
other unique features fitting them for an aquatic genera containing between 331-73 species of pri
existence. Yet the primates are most accurately mates (Table 2.1). I say 'approximately' because pri
defined with reference to a suite of generalized mate taxonomy is a restless subject and the exact
morphological traits, rather than by any single fea numbers of species and genera are still debated. As
ture. They have eyes that point forwards, so that Ian Tattersall (2007) has pointed out, some over
binocular (stereoscopic) vision is achieved. Grasping enthusiastic workers in this field have been prone to
hands and feet are typical of this group, and the 'generate new taxonomies with a remarkable lack
thumbs and great toes are often opposable. Flattened of introspection, as if they were no more than pas
nails, rather than claws, occur on at least some dig sive consequences of more lofty concerns'. As one
its. All of these traits probably emerged in arboreal example of such misguided 'taxonomic inflation',
ancestors and in forms that hunted actively for Tattersall lists no less than 23 species of the genus
insects and other small animals. Primates are also Lepilemur! Many of these are nothing more than
large-brained animals, which reproduce relatively minor genetic variants, arbitrarily raised to the sta
slowly compared to other mammals of comparable tus of species by molecular taxonomists. If the
body size. Single offspring are the norm, although reader detects a note of irritation at this point, it is
twinning sometimes occurs, and extended periods because I have been obliged to spend huge amounts
of infant and juvenile life are typical of the group. of time changing the Latin names of many of the
The expression of these traits varies throughout the primates included in the first edition of this book.
Order, in ways that have important implications for The constant shuffling of species and genus names
the understanding of primate evolution and is not helpful; it causes confusion, especially for
classification. non-taxonomists! .
The extant primates may be placed into six major Just occasionally, however, genuinely novel pri
superfamilies, as follows: mates are discovered; testimony to the fact that the
7
8 PRIMATE SEXUALITY
world's shrinking rainforests still contain some sur able new snub-nosed monkey (Rhinopithecus strykeri)
prises for primatologists. Examples include the discovered in 2010, in Myanmar (Geissmann et al.
golden bamboo lemur (Hapalemur aureus: Meier et al. 2011), new marmosets from the Amazonian rainforest
1987) and Tattersall's sifaka (Propithecus tattersalli: (e.g. Callithrix mtluesi: Mittermeier et al. 1992), and a
Simons 1988), both from Madagascar, the sun-tailed stunning array of 'new' African galagos (Bearder et al.
monkey (Cercopithecus solatus: Harrison 1988) fro~ 1995; Nekaris and Bearder 2007). Even a new macaque
Gabon, new tarsiers (Tarsius dianae: Niemitz et al. species has come to light, in northeastern India; the
1991; Tarsius lariang: Driller et al. 2009) from Central first new species of this genus to be discovered in
Sulawesi, the sanjei mangabey (Cercocebus sanjet) from over 100 years (Macaca munzala: Sinha et al. 2005).
the Udzungwa Mountains of Tanzania (Homewood Phylogenetic relationships between the six pri
and Rogers 1981), the kipunji (Rungwecebus kipunjt), mate superfarnilies are represented in simplified
also from Tanzania (Davenport et al. 2006), a remark- form in Fig. 2.1, which incorporates the two major
'
~Aye-aye
Dwarf lemurs
True lemurs
lndri
W
Galagos
~ Lorisines
'
0
Tarsiers
f Marmosets
r
Tamarins
Goeldi' s monkeys
'
Cebid monkeys
1.
~ ~::'nk~~>emid
6t
r------
Gibbons
~
._;----. Gre•t 'P"
~
Man
Figure 2.1 Phylogeny of the extant primates, showing relationships between the six superfamilies (1. Lemuroidea, 2. Lorisoidea, 3. Tarsioidea,
4. Ceboidea, 5. Cercopithecoidea, and 6. Hominoidea). The tarsiers occupy an intermediate position between superfamilies 1 + 2 and other
primates. Traditionally the tarsiers have been included with superfamilies of 1 + 2 in the suborder Prosimii, whereas superfamilies 4, 5, and 6 (the
monkeys, apes, and human beings) have been placed in the suborder Anthropoidea (Simpson 1945). An alternative arrangement, discussed in the
text, is to place the lemuroids and lorisoids together in the Strepsirhini, whilst uniting the tarsiers with the monkeys, apes, and man in the
Haplorhini. (Redrawn and modified from Martin 1995.)
PRIMATE CLASSIFICATION AND EVOLUTION 9
Table 2.1 The extant primates: alphabetical list of the genera belonging to each of the six superfamilies, together with their common names, and
numbers of species.
Genus Common name Number of species
1. Lemuroidea: Madagascar lemurs
Allocebus Hairy-eared dwarf lemur
Ava hi Avahi 3-4
Cheirogaleus Dwarf lemurs 7
Daubentonia Aye-aye
Eulemur True lemurs 5?
Hapalemur Gentle lemurs 3-5?
Jndri lndri 1
Lemur Ring-tail lemur 1
Lepilemurl' Sportive lemurs 7
Microcebus Mouse lemurs 8-13?
Mirza Coquerel's dwarf lemur 1-2?
Phaner Fork-crowned lemur 1-4?
Propithecus Sifakas 3-9?
Varecia' Variegated lemur 1?
2. Lorisoidea: Lorises and Galagos
Arctocebusd Angwantibo 2
Euoticus Needle-claw bush babies 2
Gala go• Bushbabies or galagos 4
Ga/agoides• Dwarf galagos 11
Loris Slender loris 1
Nycticebus Slow lorises 5
Otolemur Greater galagos 4
PerodicticuS9 Potto 1?
Sciurocheirus Squirrel galagos 3?
3. Tarsioidea: Tarsiers
Tarsi us Tarsiers 5
4. Ceboidea: New World monkeys
Alouatta Howler monkeys 9
Aotush Owl monkeys 1D-11?
Ateles; Spider monkeys 4
Brachytelesi Woolly spider monkey 2
Cacajao Uakaris 2
Callibel/a White-bellied pygmy marmoset
Callicebust Titi monkeys 13-28?
Callimico Goeldi's monkey 1
Callithrit Marmosets 6
Cebuel/a Pygmy marmoset
Cebus Capuchin monkeys 5
Chiropotes Bearded sakis 2-5
Lagothrix Woolly monkeys 5
Leontopithecus Golden lion tamarins 4
Mico1 · Marmosets 13
Pithecia Sakis 6?
Saguinus Tamarins 15
Saimiri Squirrel monkeys 5
(continued)
10 PRIMATE SEXUALITY
Table 2.1 Continued
Genus Common name Number of species
5. Cercopithecoidea: Old World Monkeys
Allenopithecus Allen's swamp monkey
Cercocebus Terrestrial mangabeys 7
Cercopithecus Guenons 26
Chlorocebus Vervet 1
Co/obusm Black and white colobus 5
Erythrocebus Patas monkey 1
Lophocebus Arboreal mangabeys 3
Macaca Macaques 21
Mandril/us Mandrill/drill 2
Miopithecus Talapoin 2
Nasalis Proboscis monkey
Papio" Baboons 5?
Piliocolobus Red colobus 9?
Presbytis Langurs 11
Proco/obus Olive colobus 1
Pygathrix Douc langurs 3
Rhinopithecuso Snub-nosed langurs 5
Rungwecebus Kipunji 1
Semnopithecus Hanuman langurs 7
Simias · Pagai Island langur
Theropithecus Gelada baboon 1
Trachypithecus Lutongs 17
6. Hominoidea: Apes and Human Beings
Goril/aP Gorilla 2
Homo Human beings
HylobatesG Gibbons/siamang 10--12
Pan Chimpanzee/bonobo 2
Pongo' Orang-utan 2
Based upon Hershkovitz 19 77; Napier and Napier 19 85; Gautier-Hion eta/. 1988; Mittermeier eta/. 19 88; Martin 19 90; Alterman eta/. 1995; Rowe 19 96; Groves,
2001; Campbell eta/. 2007; and Tattersall 2007.
? The exact number of species in the genus is debated.
• As many as 10 Eulemur species have been recognized by some taxonomists.
b The original species, Lepilemur mustelinus has been split into 7 species on the basis of chromosomal evidence. Most taxonomists recognize 7 species, but as many as
23 species have been proposed, many on the basis of inadequate genetic evidence.
' Two very distinct subspecies of Varecia variegata are known.
d Some authorities recognize two species of Arctocebus; A. calabarensis and A. aureus.
• Further galagine species remain to be described.
1 Nekaris and Bearder (2007) recognize four species of greater galagos.
g A second potto species Pseudapotto martini is known only from skeletal material. Its taxonomic status is disputed.
h Two species groups (red-necked and grey-necked owl monkeys) are distinguishable; the exact number of species is still debated.
; Exact numbers of species and subspecies of spider monkeys have been disputed, but 4 species are currently recognized by most authorities.
I Northern and southern forms of Brachyte/es are ranked as separate species by most authorities.
t The status of many Callicebus species is still unresolved. ·
1 The exact numbers of species in Callithrix and Mico is disputed.
m More species are recognized by some workers; the red co lobus for example has been classified as a single species with 14 subspecies, or as 4 distinct species.
• Some authorities place all baboons in a single species Papio hamadryas. Five baboon species are recognized in this book.
• The most recently discovered species, Rhinopithecus strykeri (from Myanmar), has yet to be fully described.
• The western lowland gorilla is now widely recognized as a distinct species (Gorilla gorilla).The second, more easterly species (G. beringe1) consists of two subspecies.
q The siamang was traditionally placed in its own genus, Sympha/angus, but is included in Hylobates here.
' Genetic and morphological differences between Bornean and Sumatran orang-utans lead most taxonomists to place them in two separate species: Pongo pygmaeus
and P. abelii.
