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C HAPTER 1 The of T HE T

in the Laboratory Context OF AXONOMY P

Colin Groves RIMATES School of Archaeology and Anthropology, Australian National University, Canberra, ACT 0200, Australia

3

What are ? D Taxonomy: THE OF EFINITION The biological Organizing nature species Taxonomy means classifying . It is nowadays

commonly used as a synonym for , though Disagreement as to what precisely constitutes a species P

strictly speaking systematics is a much broader sphere is to be expected, given that the concept serves so many RIMATE of interest – interrelationships, and . At the functions (Vane-Wright, 1992). We may be interested basis of taxonomy lies that much-debated concept, the in classification as such, or in the evolutionary implica- species. tions of species; in the theory of species, or in simply M ODEL Because there is so much misunderstanding about how to recognize them; or in their reproductive, phys- what a species is, it is necessary to give some space to iological, or husbandry status. discussion of the concept. The importance of what we Most non-specialists probably have some vague mean by the word “species” goes way beyond taxonomy idea that species are defined by not interbreeding with as such: it affects such diverse fields as , biogeog- each other; usually, that hybrids between different species raphy, population , ecology, ethology, and bio- are sterile, or that they are incapable of hybridizing at diversity; in an era in which threats to the natural all. Such an impression ultimately derives from the def- world and its biodiversity are accelerating, it affects inition by Mayr (1940), whereby species are “groups of conservation strategies (Rojas, 1992). In the present actually or potentially interbreeding natural popula- context, it is of crucial importance for understanding tions which are reproductively isolated from other such laboratory primates and their husbandry. groups” (the Biological Species Concept). Mayr never

The Laboratory Copyright 2005 Elsevier ISBN 0-1208-0261-9 All rights of production in any form reserved P0800261_01 7/14/05 8:00 AM Page 4

actually said that species can’t breed with each other, with which they share their range (Carr and Hughes, indeed he denied that that this was in any way a neces- 1993). Evidently in the not-too-distant past blacktail sary part of ; he merely said that, females joined whitetail breeding herds and, while the under natural conditions, they don’t. whitetail phenotype was strongly selected for, the black- Reproductive isolation, in some form, stands at the tail mtDNA has remained in the population, basis of what a species is. Having said this, it must be documentation of the hybridization event. admitted that it is no longer possible to follow Mayr’s In Primates, also, there are examples of hybridiza- concept as definitive. In a recent book (Groves, 2001, tion in the wild. A good example of the first case, see especially Chapter 3) I sketched the main reasons Cercopithecus ascanius (Redtail ) and C.mitis why this is so: () in , has been described in detail by Struhsaker et al. (1988). The two monkeys, which • It offers no guidance for the allocation of allopatric are widely sympatric, meaning that they live in the same populations. areas over a wide range, interbreed at quite noticeable • Many distinct species actually do breed with each levels, yet remain separate and clearly distinguishable other under natural conditions, but manage to and no one has ever proposed to regard them as any- remain distinct. RIMATES thing but distinct species. This case is not unlike that

P • The interrelationships of organisms under natural of the North American deer, mentioned above. conditions are often (usually?) unknown. These are two examples – one non-Primate, one • Many species do not reproduce sexually anyway. Primate – of pairs of distinct species which manage to remain distinct over wide areas even though there is Allopatry gene-flow between them. Much more common (or,

AXONOMY OF better, more readily documented) are cases where pairs T To say that two populations are allopatric means that of species occupy ranges that are largely separate but

HE their geographic distributions do not overlap – they are

T meet along their margins (parapatric), and interbreed entirely separate. This means that they do not have the where they do so. Interbreeding varies from occasional chance to breed with each other, even if they wanted to. 4 to full zones, and such cases have, unlike the There is, for example, no way of testing whether hybridization-in- cases, been regarded as evi- Macaca fuscata (of Japan), M.cyclopis (of Taiwan) and dence that reproductive isolation does not exist, so the M.mulatta (the Rhesus , of the East Asian two species should be merged into one. But there is mainland) are actually different species or not; they are ODEL no difference, in principle, from the hybridization-in-

M classified as distinct species in all major checklists, but sympatry cases. there is no objective way of testing this classification The classic study of a is that of under the Biological Species Concept. two mice, Mus musculus and Mus domesticus, across RIMATE Indeed, this is the usual situation: populations that the Jutland peninsula, Denmark (see summary in P differ, in some respect, from one another and are, by Wilson et al., 1985). The hybrid zone, as measured relevant criteria, closely related are usually allopatric. by and protein alleles, is very narrow; yet To take demonstrable reproductive isolation, the req- the mtDNA of the southern species, M.domesticus, uisite criterion under the Biological Species Concept, introgresses well across the boundary, and across the as the sine qua non of species status would be to leave seaway (the Skagerrak) into Sweden. This suggests the majority of living organisms unclassifiable except both that hybridization has been occurring, and that EFINITION OF THE by some arbitrary fiat. M.musculus has been expanding its range, and the D hybrid zone has been moving south since before the sea Natural interbreeding broke through separating Denmark and Sweden in the early Holocene. There has been no selection against The two common species of North American deer hybridization during this long period. (Odocoileus virginanus, the Whitetail, and O.hemionus, In a well-studied Primate example, two , the Blacktail) are found together over a wide geo- Papio hamadryas (Hamadryas ) and P.anubis graphic area, and are always readily distinguishable; yet (), are parapatric and hybridize where molecular studies have found evidence that there has their ranges meet in Ethiopia, the hybrid zone being been hybridization. For example, in Pecos Country, not more than a few kilometres wide. The two taxa are west Texas, four out of the nine whitetails examined adapted to more arid and more mesic environments, had mitochondrial DNA characteristic of the blacktails respectively, and the hybrid zone travels up and down P0800261_01 7/14/05 8:00 AM Page 5

the Awash River according to whether there has been a an element of process, whereas the objective aspect is the run of dry seasons or a run of wet seasons, but remains mere existence of diagnosable difference. more or less the same width. This case is therefore not The second common misunderstanding is that unlike that of the two mice in Denmark. Unlike the species are now being defined by degree of difference. Cercopithecus example, the two baboon taxa have been They are not. They are being defined by the status of shuffled back and forth between subspecies and species the difference, whether the candidates for species status (compare Jolly, 1993 and Groves, 2001). Yet what is can be diagnosed or not. There is, for example, no stan- the difference, really? dard genetic distance above which species status is involved and below which it is not. The third misunderstanding is that species must still be in some way reproductively isolated. The interbreeding What are species? criterion obviously dies hard. The baboon example and

others show that diagnosability exists irrespective of the T HE The phylogenetic persistence of the ability to hybridize. Their separateness T

is genetic rather than necessarily reproductive. OF AXONOMY species concept Groves (2001) noted that some Primate taxono- mists have already begun employing the phylogenetic Most attempts to modify the definition of a species species concept, particularly those working on South have been modifications of the Mayr concept, and relied American monkeys, and made proposals as to what a on reproductive status (see Groves, 2001, Chapter 3). full classification of the might look like. These P

Even without the practical problems summarized proposals should be regarded as a first step and are not RIMATES above, such definitions seem inherently flawed because in any way intended as definitive. they appeal to the process of how species come to be, or are maintained, when surely they should be recognized by the pattern of what they actually are. It was put suc- What are subspecies? cinctly by Cracraft (1983): “ produces taxo- 5 nomic entities, defined in terms of their evolutionary

differentiation from other such forms. These entities Subspecies are geographic segments of species that dif- D

should be called species . . . A species is the smallest fer from one another as a whole, but not absolutely. THE OF EFINITION diagnosable cluster of individual organisms within which The two criteria are: there is a parental pattern of ancestry and descent”. This • They are geographic populations (or groups of popu- is the Phylogenetic Species Concept. lations), not morphs within a single population. “Diagnosable” means 100% different in one or • They do not differ absolutely; the subspecies alloca- more heritable characters. It implies that there are fixed tion of an isolated individual is probabilistic only. genetic differences, though it does not require that they P

be demonstrable here and now in the form of DNA What proportion of one population of a species must be RIMATE sequences (given advances in knowledge, presumably distinguishable from others, in the same species, before they will be in the fullness of time). It is as nearly objec- they can be considered subspecies? This is rather arbi- tive as the evidence permits. The only query that can arise trary, although Mayr’s (1963) 75% rule – that 75% of M is whether a “parental pattern of ancestry and descent” individuals must be distinct from all those in other ODEL exists, and this is as close to inference as the concept populations – is widely adhered to. approaches. Cracraft (1983) argues against the recognition of In this concept, we cease to use the species as a subspecies: if a population is absolutely distinct, so that hypothesis of relationship: each diagnosable entity is rec- all individuals can be objectively allocated, then it is a ognized as a species, and hypotheses of relationships are full species; if not, then it is not an objective entity in reserved for some other level, whether a formal taxonomic any sense. Other adherents of the phylogenetic species rank or an informal grouping such as “species-group”. concept are less dismissive. Groves (2001) takes the There are three common misunderstandings about position that if two populations (or groups of popula- the Phylogenetic Species Concept. First, that the diag- tions) are distinguishable most of the time then it is nostic character states of a species must be evolution- valuable to dignify them with subspecific names. arily derived (evolutionary novelties). A moment’s There is a pleasing symmetry about this. Compared reflection shows that their evolutionary status introduces with traditional (subjective) arrangements, a system under P0800261_01 7/14/05 8:00 AM Page 6

which the phylogenetic species is employed and sub- categories) are plural nouns. Superfamily names end in species are considered useful categories (if less objec- –oidea, families in –idae, subfamilies in –inae and tive), the number of taxa does not change but the tribes in –ini. former subspecies, that are 100% different, are raised Genera, families and orders are quite different sorts to the rank of species. As species, not subspecies, are the of categories from species. They are artificial where units with which conservationists, biogeographers, field species are objective and they are groupings where and the like – including those concerned species are entities. It has been recognized, since the work with captive husbandry – generally work, this seems of Hennig (1966) that the function of these “higher entirely appropriate. categories” is to cluster species according to their degree of relatedness, i.e. into monophyletic groups (mono- phyletic = descended from a unique common ancestor; a monophyletic group is a group, for example, of Nomenclature species, which include not only but all the descendants of a common ancestor). A species has two names (binomial). The first is that of Formerly, were placed, alone, in the

RIMATES the (see below) and the second denotes the , while “great ” (, P species itself. Macaca mulatta, Macaca cyclopis and and orangutan) were placed in a separate family, Macaca fuscata refer to three different species of the Pongidae. It is clear, from molecular and other studies, genus Macaca. that orangutan, not , was the first to separate If we need to recognize subspecies, a third word is from this group, so the family Pongidae is not mono- simply added onto the end of the binomial. Macaca phyletic. Hence, no primatologist with any taxonomic

AXONOMY OF fuscata yakui is the subspecies from Yakushima, a small understanding would today recognize the family T island of southern Japan. It is claimed that most, but Pongidae, at least in its traditional sense. Instead, “great HE

T not all, of these individuals are distinguishable from apes” and humans are together placed in the family those on the main Japanese islands, which must now be Hominidae. 6 designated Macaca fuscata fuscata. Formerly, the order Primates was divided into The subspecies whose subspecific name repeats the two suborders: Prosimii (incorporating , name of the species is called the nominotypical sub- and ) and Anthropoidea (incorporating monkeys species, and its distribution (by definition) includes the and apes, including humans). It is evident today that

ODEL region whence the species was first described (called the tarsiers share a common ancestor with “Anthropoidea”

M type locality). which they do not share with lemurs and lorises, so the suborder Prosimii is not monophyletic. Hence, no primatologist with any taxonomic understanding would RIMATE today recognize the suborder Prosimii. Instead, tarsiers P How to classify and “Anthropoidea” are placed together in one suborder, Haplorrhini, while lemurs and lorises are placed in a species separate suborder, . The question that has recently been asked is where Once these entities have been delineated, they must be does a genus, or a family, begin and end? It is surprising arranged into groups. These groups are called genera that such a crucial question has so rarely been posed. EFINITION OF THE (singular, genus). A species may also be so isolated from The most logical answer, espoused by Goodman et al. D other species that it occupies a genus by itself. (1988), is that a genus or a family should have a certain Genera, in turn, are grouped into families and fam- time depth. Their proposal was adapted and modified ilies into orders. Most families include a large number of by Groves (2001), who suggested that a genus is genera, so are divided into subfamilies; these may in turn a group of species whose last common ancestor lived be divided into tribes, if required. The order Primates around the -Pliocene boundary, and a family is divided into suborders, these into infraorders, and is a group of genera whose last common ancestor lived these in turn into superfamilies. around the -Miocene boundary. Goodman A genus is a Latin or Latinized noun in the nomi- et al. (1988) also proposed time depths for tribes and native singular. It forms the first word in the binomial for the infra-, sub- and super-ranks. Groves (2001), species name (or trinomial subspecies name). Families however, considered that, as these are ranks inserted and orders (and their various sub- and superordinate only for convenience, as when, for example a family P0800261_01 7/14/05 8:00 AM Page 7

contains a large number of genera which are better dubbed “slow”, can move with surprising speed when handled by grouping them in some way, it is unneces- pressed; both types can bite hard, and the bite of Slow sary to designate time depths for them. lorises is toxic (Alterman, 1995). Time depths are sometimes ascertained from fossil evidence, but more usually from molecular clocks. The and Otolemur major families of Primates are unaffected by adopting a time/rank criterion, but there are implications for some The four species of Galagidae (bushbabies) that are genera. sometimes kept in laboratories are: At the end of the chapter an appendix presents a • Galago senegalensis (). They are controversial outline classification of Primates to genus. actually found all over western, northeastern and southeastern , are grey with yellow limbs, and

A commentary on genera dark eye-rings with a white stripe between them. They T are agile and make long hops. Gestation is 142 days HE

commonly housed and they usually have single births. T in laboratories • Galago moholi (Moholi Bushbaby), from southeastern OF AXONOMY and southern Africa, are more buffy with larger ears Microcebus and more prominent face pattern. They are agile and make long hops. Gestation is 125 days and they The nocturnal mouse lemurs (genus Microcebus) are the nearly always give birth to twins. smallest living Primates and are sometimes kept in labo- • Otolemur crassicaudatus (Brown ), P

ratories, where they must be carefully maintained on an RIMATES from southeastern Africa. They are very large, bushy- and diet. They are studied for their unusual tailed, big-eared and brown with a pale face. They do metabolism (Perret and Aujard, 2001) and for their not hop. Gestation is 135 days and they usually bear reproductive physiology (Aslam et al., 2002), particu- twins or triplets. larly the environmental cues that control their reproduc- • Otolemur garnettii (), from tive seasonality. They commonly, but not invariably, eastern Africa, is similar to O.crassicaudatus but is 7 experience lowered metabolic rates during the dry season rather smaller, shorter-eared, more greyish-toned

and, in preparation for this, they store up fat in the tail. D and has a face that is not pale. It sometimes hops. Knowledge of mouse- taxonomy has grown THE OF EFINITION Gestation is 130 days; usually producing single steadily over the past ten years. In 1990, two species were births. known, one in the dry forests of western and southern Madagascar and one in the rainforests of the east. By 2000, it had been shown that there are seven species Saimiri in the western forests alone (Rasoloarison et al., 2000) Squirrel monkeys are agouti-coloured (“agouti” means and further biodiversity can be predicted for the east- that their hairs are banded, usually with black and yel- P ern forests. RIMATE lowish), with characteristic white faces with a black muz- Other genera of Malagasy lemurs are probably zle, hence their German name Totenkopfaffen meaning housed in a few laboratories but, in general, this cannot

“death’s-head monkeys”. They are easily kept in labo- M be recommended as their husbandry is not problem-free. ratories but they need space and to be kept in social ODEL groups. Their diet is fruit and some leaves, and they and Nycticebus catch , often on the wing. A supply of live insects in the laboratory can keep them occupied for quite a Slender and Slow lorises are the only Asian strepsir- while, and so forms a source of behavioural enrichment rhines. Like mouse lemurs, they are nocturnal. Slender for them. lorises, of which there are two species (L.tardigradus in There are five species of squirrel monkey, as follows: the wet zone of and L.lydekkerianus in the dry zone of Sri Lanka and in southern ), feed 1. Gothic type, characterized by a white face-mask, almost entirely on insects, especially ants (Nekaris and forming a high arch above each eye, and a bushy tail Rasmussen, 2003), plus some vegetable matter. Slow tuft. lorises, of which there are three species (Groves, 2001) a. Saimiri sciureus (Common squirrel monkey). This are more vegetarian, especially frugivorous, but also is the widespread species of the South American require some prey. Lorises, despite some being rainforests, mainly north of the Amazon, but P0800261_01 7/14/05 8:00 AM Page 8

extending south of the lower course of the season lasts less than a week, while in S.boliviensis, it Amazon. Body colour is greyish or greenish to extends over two months. In both species the males put reddish agouti, crown greenish or greyish agouti, on fat around the shoulders in the breeding season often mixed with black, and ears are tufted. (“fatted males”) and compete vigorously for matings. Hands, feet and forearms are orange or yellowish Finally, there is a bizarre and unexpected difference or merely tinged with this tone. in the males’ threat display. The male S.boliviensis utters b. Saimiri ustus (Bare-eared squirrel monkey). This a whining threat to other males but, in S.sciureus, the species is from south of the Amazon, west of the dominant male spreads his legs and subjects a subordi- R. Xingu. It is larger than the previous species and nate male to a penile erection. This can be elicited by is distinguished by its untufted ears and the grey presenting the male with a mirror, and he will perform colour of the thighs which contrasts with the the display to his mirror image. body tone. The behaviour of S.oerstedti is different again, as c. Saimiri oerstedti (Central American squirrel mon- Boinski and Cropp (1999) record, but this species is key). This comes from isolated areas in Costa Rica IUCN-Endangered and on CITES Appendix I, so can- and . The body colour is reddish or not be held in laboratories.

RIMATES orange-red; the crown is generally black (but P agouti in some males) and the ears are tufted. 2. Roman type, characterized by white colour restricted Aotus to a narrow line above the brows and no bushy tuft. Night monkeys ( monkeys, Douroucoulis) are of d. Saimiri boliviensis (Black-capped squirrel special biomedical interest because some of them have monkey). These come from , and proved susceptible to falciparum . Because AXONOMY OF

T far western . The body colour is greenish- susceptibility has been found to depend on species, correct taxonomic determination is vital, but this is HE agouti but with black tones of varying intensity, T the crown is black or just black-bordered, in often extremely difficult. In addition, Defler et al. (2001) some males, and the tail is often blackish on the showed that the names of the various species/subspecies 8 dorsal surface. from and Panama have been wrongly applied e. Saimiri vanzolinii (Black squirrel monkey). These and they also argue that what have commonly been are restricted to the region where the R. Japurá regarded as subspecies are actually distinct species. The meets the upper Amazon and are distinguished by following arrangement according to Groves (2001), was ODEL their black dorsal colour. modified according to Defler et al. (2001): M Probably only two of these species (S.sciureus and 1. Grey-necked group, in which the sides of the neck are S.boliviensis) are likely to be held in laboratories, but it greyish, like the body. RIMATE is very important to distinguish them clearly because a. Aotus zonalis. Defler et al. (2001) showed that P their behaviours are very different. Boinski and Cropp this short-haired , which lacks any (1999) have summarized the differences and empha- interscapular whorl or crest, is the one from low- sized their significance for laboratory husbandry and land Panama. It was formerly, but wrongly, called other purposes. In S.boliviensis, females are more aggres- Aotus lemurinus lemurinus, and is probably a distinct sive, form social coalitions and are dominant to males, species, although generally similar in external whereas in S.sciureus the males are dominant. The male appearance to the real A.lemurinus. Karyotype: EFINITION OF THE in S.boliviensis is more peripheral in the social group 2n =55–56. It has low susceptibility to malaria. D and, in the wild, males emigrate from their social groups. b. Aotus lemurinus. These come from the Andes of In S.sciureus, it is the females that emigrate and the males Colombia, and perhaps Panama. The darkest defend the young keenly and are well integrated into the species, it has long shaggy pelage and lacks any group. Males of S.boliviensis can be kept in all-male interscapular whorl or crest. Underparts are yel- groups, but those of S.sciureus cannot. Bisexual groups lowish to pale orange and this colour extends of S.sciureus range in number from about 15 to 50, whereas down the inner aspects of limbs to knee and those of S.boliviensis are typically over 50 in number. elbow but does not extend forward to the throat. S.sciureus are more fertile, breeding every year, and Hands and feet are dark. Individuals may infants are weaned after six months. S.boliviensis usu- be more greyish or more reddish and the devel- ally breed every second year and the infants are weaned opment of a dark dorsal stripe is variable. after about 19 months. In S.sciureus the breeding 2n= 58. They have low susceptibility to malaria. P0800261_01 7/14/05 8:00 AM Page 9

The species is not the same as the one described species that occurs in the vicinity of the impor- by Hershkovitz (1983) and by Groves (2001) as tant centre of Iquitos), was even described Aotus lemurinus lemurinus, but the one that has from laboratory specimens and is resistant to become known as Aotus hershkovitzi. falciparum malaria. c. Aotus griseimembra. This “species” is confusing i. Aotus nigriceps. These come from Brazil south of and may be a totally spurious association of speci- the Amazon and west of the R. Tapajós, into Peru. mens, from the lowlands of eastern Colombia, These are iron-grey with a brownish wash on the which resemble A.zonalis but lack the dark hands mid dorsal region, and a very conspicuous facial and feet. It includes specimens of uncertain origin pattern of broad black stripes and white areas. with 2n = 52–54 karyotype, known to be suscepti- Underparts are whitish and orange, this zone ble to falciparum malaria (see Def ler et al., 2001). extending up the sides of the neck. 2n = 51 (male), Much more information is required on what phe- 52 (female).

notype occurs where and has what genotype. j. Aotus azarae. These occur south of the Amazon, T HE d. Aotus brumbacki. Known only from the highlands between the Tapajós and Tocantins Rivers, into T

of Meta, Colombia, at 467–1543 metres. It is dis- Bolivia and . They are distinguished by OF AXONOMY tinguished by its interscapular crest; its longitudi- an interscapular whorl. They are very like Aotus nal gular gland with hairs parted on either side of nigriceps but may be more buffy or olive with it; its yellowish, not white, spots above the eyes black digits and deep red underparts but this and its pale orange underparts extending to the zone does not extend far up the sides of the neck posterior part of the throat and by 2n = 50. or the inner aspects of limbs, beyond the elbows P

Highly susceptible to falciparum malaria. and knees. 2n=49 (male), 50 (female). There are RIMATES e. Aotus vociferans. It occurs from southern Colombia three geographic forms which may even be dis- into northern parts of Brazil and Peru. It is distin- tinct species: the Paraguayan A.a.azarae with its guished by its interscapular whorl and circular shaggy pelage; A.a.boliviensis from Bolivia, more throat gland, with hairs radiating from its brown- olive with contrasting grey limbs; and A.a.infula- ish colour, black hands and feet and thicker crown tus from southern Brazil, with more white on 9 stripes than other species of the grey-neck group, the face.

orange-white underparts extending to wrists and D It will be seen that there is a great deal still to be learned ankles, black tail that is reddish under its proximal THE OF EFINITION about night monkeys, particularly with regard to half and 2n = 46. Highly susceptible to falciparum matching up karyotypes with place of origin. The dif- malaria. ferential susceptibility of different species to malaria is f. Aotus trivirgatus. This is found from eastern perhaps predictable from the altitude at which each Colombia east to Guyana. It is distinguished lives. They are all thought to be basically nocturnal, from all other members of the grey-neck group and live in mated pairs. Their inquisitiveness, docility by its strongly contrasting orange dorsal stripe. and tameability make them very attractive charges for P Hands and feet are dark, face pattern very incon- RIMATE laboratory handlers. spicuous and underparts are orange. Malaria sus- ceptibility and karyotype are not known. 2. Red-necked group, in which the red of the underside M Callithrix ODEL extends not only well forward on the throat, but also up onto the sides of the neck. In the 1960s, four species of true marmosets were g. Aotus miconax. These occur in a small region in recognized: Callithrix jacchus (Common marmoset) northwestern Peru. They are light brownish or red- from the Atlantic seaboard of Brazil, C.argentata and dish grey, bushy-tailed, and have an inconspicu- C. humeralifer (Silvery and Tassel-eared marmosets) ous face pattern and pale orange underparts. from the southern Amazonian forests, and Cebuella pyg- Malaria susceptibility and their karyotype are not maea (Pygmy marmoset) from the upper Amazon trib- known. utaries. The latest count is 21 with 6 in the Atlantic h. Aotus nancymaae. These are from a small area forests, 14 Amazonian, plus the same pygmy species, along the Peru-Brazil border. They are very like now called Callithrix pygmaea. A.miconax but greyer, with a dark median dorsal Molecular data show that the Atlantic and zone and 2n = 54. This species, which is com- Amazonian marmosets are not closely related and monly held in laboratories (because it is the the pygmy marmoset is more closely related to the P0800261_01 7/14/05 8:00 AM Page 10

Amazonian group and the three species-groups were Other species of tamarin, mainly of the Saguinus separated around five million years ago (Goodman et al., fuscicollis group (the Saddleback Tamarins, of which 1998), which is just too recently for generic separation. there may be one or several species, all very small in Consequently, it is best to place them all in one genus, size, 350g compared to about 500g in the cottontop), Callithrix, with three species-groups or subgenera may also be kept in laboratories. (Callithrix [Atlantic], Mico [Amazonian] and Cebuella [Pygmy]). The old, “traditional” classification, which placed the pygmy marmoset in the genus Cebuella, and the rest combined under Callithrix, is unacceptable. These are the monkeys that are often lumped together Probably the only species likely to be held in labo- as vervets, and formerly included in the genus ratories is the Common Marmoset, Callithrix jacchus. Cercopithecus. Unlike the latter, however, they live This has a pelage mottled in black, grey and yellow, a mainly in open country or savannah-woodland and not black-and-white striped tail, a white patch on the fore- in dense forest. The distribution of the genus is through- head and long white tufts arranged in an arc above out the non-forested areas of sub-Saharan Africa. There and in front of the ears. It has a wide range in eastern- are several species which may well differ physiologically

RIMATES most Brazil, in dry coastal and inland forest. It lives in and in disease susceptibility: P mated pairs which bear twins and these are carried Chlorocebus sabaeus, the African , a about at first by the father and later by the older siblings, West African species, found from Senegal east probably being transferred to the mother essentially only for suck- to Ghana. It is a grizzled golden greenish colour with ling (“helper system”). The sexual maturation of the off-white underparts, a yellow tail-tip, and yellow older offspring is suppressed if they are not allowed to cheek directed upward from a whorl in front

AXONOMY OF disperse. of the ears and over the temples. The scrotum is very T An important part of the diet for all marmosets pale blue. HE

T is tree exudates (gum, resin), and the lower incisor and Chlorocebus aethiops, the Monkey. This is canine teeth are long and narrow, arranged in a semi- found in eastern Sudan and western Ethiopia. It is griz- 10 circle, and used for digging into bark to allow exudates zled olive with the crown yellow, grey limbs, white to run out. This notching activity is almost constant, so underparts, and a white tuft at the base of the tail; there marmosets must be supplied with sturdy wooden is a white brow-band, which is continuous with the very perches and supports in captivity. They scent-mark long, white cheek whiskers, and there is a sparse white

ODEL their assiduously and when placed in a new moustache. The scrotum is sky blue.

M cage a marmoset will spend the initial period marking Chlorocebus djamdjamensis is a rare species from all over it, substituting the previous owners’ scent with the Bale Mountains, Ethiopia. its own. Chlorocebus tantalus, the , is found RIMATE from Ghana to Sudan, Uganda and northwestern . P Saguinus It looks very like the Grivet but the white, sinuous brow- band is separated from the cheek whiskers, which are Tamarins are related to true marmosets but lack the stiff, yellowish and black-tipped, by a black line from eye for bark notching. Seventeen species are to temples. The scrotum is sky blue like the Grivet’s and currently recognized but this is very likely an under- is surrounded by long orange hairs. estimate. The most familiar species in laboratories is Chlorocebus pygerythrus, the true , is EFINITION OF THE Saguinus oedipus, known as the Cottontop or Pinché, found widespread from eastern Ethiopia south to D which has an almost bare (sparsely haired) black face, the southern tip of Africa. This differs from the Grivet an agouti grey-brown body, red rump and thighs, white and the Tantalus by the limbs not being grey, by the limbs and underside, and a long “Iroquois” hairstyle. dark hands, feet and tail tip, the short bright red hair In the wild it is confined to a tiny area in Colombia, in the perineal region, and the short white cheek from the Atlantic coast to the lower Magdalena and whiskers which join the brow-band to form a continu- Cauca rivers. It spontaneously develops colon cancer, ous face-ring which grades into the greenish speckled which has rendered it of great biomedical interest, neck and crown. The scrotum is turquoise blue. The and from about 1960 to 1975 some 30–40,000 were Ethiopian and Kenyan subspecies, C.p.hilgerti, tends to imported to the USA. It is now regarded as endangered be pale brownish yellow; the Tanzanian C.p.rufoviridis by IUCN, and there are probably more in captivity averages more fawn and the underparts are often red- than there are in the wild. der, the cheek whiskers longer; and the southern P0800261_01 7/14/05 8:00 AM Page 11

African C.p.pygerythrus is more grey or olive. There are Papio ursinus, the , comes from also some small-sized subspecies on coastal offshore southern Africa (south of the Zambezi). It is as large islands. as the Anubis or larger and is black in the far south, Chlorocebus cynosuros, the , is from becoming fawn to the north with no mane. Angola, western , and the savannah country of The Anubis, Yellow and Chacma Baboons (“savan- southern D.R.Congo. This is like the Vervet but paler, nah baboons”) live in multimale, multifemale troops and above all has a pale, blotched face (all other species with dominance hierarchies. The Hamadryas lives in have a black face), and pale palms and soles; the cheek harems, the surplus males associating in bachelor groups, whiskers are long, and directed upward and backward. and a number of harems and bachelor groups come The scrotum is lapis blue. together to form large bands. The basic behavioural Long regarded as a minor biomedical source, this difference is that hamadryas males herd females, and this genus has leapt into prominence because of the discovery has striking consequences for the social organization as

of the SIV “African green monkey”. There is a need to well as the temperament of both sexes. Guinea Baboons T HE examine populations of other species for SIVs, but this are poorly studied but may be more like hamadryas. T

will be conveniently done by trap-release investigations This may not exhaust the biological differences OF AXONOMY in the wild, rather than in the laboratory. between baboon taxa. It has been reported that the Cape of Good Hope baboons, which are P.ursinus, Papio mate in a mount series, with ejaculation apparently occurring only at the end of the series. In contrast, Baboons have long been favoured research subjects. those in Nairobi National Park (P.anubis), typically P

Studies on reproductive biology, in one species of baboon ejaculate after a single mount (Hall and DeVore, 1965) RIMATES (Birrell et al., 1996), have been facilitated by housing but these 40-year-old observations need to be con- them in their natural social groups, minimizing undue firmed and extended. stress and thus enabling apparently normal processes of pregnancy, including hormonal levels, to be continu- Cercocebus ously monitored, as briefly described by Horam et al. 11 (1992). Baboons are widely used for these and other Mangabeys are now regarded as belonging to two distinct

research areas in the laboratory. The potential draw- genera: the arboreal group, Lophocebus, are related to D back is their large size, requiring large cages, preferably Papio, while the semi-terrestrial mangabeys separated THE OF EFINITION with outdoor runs, if they are to be kept under humane from the only four million years ago and are conditions. They are strikingly intelligent compared to therefore regarded, by Goodman et al. (1998), as con- Platyrrhines, and even to Vervets, and, for full behav- generic. I shall adopt this classification here. The prior ioural enrichment, they require social interaction and generic name is Cercocebus, of which is intellectual stimulation. This includes having their therefore a subgenus. food scattered, so that they have to forage for it, rather The only that is widely kept in the lab- P than simply collecting it from a tray. There are five oratory is the , Cercocebus atys, which RIMATE species of baboon: is found in the far west of Africa, from Senegal east to Papio hamadryas, the Hamadryas, Mantled or the Nzo-Sassandra river system in the Ivory Coast. Its Sacred Baboon. This comes from arid environments M

endemic SIV is thought likely to be the source of ODEL around the Red Sea in northeast Africa and Arabia. human HIV2. The male is grey with a huge mane and white cheek whiskers, red face and rump skin. The female is browner and maneless with a black face. Macaca Papio papio, the , is from far western are, without a doubt, the most widespread lab- Africa. It is reddish, with a large mane in the male. oratory Primates. The species-groups are well-separated, Papio anubis, the Anubis or Olive Baboon, is from with strong morphological and behavioural differences Mali east to Ethiopia and Kenya. It is much larger than between them. There is every indication of a considerable Hamadryas and Guinea Baboons and is olive brown, time depth (see below). with a mane in adult male. Papio cynocephalus, the , is from 1. African macaques. There is just one species, the Tanzania south to the Zambezi. It is yellowish with (M.sylvanus) of the Atlas region, white underparts and white cheeks and no mane. which is now endangered. P0800261_01 7/14/05 8:00 AM Page 12

2. Asian macaques. M.mulatta, the Rhesus Monkey, comes from the northern half of the Indian subcontinent, • M.nemestrina group: These are short-tailed, long- northern Burma, northern Indochina, and faced macaques. In the non- species, the much of . It has a short curly tail and is crown hairs radiate from a central whorl and there brown with a reddish tone on its hindparts, are cheek whiskers. The female experiences sexual including hindlegs. skin swellings at mid cycle, like baboons and M.cyclopis, the Formosan Rock Macaque, mangabeys. comes from Taiwan. It is darker than the M.silenus, the Lion-tailed Macaque. This is a Rhesus without its reddish hindparts and has highly from the Western bushy cheek whiskers and a longer tail. Ghats of India. It is black, with long grey cheek M.fuscata, the , is from whiskers. Honshu, Shikoku, Kyushu, Yaku, and many M.nemestrina, the Southern Pigtail, is from offshore islands of central Japan. It is yellowish Peninsular Malaysia, Sumatra, Bangka and brown with no reddish tone on its hind parts, Borneo. It is agouti brown, much darker in the and has a very short, furry tail. median dorsal region, with blackish crown hair RIMATES • M.sinica group: tails of this group vary in length

P and short cheek whiskers. and they usually have a whorl on their crown and M.leonina, the Northern Pigtail, is from main- a pink or brown face. There is periodic reddening land Southeast . It is uniform agouti of the genital area at mid cycle, but no sexual golden brown with brown crown, fairly long swelling. cheek whiskers and a red streak at the lateral M.sinica, the , is from Sri corner of each eye. AXONOMY OF Lanka. Their tail is longer than the head and T Mentawai Island: Macaques are represented by body and there is a prominent whorl on the

HE two species, both critically endangered, from

T crown, with long hairs radiating from it and the Mentawai Is. west of Sumatra. reaching forward to brows in a “toupée”. Sulawesi Macaques: These are six or seven M.radiata, the , is from south- 12 species from Sulawesi, most of them now ern India (south of the range of Rhesus endangered. The Crested Macaque or “Black Monkey; the approximate dividing line is the ”, M.nigra, was formerly kept in a few lab- Tapti and Krishna Rivers). Their tail is usually, oratories to investigate the occurrence of spon-

ODEL but not always, as long as the head and body taneous diabetes. The only non-endangered M and the crown hair is short in front, leaving a species, the , M.tonkeana, is very short-haired forehead. kept in a few laboratories. M.assamensis, the Macaque, is from cen- RIMATE • M.fascicularis: the Long-tailed or Crab-eating tral east to southern China and north P Macaque is from which includes . It is much larger and shorter-tailed , southern Vietnam and central Burma, to than others of the group, often lacking the western and southern Indonesia and the Philippines. “toupée”, but with prominent cheek whiskers. Their tail is longer than head and body which is brown M.thibetana, the Milne-Edwards’s Macaque, is with grey or black tones with crown hair directed from central China. It is the largest macaque, backward and outward, sometimes with a small crest very short-tailed, dark brown with a bushy pale EFINITION OF THE and there is a light spot at the inner corner of the beard and cheek whiskers. D eyelid. There are no sexual swellings. Morales and Melnick (1998), noting that the • M.arctoides: the Stumptail or Bear Macaque is fossil record reports a split between African and Asian from mainland Southeast Asia. This is an odd macaques (i.e. between M.sylvanus and the rest) of at species with a short tail, shaggy dark brown pelage, least 5.5 million years, dated the other major separa- a red face, which becomes dark brown, often tions as follows: blotchily, in sunlight and it becomes bald at matu- Sulawesi macaques at 4.5 Ma, hence the nemestrina rity. There are no sexual swellings. group somewhat before this: • M.mulatta group: These are short-tailed, rather short-faced macaques with crown hair directed M.fascicularis from the mulatta + sinica groups at backwards and a pink or red face. There are no 3.5 Ma. periodic sexual swellings. The mulatta and sinica groups at 2.5 Ma. P0800261_01 7/14/05 8:00 AM Page 13

M.fuscata from M.mulatta at 0.5 Ma—after the while , and orangutans are rele- beginning of diversification within M.mulatta itself gated to the family Pongidae, to (both M.fuscata and M.cyclopis are closer, in mtDNA, 2. a -based scheme in which all are placed in to the Chinese than to the Indian M.mulatta). Hominidae, with orangutans put in their own subfamily, Ponginae, and the others combined in The really astonishing molecular finding is that a subfamily with three tribes Gorillini, M.arctoides has the mtDNA of M.fascicularis but Panini, , to the Y- DNA of the M.sinica group (Tosi 3. the time-depth-based scheme in which not only are et al., 2000). The favoured hypothesis is that the the three tribes abolished, along with a family division species is a stabilized hybrid between M.fascicularis between “great apes” and “lesser apes” (), but and proto – M.assamensis/thibetana – so far the only two of the genera are now even combined. plausibly hypothesized case of a species of hybrid origin among Primates. Whereas all Primates have special husbandry needs, T

for housing, socialisation, and behavioural enrichment, HE

it is certainly true that the needs of apes, whether human T

Homo OF AXONOMY or non-human, are beyond those of other Primates. Put Goodman et al. (1998) calculated, on the basis of their simply, there is more potential for an ape, such as molecular data, that the ancestors of humans and chim- a chimpanzee or human, to experience distress, bore- panzees separated only six million years ago. As this is dom, discomfort or pain than other Primates. Whether less than the time for generic separation, they proposed or not we consider human rights, such as described in

to combine them into one genus: there would thus be Cavallieri and Singer (1993) and enacted, in modified P a single genus () with two subgenera (Homo and form, in law in New Zealand, to be appropriate for RIMATES ). Groves (2001), adopting a looser time-frame for other apes, humane concerns dictate that, at the very generic separation, retained Pan as a distinct genus. least, we approach their treatment with an extra degree The proposal to sink Pan into Homo was, however, of care. endorsed by Watson et al. (2001). Chen and Li (2001), on the basis of 53 non-transcribed DNA segments, cal- 13 culated the human–chimpanzee separation at 4.6 to Correspondence 6.2 Ma, while Wildman et al. (2003) put it at between D Any correspondence should be directed to Colin THE OF EFINITION 5 and 6 Ma. On the time-depth criterion, there seems Groves, School of Archaeology and Anthropology, no longer any reason to keep the two genera separate. Australian National University, Canberra, ACT 0200. The subgenus Pan has two species: Homo (Pan) Tel: (+612) 6125 4590. [email protected] troglodytes and H.(P.) paniscus. Both are currently kept in laboratories: H.paniscus (Bonobo or Pygmy Chim- panzee) only for research, and H.troglodytes

(Common Chimpanzee) which is unfortunately no P References RIMATE longer “common” but mostly now in retirement from research, except for a few instances for continuing Alterman, L. (1995) In Alterman, I., Doyle, G.A. and Izard,

research in infectious disease such as HIV and hepatitis. M M.K. (eds), Creatures of the Dark: The Nocturnal The question of whether it is ethical to use chim- ODEL , 413–424. New York: Plenum Press. panzees in discomforting, disabling or potentially termi- Aslam, H., Schneiders, A., Perret, M., Weinbauer, G.F. and nal research, seems more sharply focused if they are Hodges, J.K. (2002). Reproduction 123, 323–332. now to be regarded as a species of the human genus. In Birrell A., Hennessy, A., Gillin, A.G., Horvath, J.S. and fact, the evidence for self-awareness, and other human- Tiller, D.J. (1996). J. Med. Primatol. 25, 287–293. like cognitive and emotional qualities in chimpanzees, Boinski, S. and Cropp, S.J. (1999). Int. J. Primatol. 20, gorillas and orangutans has been available for some years 237–256. (see, for example, Russon et al., 1996) and research in Carr, S.M. and Hughes, G.A. (1993). J. Mamm. 74, these is not even in question. All that has changed is the 331–342. taxonomy. Indeed, it is interesting to reflect how tax- Cavallieri, P. and Singer, P. (1993). The Great Ape Project: onomy has moved from: Equality Beyond Humanity. Chen, F-C. and Li, W-H. (2001). Am. J. Hum.Genet. 68, 1. a grade-based, anthropocentric scheme whereby 444–456. humans belong alone in one family, Hominidae, Cracraft, J. (1983). Curr. Ornithol. 1, 159–187. P0800261_01 7/14/05 8:00 AM Page 14

Defler, T.R., Bueno, M.L. and Hernández-Camacho, J.I. Rasoloarison, R., Goodman, S.M. and Ganzhorn, J.U. (2001). Neotrop. Primates 9, 37–52. (2000). Int. J. Primatol. 21, 963–1019. Goodman, M., Porter, C.A., Czelusniak, J., Page, S.L., Russon, A.E., Bard, K.A. and Parker, S.T. (1996). In Schneider, H., Show, J., Gunnell, G. and Groves, C.P. Russon, A.E., Bard, K.A. and Parker, S.T. (eds), Reaching (1998). Mol. Phyl. Evol. 9(3), 585–598. into Thought: The Minds of the Great Apes. Cambridge: Groves, C. (2001). Primate Taxonomy viii, Washington, DC: Cambridge University Press. Smithsonian Institution Press. Struhsaker, T.T., Butynski, T.M. and Lwanga, J.S. (1988). Hall, K.R.L. and DeVore, I. (1965). In I. DeVore (ed.), In Gautier-Hion, A., Bourlière, F., Gautier, J-P. and Primate Behavior, pp 53–110. New York: Holt, Rinehart Kingdon, J. (eds), A Primate Radiation: Evolutionary & Winston. Biology of the African , pp 477–497. New York: Hennig, W. (1966). Phylogenetic Systematics. Urbana: Cambridge University Press. University of Illinois Press. Tosi, A.J., Morales, J.C. and Melnick, D.J. (2000). Mol. Hershkovitz, P. (1983). Two new species of night monkeys, Phyl. Evol., 17, 133–144. genus Aotus (, Platyrrhini): a preliminary report Vane-Wright, R.I. (1992). Species . In Global on Aotus taxonomy. Amer. J. Primatol. 4, 209–43. Biodiversity 1992: a Report Compiled by the World Horam, C.J., Harewood, W.J., Phippard, A.F. and Conservation Monitoring Centre, pp 13–16. B. Groombridge

RIMATES Horvath, J.S. (1992). Aust. Primatol. 7, 1:11. (ed.), London: Chapman & Hall.

P Jolly, C.J. (1993). In Kimbel, W.H. and Martin, L.B. (eds), Watson, E.E., Easteal, S. and Penny, D. (2001). In Species, Species Concepts, and Primate Evolution, Tobias, P.V., Raath, M.A., Moggi-Cecchi, J. and pp 67–107. New York: Plenum Press. Doyle, G.A. (eds), Humanity from African Naissance to Mayr, E. (1940). Amer. Nat. 74, 249–278. Coming Millenia, pp. 307–318. Italy: Firenze University Mayr, E. (1963). Animal Species and Evolution. Harvard: Press. Belknap Press. Wildman, D.E., Uddin, M., Liu, G-z., Grossman, L.I. and AXONOMY OF Morales, J.C. and Melnick, D.J. (1998). J. Hum. Evol. 34, Goodman, M. (2003). PNAS 100, 7181–7188. T 1–28. Wilson, A.C., Cann, R.L., Carr, S.M., George, M., HE

T Nekaris, K.A.I. and Rasmussen, D.T. (2003). Int. J. Gyllensten, U.B., Helm-Bychowski, K.M., Higuchi, R.G., Primatol. 24, 33–46. Palumbi, S.R. and Prager, E.M. (1985). Biol. J. Linn. Soc. Perret, M. and Aujard, F. (2001). Amer. J. Physiol. 281, 26(4), 375–400. 14 R1925–R1933. ODEL M RIMATE P EFINITION OF THE D P0800261_01 7/14/05 8:00 AM Page 15

SUBFAMILY Aotinae Appendix GENUS Aotus SUBFAMILY Callitrichinae An outline classification of living Primates: GENERA: Callithrix, Callimico, Leontopithecus, SUBORDER Strepsirrhini Saguinus INFRAORDER FAMILY FAMILY GENERA: Pithecia, Chiropotes GENERA: Microcebus, Mirza, Cheirogaleus, FAMILY Allocebus, Phaner SUBFAMILY Alouattinae FAMILY GENUS Alouatta GENERA: Lemur, Hapalemur, Prolemur, SUBFAMILY Atelinae Eulemur, Varecia GENERA: Ateles, Brachyteles, Lagothrix, Oreonax T FAMILY Lepilemuridae HE 1 GENUS Lepilemur T

FAMILY FAMILY Cercopithecidae OF AXONOMY GENERA: , Propithecus, Avahi SUBFAMILY INFRAORDER Chiromyiformes TRIBE FAMILY Daubentoniidae GENERA: Cercopithecus, , GENUS Daubentonia , Chlorocebus, Miopithecus, Allenopithecus

INFRAORDER Lorisiformes P

FAMILY TRIBE RIMATES GENERA: Loris, Nycticebus, Perodicticus, GENERA: Papio, , Lophocebus, Arctocebus, Propotto Cercocebus, Macaca FAMILY Galagidae SUBFAMILY GENERA: Galago, Euoticus, Otolemur, GENERA: Colobus, Procolobus, Piliocolobus, Galagoides Presbytis, Semnopithecus, Trachypithecus, 15 SUBORDER Haplorrhini Pygathrix, Rhinopithecus, Nasalis, Simias

INFRAORDER FAMILY Hominidae D FAMILY Tarsiidae SUBFAMILY Hylobatinae THE OF EFINITION GENERA: Tarsius, Cephalopachus, unnamed GENERA: , Hoolock, third genus Symphalangus, Nomascus INFRAORDER Simiiformes SUBFAMILY Homininae Platyrrhini1 TRIBE Pongini FAMILY Cebidae GENUS Pongo TRIBE Hominini SUBFAMILY Cebinae P RIMATE GENERA: Cebus, Saimiri GENERA: Homo, Gorilla 1Platyrrhini and Catarrhini are left unranked. This is a perfectly acceptable procedure when too many divisions are needed for the number of ranks ordained. M ODEL P0800261_01 7/14/05 8:00 AM Page 16