BLBS036-Voevodin April 8, 2009 13:57 Part I: Introduction to Primatology and Virology COPYRIGHTED MATERIAL BLBS036-Voevodin April 8, 2009 13:57 BLBS036-Voevodin April 8, 2009 13:57 1 Classification of Nonhuman Primates 1.1 Introduction that the animals colloquially known as monkeys and 1.2 Classification and nomenclature of primates apes are primates. From the zoological standpoint, hu- 1.2.1 Higher primate taxa (suborder, infraorder, mans are also apes, although the use of this term is parvorder, superfamily) usually restricted to chimpanzees, gorillas, orangutans, 1.2.2 Molecular taxonomy and molecular and gibbons. identification of nonhuman primates 1.3 Old World monkeys 1.2. CLASSIFICATION AND NOMENCLATURE 1.3.1 Guenons and allies OF PRIMATES 1.3.1.1 African green monkeys The classification of primates, as with any zoological 1.3.1.2 Other guenons classification, is a hierarchical system of taxa (singu- 1.3.2 Baboons and allies lar form—taxon). The primate taxa are ranked in the 1.3.2.1 Baboons and geladas following descending order: 1.3.2.2 Mandrills and drills 1.3.2.3 Mangabeys Order 1.3.3 Macaques Suborder 1.3.4 Colobines Infraorder 1.4 Apes Parvorder 1.4.1 Lesser apes (gibbons and siamangs) Superfamily 1.4.2 Great apes (chimpanzees, gorillas, and Family orangutans) Subfamily 1.5 New World monkeys Tribe 1.5.1 Marmosets and tamarins Genus 1.5.2 Capuchins, owl, and squirrel monkeys Species 1.5.3 Howlers, muriquis, spider, and woolly Subspecies monkeys Species is the “elementary unit” of biodiversity. 1.5.4 Titis, sakis, and uakaris Strictly speaking, the only natural grouping of animals 1.6 Concluding remarks is a population. The species is defined as a group of populations whose individual members interbreed and 1.1. INTRODUCTION produce fertile offspring in their natural habitat. In prac- The order Primata includes humans and animals that tice, the use of this definition may be problematic, for are our closest living “relatives” in the animal kingdom. example, for clearly distinct and fertile hybrids existing There are many definitions of a primate. None of them in the wild. As a result, there are multiple disagreements are completely satisfactory. As a result, there are dis- regarding species rank for the morphologically and/or agreements regarding inclusion of some animal taxa in behaviorally distinguishable nonhuman primate (NHP) the order Primata. At the same time, it is indisputable populations.3,4,10,12 3 BLBS036-Voevodin April 8, 2009 13:57 4 Part I / Introduction to Primatology and Virology The nomenclature of NHP species is binomial, that is, species level, we follow the classification described in the scientific names of the species consist of two Latin literature.4,12 words. The first capitalized word identifies the genus (plural—genera). The second, lowercase word identifies the species within the genus. The scientific names of 1.2.1. Higher Primate Taxa (Suborder, Infraorder, species are italicized. For example, Macaca mulatta is Parvorder, Superfamily) the species mulatta within the genus Macaca. The primates are divided into two suborders: Strep- The nomenclature of NHP subspecies is trinomial. sirrhini and Haplorrhini (Figure 1.1). Strepsirrhini The full scientific name of a subspecies name consists are divided into three infraorders: Lemuriformes of three words: the binomial species name and the third (lemurs), Chiromyiformes (aye-ayes), and Lorisiformes word identifying the subspecies. For example, the com- (loris). Haplorrhini are divided into two infraorders: mon chimpanzee species (Pan troglodytes) is usually di- Tarsiiformes (tarsiers) and Simiiformes (simians, i.e., vided into four subspecies: Pan troglodytes troglodytes, monkeys and apes). The problematic group is tarsiers, Pan troglodytes schweinfurthii, Pan troglodytes verus, also called tree shrews. There is no agreement as and Pan troglodytes vellerosus. The names of the sub- to whether or not they belong to the primate order. species are usually written in abbreviated form, for ex- Placing tarsiers together with simians is also disputed. ample, P. t. troglodytes and P. t. schweinfurthii.The Traditionally, lemurs, aye-ayes, lories, and tarsiers (if notion of subspecies is very useful for understanding the latter are included in the primates) are considered as the natural history of simian viruses. prosimians. In addition to the scientific names, virtually all pri- The simian part of primate classification starts at the mate species and many subspecies have common or ver- parvorder level. The simians are divided into Platyrrhini nacular names. The common names are obviously dif- (literally “broad or flat-nosed”) and Catarrhini (liter- ferent in various languages; however, the English names ally “downward-nosed”). All Platyrrhini species live are used predominantly in the scientific literature.11 For in South America—hence their common name the example, the common name for Macaca mulatta is rhe- New World monkeys (NWMs). There are no Catar- sus monkey; its capitalized version, Rhesus Monkey, is rhine species in the New World, except African green also used. Some simian species have more than one com- monkeys (AGMs), which were introduced to several mon name; for example, Papio hamadryas is called the Caribbean islands (St. Kitts, Nevis, and Barbados) in his- Sacred Baboon or Hamadryas Baboon. Despite the in- torically recent times (seventeenth century). All African trinsic ambiguity of common names, they are useful, for and Asian simian species, except apes, are Old World example, for describing NHPs whose taxonomic status monkeys (OWMs). is undetermined or controversial. Common names are The division into monkeys and apes is formalized at also easier to pronounce and memorize than the Latin the superfamily level: the members of Cercopithecoidea binomial designations. superfamily are monkeys while the members of Homi- Ideally, the hierarchy of primate taxa should reflect noidea superfamily are apes (Figure 1.2). the evolutionary history. In such cases, classification All 152 currently recognized OWM species are in- would be invariant. However, the incompleteness of cur- cluded in one family—Cercopithecidae. This family rent knowledge allows multiple hierarchies of primate is divided into two subfamilies: Cercopithecinae and taxa—hence the existence of different classifications of Colobinae (Figure 1.2). There are 11 Cercopithecinae primates. Most of the inconsistencies between various genera and 10 Colobinae genera. Cercopithecinae gen- classifications are located at levels higher or lower than era with 42 chromosomes diploid karyotype (Papio, species. Taxa whose rank is higher than species are “ar- Theropithecus, Mandrillus, Cercocebus, Lophocebus, tificial” in the sense that their definitions are based on and Macaca) are combined in the tribe Papionini14,35 subjectively chosen criteria. (Figure 1.3). The tribe level is not universally used in In this book, we mainly follow Groves’ classification the classifications of primates. For instance, it is not of primates which is the most widely used.10 This clas- included in Groves’ classification. However, the term sification includes 375 simian species (Tables 1.1–1.4). Papionini is commonly used in the descriptions of Information on NHP subspecies is included only if it simian immunodeficiency virus (SIV) and other simian is relevant in a context of simian virology. At the sub- retrovirus hosts. BLBS036-Voevodin April 8, 2009 13:57 1 / Classification of Nonhuman Primates 5 Figure 1.1. Higher primate taxa (order, suborder, infraorder, and parvorder). Shaded boxes—taxa which include monkeys and apes. Figure 1.2. Catarrhini taxa (down to genus level). BLBS036-Voevodin April 8, 2009 13:57 6 Part I / Introduction to Primatology and Virology Ta b l e 1 . 1 . Old World Monkeys: Subfamily Cercopithecinae Genus/Species Common Name Geographical Distribution Chlorocebus African green monkey C. aethiops Grivet monkey or grivet Sudan, Eritrea, Ethiopia C. cynosuros Malbrouck monkey S DRC,* Angola, N Namibia, Zambia C. djamdjamensis Bale Mountains vervet Ethiopia C. pygerythrus Vervet monkey or vervet Ethiopia, Somalia, Kenya, Tanzania, Zambia, Zimbabwe, RSA† C. sabaeus Green monkey Senegal, Guinea-Bissau, Guinea, Sierra Leone, Liberia, Cote d’Ivoire, Ghana C. tantalus Tantalus monkey Ghana, Togo, Benin, Nigeria, Cameroon, CAR,‡ Kenya Cercopithecus C. albogularis Sykes’ monkey Ethiopia to RSA, S&E DRC, NW Angola C. ascanius Red-tailed monkey Uganda, DRC, Zambia, Angola, CAR, W Kenya C. campbelli Campbell’s monkey Senegal, Liberia, Cote d’Ivoire C. cephus Mustached guenon Gabon, R of Congo,§ S Cameroon, Equatorial Guinea, SW CAR, NW Angola C. denti Dent’s monkey DRC, Rwanda, W Uganda, CAR C. diana Diana monkey Sierra Leone, Liberia, Cote d’Ivoire C. doggetti Silver monkey DRC, S Burundi, NW Tanzania, Rwanda, S Uganda C. dryas Dryas monkey DRC C. erythrogaster White-throated guenon S Nigeria, Benin C. erythrotis Red-eared guenon S&E Nigeria, Cameroon, Bioko Isl (Equatorial Guinea) C. hamlyni Hamlyn’s monkey E DRC, Rwanda C. kandti Golden monkey DRC, Uganda, Rwanda C. l’hoesti L’Hoest’s monkey E DRC, W Uganda, Rwanda, Burundi C. lowei Lowe’s monkey Cote d’Ivoire, Ghana C. mitis Blue monkey DRC, Kenya, Rwanda, N Angola, NW Zambia C. mona Mona monkey Ghana, Togo, Benin, Nigeria, Cameroon C. neglectus De Brazza’s monkey SE Cameroon, R of Congo, DRC, Equatorial Guinea, Gabon, Uganda, N Angola, W Kenya, SW Ethiopia, S Sudan C. nictitans Greater spot-nosed monkey Liberia, Cote d’Ivoire, Nigeria, DRC, CAR, Equatorial Guinea, Cameroon C. petaurista Lesser spot-nosed monkey Gambia, Guinea, Guinea-Bissau, Sierra Leone, Liberia, Cote d’Ivoire, Ghana, Togo C. pogonias Crowned monkey SE Nigeria, Cameroon, Equatorial Guinea, N&W Gabon, W DRC C. preussi Preuss’s monkey Cameroon, Equatorial Guinea C. roloway Roloway monkey Cote d’Ivoire, Ghana C. sclateri Sclater’s guenon SE Nigeria C. solatus Sun-tailed monkey Gabon C. wolfi Wolf’s monkey DRC, NE Angola BLBS036-Voevodin April 8, 2009 13:57 1 / Classification of Nonhuman Primates 7 Ta b l e 1 . 1 . (Continued) Genus/Species Common Name Geographical Distribution Erythrocebus Patas E.