African Zoology

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A new species for South Africa (: Strepsirhini: Galagidae)

Fabien Génin, Ayabulela Yokwana, Nokuthula Kom, Sébastien Couette, Thibault Dieuleveut, Stephen D Nash & Judith C Masters

To cite this article: Fabien Génin, Ayabulela Yokwana, Nokuthula Kom, Sébastien Couette, Thibault Dieuleveut, Stephen D Nash & Judith C Masters (2016) A new galago species for South Africa (Primates: Strepsirhini: Galagidae), African Zoology, 51:3, 135-143

To link to this article: http://dx.doi.org/10.1080/15627020.2016.1232602

Published online: 31 Oct 2016.

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Download by: [Bibl de L'Univ de Bourgogne] Date: 02 November 2016, At: 00:49 African Zoology 2016, 51(3): 135–143 Copyright © Zoological Society Printed in South Africa — All rights reserved of Southern Africa AFRICAN ZOOLOGY ISSN 1562-7020 EISSN 2224-073X http://dx.doi.org/10.1080/15627020.2016.1232602

A new galago species for South Africa (Primates: Strepsirhini: Galagidae)

Fabien Génin1*, Ayabulela Yokwana1, Nokuthula Kom1, Sébastien Couette2, Thibault Dieuleveut3, Stephen D Nash4 and Judith C Masters1

1 African Initiative for Ecology and Speciation, Department of Zoology and Entomology, University of Fort Hare, Alice, South Africa 2 Ecole Pratique des Hautes Etudes, Laboratoire Paléobiodiversité et Evolution and UMR uB CNRS 6282 “Biogéosciences”, Université de Bourgogne, Dijon, France 3 Emirates Center for Wildlife Propagation, Missour, Morocco 4 10 Bayles Avenue, Stony Brook, New York, USA * Corresponding author, email: [email protected]

The primate fauna of South Africa has historically been viewed as comprising three diurnal cercopithecoid taxa – chacma baboons (Papio ursinus), vervet (Chlorocebus pygerythrus) and samango monkeys (Cercopithecus albogularis) – and two nocturnal lorisoid species – the thick-tailed greater galago (Otolemur crassicaudatus) and the southern lesser galago (Galago moholi). Here we report the positive identification of a third galago species within South Africa’s borders: the Mozambique dwarf galago or Grant’s galago, Galagoides granti (Thomas and Wroughton, 1907). The taxon was previously held to be restricted to Mozambique, eastern Zimbabwe, Malawi and Tanzania, but we have also observed it in the sand forest of Tembe Elephant Park and the Tshanini Community Reserve, near the Mozambique border. The species was formerly mistaken for Galago moholi, erroneously (we believe) extending the range of the latter species into northern KwaZulu-Natal. In South Africa the two small are unlikely to have overlapping ranges: Galago moholi prefers dry savanna woodlands, whereas Galagoides granti is apparently confined to dry sand forest. However, both species may coexist with the larger and more widespread Otolemur crassicaudatus, an inhabitant of moist savanna, forest edge and thicket. The true South African ranges of both small galago species need to be ascertained.

Keywords: dwarf galagos, Galagoides, sand forest, Tembe, Tshanini

Introduction

Conservation of South Africa’s biodiversity requires and olfactory signals. Speciation hence may not involve the accurate identification of the units that comprise obvious changes in gross morphology, giving rise to cryptic it. Most studies of biodiversity focus on species as the species complexes (Henry 1985; Masters and Spencer units of conservation, not only because they consist of 1989), or groups of reproductively independent species with lineages with independent evolutionary histories and fates very similar morphologies. Loud calls are by far the most (Simpson 1951; Wiley 1978), but also because they have accessible, reliable and non-invasive identifiers of galagid unique suites of ecological adaptations and relationships species (Masters 1993; Bearder et al. 1995; Masters to the environment (Schluter 2001). Species emergence and Couette 2015); indeed, galagos owe their colloquial and extinction are driven by environmental change, and name ‘bushbabies’ to the specific long-distance advertise- speciation is an irreversible process that fixes the range ment call of the thick-tailed greater galago, Otolemur of genetic variation and adaptive potential for a species’ crassicaudatus. Pelage colouration – one of the primary metapopulation (Futuyma 1987). Hence, for conserva- characters used by taxonomists to classify variation – is tionists to construct an accurate picture of the environ- likely to have evolved in galagids under selective pressure mental requirements for the survival of a community, it is for concealment from predators while the are crucial that they have the correct taxonomic information resting during the daytime, rather than as an indicator of for that community. specific distinction. Hence, taxa such as Otolemur spp., For many species, morphology is a good indicator of which occupy less dense and highly seasonal forests that specific identity, but this is not always the case. In nocturnal lose their leaves in the dry season, show discrete regional species such as galagos (bushbabies or nagapies), and probably seasonal patterns of colouration on the head, active when light intensity is low, the location, attraction dorsum and tail, as well as in the colours of the hands and and identification of potential mating partners is seldom feet. Dwarf galagos, which inhabit coastal and/or evergreen dependent on visual signals, particularly those that are forests, show much less regional variation, although there encoded into the animals’ morphology. Instead, communi- is a notable increase in rufous colouration the closer the cation among species members is largely based on vocal animals are found to the Equator.

African Zoology is co-published by NISC (Pty) Ltd and Taylor & Francis 136 Génin, Yokwana, Kom, Couette, Dieuleveut, Nash and Masters

South Africa’s galagid fauna was previously held to comprise only the thick-tailed greater galago (Otolemur crassicaudatus) and the southern lesser galago (Galago moholi). The Mozambique dwarf galago or Grant’s galago (Galagoides granti; Figure 1) was previously believed to be restricted to Mozambique, the eastern highlands of Zimbabwe, Malawi and southern Tanzania (Smithers 1983; Skinner and Smithers 1990; Skinner and Chimimba 2005). Kyle (1996) reported sightings of Galago moholi in northern KwaZulu-Natal, a record that struck us as anomalous given the species’ preference for dry savanna woodland. More detailed surveys of Tembe Elephant Park and the nearby Tshanini Community Reserve revealed that the small-bodied galagids present in these areas are in fact Galagoides granti (Thomas and Wroughton, 1907). In this contribution we present the results of our first field study of this new addition to South Africa’s primate fauna. We abbreviate the genus Galagoides as Gs to distinguish it from the abbreviation used for Galago (G).

A brief systematic history of Grant’s galago Galagoides granti was described as Galago granti by Thomas and Wroughton (1907: 286) as ‘a member of the moholi group, with an unusually bushy black-tipped tail.’ It was named for Captain CHB Grant who collected a series of eight specimens at Coguno, in Inhambane province in southern Mozambique, one of which became the type of the new taxon. In 1931, Ernst Schwarz, one of the twentieth century’s most fervent taxonomic lumpers, relegated Gs. granti to subspecies status within G. senegal- ensis (Schwarz 1931), a practice that was widely followed (Allen 1939; Roberts 1951; Hill 1953; Smithers and Tello 1976; Petter and Petter-Rousseaux 1979; Smithers 1983). Also subsumed under G. senegalensis by Schwarz (1931), Hill (1953) and subsequent authors were G. moholi and three taxa now considered to be allied with G. granti: Gs. cocos (from Kenya), Gs. nyasae (from Malawi) and Gs. zanzibaricus (from Zanzibar). Kingdon (1971) recognised Gs. zanzibaricus as a distinct species, a proposal supported by Groves (1974) who suggested that Gs. granti was likely to be the southern representative of the Zanzibar species. Galagoides zanzibaricus granti was the followed for more than 20 years (Meester et al. 1986; Jenkins 1987; Skinner and Smithers 1990; Groves 1993). Following recommendations by Bearder et al. (1996), Honess and Bearder (1996) and Kingdon (1997), Gs. granti has been treated more recently as a distinct species within the Zanzibar group (Masters and Bragg 2000; Groves 2001; Grubb et al. 2003; Groves 2005; Butynski et al. 2006, 2013; Nekaris 2013; Masters and Figure 1: Adult Galagoides granti in Tshanini Community Reserve. Couette 2015; Pozzi et al. 2015). Photo by Hajarimanitra Rambeloarivony

Methods our initial search for dwarf galagos in the reserves. The Study sites region consists of flood plains based on clay, covered in Captain Grant recorded the following observation of the parts with ancient, parallel, east–west-orientated sand Gs. granti type locality: ‘Inland from Inhambane the country dunes – the relicts of an ancient sea shore. It forms the is composed of more or less undulating, sandy flats, southernmost extent of a much larger domain extending densely bushed and timbered’ (Thomas and Wroughton well into Mozambique. The vegetation is a complex mosaic 1907: 285). This description fits Tembe Elephant Park and of dry forest dominated by large endemic sand forest Tshanini Community Reserve equally well, and inspired newtonias (Newtonia hildebrandtii), thicket, woodland African Zoology 2016, 51(3): 135–143 137 and savanna grassland. Similar, naturally fragmented sand forests occur in a few other localities in northern KwaZulu-Natal, sometimes in protected areas (e.g. Mkuze and Ndumo). They form the southern limit of distribu- (2) tion for a number of locally rare species, such as the suni (Neotragus moschatus), the four-toed elephant shrew (Petrodromus tetradactylus) and the plain-backed sunbird (Anthreptes reichenowi).

Preliminary survey 2 In this contribution we report the results of preliminary observations carried out from 2011 to 2014. We observed Grant’s galagos only in the dry sand forest and dense woodland of Tembe Elephant Park (six nights) and the Tshanini Community Reserve (12 nights). We conducted our initial studies in Tembe Elephant Park (27.0486° S, 32.4222° E). While populations of both Otolemur crassi- caudatus and Gs. granti were both accessible and relatively KWAZULU-NATAL abundant, so were the populations of lions (Panthera leo) 2 and elephants (Loxodonta africana), which hindered our nocturnal surveys. We therefore moved our field site to Tshanini Community Reserve, which is situated approxi- mately 6 km to the south of the southern border of Tembe Elephant Park (Figure 2; see also Gaugris et al. 2004). Our observations focused on sleeping sites, because they form the focus of activity at the beginning and end of the galagos’ nocturnal activity period.

2 Recording methods Animals were first recorded opportunistically, between A A January 2012 and March 2014, and then systemati- cally, during the population density survey in September 2014. We recorded vocalisations using a SEINHEISER MKE600 semi-directional microphone and a ROLAND R-26 0 50 100 digital recorder. We focused on three selected calls, most frequently emitted by Gs. granti and well described in the 32 33 literature: the incremental loud call regarded as specifically diagnostic (Bearder et al. 1995), and the more conserved Figure 2: Map showing the sites where Galagoides granti has ‘buzz screech’ and ‘yap’, used as alarm calls by other been observed in South Africa. Tembe Elephant Park and Tshanini Galagoides and Galago species. Community Reserve are indicated by arrows

Population survey Because of the complexity of the habitat, we surveyed the last hour of the nocturnal activity period. Over these portions of a single 9.6 km transect twice daily (evening and 6 d, we conducted a total of 12 h of early evening surveys morning) that crossed three subhabitats: (1) sand forest: (between 18:00 and 22:00), 12 h of early morning surveys two patches of tall sand forest and a portion of low sand (between 02:00 and 06:00), and a single 6 h diurnal survey forest and thicket; (2) savanna: Terminalia–Combretum (06:00–12:00) for a comparison of background noise and savanna grassland; and (3) woodland: a dense woodland to mark the survey path with biodegradable tape. We rich in creepers and lianas on clay marking a transition walked the path at an average speed of approximately between the first two subhabitats along the dry bed of an 1 km h−1, stopping every 100 m to record for 5 min. The ancient river. The 9.6 km transect was divided into three 3.2 time taken to cover each 3.2 km survey sector was approxi- km parts that could be covered in a single survey period. mately 4 h. We also recorded galagos we encountered as To avoid double counts, the boundaries between survey we moved, identified either by calls or by the reflection of sectors were located in areas of unsuitable habitat (open the tapetum in the light of our headlamps. The recording grassland), and each portion had a different subhabitat equipment was turned on each time an was located, constitution (dense sand forest, dense woodland, mosaic of and we approached the subjects when possible. We sand forest and grassland–savanna). recorded the GPS coordinates and height above ground of To optimise the chance of recording the animals, we the animals when they were first sighted. In addition, we conducted recording surveys over a period of 6 d focusing measured the distance from the observer to the occupied on the times when galagos are known to be particularly tree using a BOSCH 80 laser telemeter, to assess visibility active and vocal (Harcourt and Nash 1986), i.e. the first and and correct our estimates of population density in the 138 Génin, Yokwana, Kom, Couette, Dieuleveut, Nash and Masters heterogeneous habitat: the maximum distance of visual Masters 1993; Bearder et al. 1995, 1996). The Mozambique detection measured in each subhabitat was used to dwarf galago has a high-frequency, modulated loud call calculate the width of the survey path and convert linear typical of the Galagoides species east of the African Rift. abundance in individuals km–1 into surface-based popula- This type of call contrasts strongly with the low-frequency, tion density. almost tonal loud call of G. moholi. Mozambique dwarf galagos belong to the cluster of so-called ‘incremental Results callers’ (Bearder et al. 1995; Kingdon 1997): the loud calls are made up of repeated short units given in groups of Sleeping sites and general observations increasing number (increments) (see Figure 3). By contrast, In 24 nights of surveys we identified six sleeping sites, four southern lesser galagos utter a metronomic two-unit bark of which were on the population density survey transect. with a shorter second unit (‘repetitive callers’). All were located in deep tree holes in tall sand forest Incremental calls are most often used as cohesive habitat, situated 3–14 m above ground in living (n = 5) or gathering calls when animals exit (n = 12) or return to (n = 7) dead (n = 1) trees. Of these six sites, four were occupied their sleeping sites. They are also emitted sporadically by groups of three females, one by a female and an throughout the night, probably when animals meet the scent infant (Figure 3), and one by a male. We also found an marks of nearby or affiliated individuals (n = 3). Such calls unoccupied galago branch-nest (probably built by greater always elicited responses from nearby individuals. galagos) in woodland habitat, and three O. crassicaudatus sleeping sites, all in large savanna trees. Buzz screech alarm We observed five social encounters between female The one-unit buzz screech used by the Mozambique dwarf dwarf galagos during the night, which were accompanied by galago is similar and probably homologous to the chow-ha social calls (descending screech, chatter). Foraging animals, alarm call given by G. moholi. The call is shared by all however, were generally observed alone (n = 9). When members of the Gs. zanzibaricus species complex, and foraging, dwarf galagos used all vegetation strata, from is reminiscent of the two-unit, more explosive alarm call the upper canopy to the leaf litter, where they were seen emitted both by Gs. demidoff and Gs. orinus. The buzz foraging for insects (n = 4). They were also observed feeding screech is rather stereotyped but of variable duration, on Combretum molle and Sclerocarya birrea gum (n = 3) sometimes uttered in isolation (in response to a low level and on the nectar of the introduced Agave sisalis (n = 1). of disturbance), but more often associated with yaps, and sometimes with more complex calls (chatter or irregular Population densities emission of short, modulated units and double units The results of our transect surveys are presented in resembling the basic units of the loud call). Table 1. Our values for Gs. granti are similar to other abundance estimates for the species in East Africa (Honess Mobbing yaps et al. 2013), although linear rates of encounter are not In contrast, the mobbing yap is the most phylogenetically directly comparable because the method is very sensitive conserved of all galago vocalisations. It is not peculiar to to variation in visibility. Our data indicate that the overall the Galagoides group, and cannot be used to distinguish population density of the thick-tailed greater galago is much the two small galagos found within South Africa (the higher than that of the Mozambique dwarf galago, but apparent differences observed in Figure 3 are probably an this is essentially due to the higher density of its preferred artefact of sound degradation affecting the transmission of habitat in the subhabitat mosaic. Indeed, Gs. granti was higher frequencies, as the maximum energy occurs around more abundant than O. crassicaudatus within its own 4 kHz in all species). The yap serves as a mobbing call and preferred habitat of tall sand forest. This habitat preference is sometimes used in conjunction with the less frequently is likely to be related to the species’ use of large, hollow emitted buzz screech (n = 5). It was emitted in the presence trees as sleeping sites. Dwarf galagos do venture into more of a ‘parked’ infant, or when an animal’s path was blocked open habitat (seven observations), but only later in the by a human observer. night when foraging. A similar use of habitat is seen in the closely related Gs. zanzibaricus (FG pers. obs.). Discussion

Vocalisations The recent discovery of Grant’s galago within the borders During the population survey, animals were more often of South Africa carries the implication that previous detected by their calls (n = 25) than by their eye shine observations of small-bodied galagos in northern KwaZulu- (n = 6). Figure 3 presents comparative sonagrams of Natal may have been mistakenly attributed to G. moholi, Gs. granti calls recorded at Tshanini Community Reserve erroneously extending the distribution of this species into with various other galago calls, including Gs. granti calls the extreme north-eastern part of South Africa. We hence recorded in southern Tanzania and vocalisations emitted have a situation in which one of South Africa’s relatively by G. moholi. Three calls were selected for analysis on the common small species, the lesser galago or basis that they were most frequently emitted. nagapie, has suddenly become data deficient, as we do not know the true extent of its distribution. We are similarly Loud/advertisement calls ignorant of the extent of the distribution of Gs. granti within Galago loud calls are known to be highly reliable and readily the country’s borders. A pressing research need is thus to accessible indicators of species identity (Zimmermann 1990; determine the ranges of these two species, a task which African Zoology 2016, 51(3): 135–143 139 : ) ): ): ( i i (

i ( n a r oo l g ono n r ag o ago i a l ago i a l a l : ), showing the three call types uttered most frequently by Galagoides granti : ) : ) : )

( f ( c i (

i

n o f a i a r r g an i

ago i ago i a l ago i a l a l spp. and lesser galagos ( Galago moholi Galagoides ): ): : ) i ( i (

i ( n n a a

r r oo l g g ag o ago i ago i a l a l a l the incremental loud call, buzz screech and mobbing yap Figure 3: Comparative sonograms of eastern and western 140 Génin, Yokwana, Kom, Couette, Dieuleveut, Nash and Masters

Table 1: Comparison of Galagoides granti and Otolemur crassicaudatus abundance in Tshanini Community Reserve in three kinds of habitat

Linear density (encounters km−1) Population density (strip width method) (individuals km−2) Species Sand forest Woodland Savanna Sand forest Woodland Savanna Galagoides granti 1.3 1.4 0.2 90.9 21.3 4.2 Otolemur crassicaudatus 0.8 2.8 2.1 54.5 42.7 40.7

Table 2: Average body and skull measurements (±SE) of museum specimens of Galagoides granti and Galago moholi. General body measurements were taken by the collectors on freshly killed specimens and recorded by us from museum records. Skull lengths were measured by us using digital callipers to 0.1 mm accuracy

Average measurement Galagoides granti Galago moholi Head-body length (mm) 153.7 ± 1.64 (n = 50) 147.7 ± 1.46 (n = 50) Tail length (mm) 220.5 ± 2.39 (n = 50) 223.7 ± 1.73 (n = 50) Hind foot length (mm) 58.5 ± 0.54 (n = 50) 57.2 ± 0.68 (n = 50) Ear length (mm) 38.2 ± 0.41 (n = 50) 36.6 ± 0.43 (n = 50) Body weight (g) 146.8 ± 7.14 (n = 20) 153.5 ± 2.52 (n = 50) Total skull length (mm) 42.3 ± 0.24 (n = 38) 39.4 ± 0.19 (n = 50) (prosthion to opistocranion)

requires input from field researchers, wildlife conserva- nasal opening, suggesting that the extended condition is tionists and enthusiasts, in addition to our own continued ancestral. Galagoides spp., as befits their locomotor mode, surveys. To assist field identification of the two small galago have relatively unflexed basicrania and flatter braincases, species, we provide a summary of morphological and whereas the skulls of Galago taxa are more globular, with a behavioural clues to their respective identities. higher braincase and a more flexed basicranium. In the field Galagoides spp. are more quadrupedal Distinguishing South Africa’s two smaller galago species than Galago spp. When they leap from tree to tree, they The two species are very similar in body size; compara- make first contact with the landing surface either with the tive measurements gathered from specimens stored in hands or with all four extremities together. Galago spp., museum collections worldwide are presented in Table 2. by contrast, are specialised ricochetal leapers (Oxnard et The major features distinguishing Gs. granti from G. moholi al. 1990). They swing their hind limbs forward during the are illustrated in Figure 4. Galagoides granti is generally course of the leap and land feet first. This more derived darker and browner than G. moholi with a dark bushy tail locomotion, associated with much longer hind limbs and (see also Figure 1), whereas the dominant colour on the a more globular skull, is an adaptation to moving through head, dorsum and outer surfaces of the limbs of G. moholi relatively open savanna woodland habitat, where the trees is pale grey washed with varying degrees of russet brown, are widely spaced. and the tail is slender and coated with a grizzled mix of The most reliable character for field identification of brown and grey hairs; the limbs are washed with pale Grant’s galago is its distinctive vocal repertoire. The calls yellow. The ventral surface of Gs. granti is yellow to cream- given most frequently, particularly in the presence of an buff, in contradistinction to the white ventrum of G. moholi. observer, are the buzz screech and clearer, high-pitched The shape of the snout is diagnostic. In Grant’s galago it yaps. Similar calls are emitted by G. moholi, however, and is narrow and pointed, and the nasal profile is concave they are not informative of species identity to unfamiliar (Figure 5), whereas lesser galagos have a short, square ears. The loud advertisement call, in contrast, distinguishes muzzle and a straight nasal profile. In both taxa the eyes the two small galagos in South Africa unambiguously. The are surrounded by black circumocular rings, which contrast loud call of Gs. granti is described as incremental because with a white to pale grey stripe that traverses the length new modulated units are added in a complex sequence. of the nose, but in lesser galagos the face is more or less This call, uttered more frequently near sleeping sites and suffused with white. sporadically throughout the night, contrasts markedly with The skulls of the two taxa are readily distinguished. the regularly repeated, monotonous, lower-frequency tonal Galagoides spp. have a relatively large, unreduced M3 that loud call signalling the presence of G. moholi. approximates the molarised P4 in size, whereas the same Finally, the two small galago species also differ signifi- tooth is much reduced in Galago spp., in correspondence cantly in their preferred habitats, which are unlikely to with their shorter snouts. The difference in the nasal coexist within the boundaries of South Africa. The southern profiles is very evident (see illustrations in Smithers 1983; lesser galago is an inhabitant of dry savanna woodland, Skinner and Smithers 1990; Skinner and Chimimba 2005). often riverine woodlands in the driest parts of their range, In Galagoides spp. the premaxillary bones are extended to whereas the Mozambique dwarf galago is a dry forest form a tube that causes the upper jaw to project beyond and dense woodland specialist. Both species may coexist the lower jaw; in Galago spp. the premaxillaries are not locally with the much larger thick-tailed greater bushbaby extended beyond a relictual nub on the midline beneath the (Otolemur crassicaudatus), which is found in a variety of African Zoology 2016, 51(3): 135–143 141

Figure 4: Morphological comparison of Galagoides granti and Galago moholi. Drawings by Stephen D Nash

granti has a clear predilection for mosaics of thicket and tall, mature woodland rich in creepers and lianas, connected to patches of tall dry forest used exclusively during the daytime resting period. The range of the South African population is limited in the west by the eastern escarpment and in the east by the Indian Ocean coastline, confirming a preference for subtropical conditions. Linder et al. (2012) compared the distributions of plants and vertebrates in sub-Saharan Africa, and identified five or six distinct biogeographic regions on the subcontinent, depending on the taxa examined. The ranges of the three South African galago species match two of these regions, but no two species have the same habitat preference, implying that the three lineages colonised South Africa via distinct routes and probably at different times (Pozzi 2016). Linder and colleagues identified a distinct Mozambique biogeographic domain characterised by many endemic plants and birds, but few endemic . In South Figure 5: Lateral view of a Galagoides granti juvenile showing the Africa the Mozambique region is probably confined to the concave nasal profile, the extended upper jaw, and the contrasting Tembe–Tshanini area, the vast majority of it occurring eye rings and nasal stripe. The eye rings darken in maturity further north. (1) Galagoides granti has an exclusively Mozambique habitats (moist savanna woodland, thicket and forest edge). distribution that reaches the western foot of the eastern escarpment in Zimbabwe and Malawi. It is a rare forest Habitat preferences and biogeography of South African and dense woodland specialist localised in South Africa, galagos where we have observed it only in the Tembe and Like other eastern dwarf galagos, Gs. granti prefers Tshanini reserves, which are hence likely to mark the well-wooded habitat for sleeping sites, although the animals southern extreme of the Gs. granti distribution (Figure 2). venture into more open habitat while foraging. Galagoides (2) Galago moholi has a restricted dry Zambezian 142 Génin, Yokwana, Kom, Couette, Dieuleveut, Nash and Masters

distribution excluding the Mozambique domain and Conservation 21: 63–79. matching the distribution of much more open savanna Butynski T, Kingdon J, Kalina J. 2013. Mammals of Africa, vol. II: woodland and miombo. In South Africa, it is restricted to Primates. London: Bloomsbury. Futuyma DJ. 1987. On the role of species in anagenesis. American flood plains and riverine Vachellia karroo (Acacia karoo) Naturalist 130: 465–473. woodland, from Pretoria to Limpopo province. Gaugris JY, Matthews WS, van Rooyen MW, Botma J du P. 2004. (3) Otolemur crassicaudatus has a broad Zambezian distri- The vegetation of Tshanini Game Reserve and a comparison bution including the Mozambique domain. However, its with equivalent units in the Tembe Elephant Park in Maputaland, distribution is patchy and follows deep valleys where South Africa. Koedoe 47: 9–29. its preferred habitat of moist savanna woodland, forest Groves CP. 1974. Taxonomy and phylogeny of prosimians. In: edge and thicket occurs. In South Africa, the species Martin RD, Doyle GA, Walker AC (eds), Prosimian biology. is restricted to areas of Limpopo and Mpumalanga London: Duckworth. pp 449–473. provinces and subtropical KwaZulu-Natal. It coexists Groves CP. 1993. Order Primates. In: Wilson DE, Reeder locally with G. moholi and Gs. granti in the north and the DM (eds), Mammal species of the world: a taxonomic and geographic reference (2nd edn). Washington, DC: Smithsonian north-east of its distribution, respectively. Institution Press. pp 243–277. The KwaZulu-Natal coastal region is characterised by Groves CP. 2001. Primate taxonomy. Washington, DC: subtropical transitional conditions, indicative of climatic Smithsonian Institution Press. fluctuations in the recent past that have left behind a Groves CP. 2005. Order Primates. In: Wilson DE, Reeder great number of isolated, relictual populations of tropical DM (eds), Mammal species of the world: a taxonomic and species (e.g. the green barbet, Stactolaema olivacea). The geographic reference (3rd edn). Baltimore: Johns Hopkins Mozambique dwarf galago is an addition to this already University Press. pp 111–184. impressive list. The northern sand forest has many other Grubb P, Butynski TM, Oates JF, Bearder SK, Disotell TR, Groves rarities of Zambezian (suni, four-toed elephant shrew, CP, Struhsaker TT. 2003. Assessment of the diversity of African red squirrel and African broadbill), or Mozambican (plain- primates. International Journal of Primatology 24: 1301–1357. Harcourt CS, Nash LT. 1986. Social organization of galagos backed sunbird) affinities. Further investigations will in Kenyan coastal forests. I. Galago zanzibaricus. American include a thorough survey of all the sizeable sand forest Journal of Primatology 10: 339–355. fragments in northern KwaZulu-Natal, with a special Henry CS. 1985. Sibling species, call differences, and speciation emphasis on other types of sand forest (e.g. the Mkuze in green lacewings (Neuropoda: Chrysopidae: Crysoperla). and Ndumo riverine sand forest and gallery forest). Evolution 39: 965–984. Such assessments would be particularly valuable as the Hill WCO. 1953. Primates: comparative anatomy and taxonomy, presence of a rare, CITES II protected species may help vol. I: Strepsirhini. Edinburgh: University of Edinburgh Press. to enhance the conservation status of the region. The Honess PE, Bearder SK. 1996. Descriptions of the dwarf galago extreme north of Maputuland is poorly developed and species of Tanzania. African Primates 2: 75–79. deserves more attention, especially targeting the conserva- Honess PE, Bearder SK, Butinsky TM. 2013. Galagoides granti Mozambique dwarf galago (Grant’s dwarf galago). In: Butynski tion of forest habitat. T, Kingdon J, Kalina J (eds), Mammals of Africa, vol. II: Primates. London: Bloomsbury. pp 454–456. Acknowledgements — We acknowledge the important contribu- Jenkins P. 1987. Catalogue of primates in the British Museum tions made by Prof. Dai Harbert, who willingly shinned up trees (Natural History). London: British Museum (Natural History). and faced down elephants in the interests of science, and Greg Kingdon J. 1971. East African mammals: an atlas of evolution in Davies, whose pursuit of sunbirds was crucial to the discovery Africa, vol. I: Primates. London: Academic Press. of dwarf galagos in South Africa. Dr Iris Dröscher, Hajarimanitra Kingdon J. 1997. The Kingdon field guide to African mammals. Rambeloarivony and Tarik Bodasing showed similar fortitude, London: Academic Press. and we are grateful to them for sharing their expertise and their Kyle R. 1996. Sight records of Galago moholi, the lesser photographs. The project was funded by National Research bushbaby, in KwaZulu-Natal. Lammergeyer 44: 39–40. Foundation grants 93924 awarded to FG, and 92541 and 90772 Linder HP, de Klerk HM, Born J, Burgess ND, Fjeldsa J, Rahbek awarded to JCM; grant number GB-TAP 4120 awarded by the C. 2012. The partitioning of Africa: statistically defined Synthesys Program to SC; and an ABIC grant awarded to JCM biogeographical regions in sub-Saharan Africa. Journal of by the Royal Museum for Central Africa through a Framework Biogeography 39: 1189–1205. Agreement with the Belgian Development Co-operation. Masters JC. 1993. Primates and paradigms: problems with the identification of genetic species. In: Kimbel WH, Martin LB (eds), References Species, species concepts, and primate evolution. New York: Plenum Press. pp 43–64. Allen GM. 1939. A checklist of African mammals. Bulletin of the Masters JC, Bragg NP. 2000. Morphological correlates of Museum of Comparative Zoology 83: 1–763. speciation in bush babies. International Journal of Primatology Bearder SK, Honess PE, Ambrose L. 1995. Species diversity 21: 793–813. among galagos with special reference to mate recognition. In: Masters JC, Couette S. 2015. Characterizing cryptic species: Alterman L, Doyle GA, Izard MK (eds), Creatures of the dark: a morphometric analysis of craniodental characters in the the nocturnal prosimians. New York: Plenum Press. pp 331–352. dwarf galago genus Galagoides. American Journal of Physical Bearder SK, Honess PE, Bayes M, Ambrose L, Anderson M. 1996. Anthropology 158: 288–299. Assessing galago diversity – a call for help. African Primates 2: Masters JC, Spencer HG. 1989. Why we need a new genetic 11–15. species concept. Systematic Zoology 38: 270–279. Butynski TM, de Jong YA, Perkin AW, Bearder SK, Honess PE. Meester J, Rautenbach IL, Dippenaar NJ, Baker CM. 1986. 2006. Taxonomy, distribution, and conservation status of three Classification of southern African mammals. Transvaal Museum species of dwarf galagos (Galagoides) in eastern Africa. Primate Monographs 5: 1–359. African Zoology 2016, 51(3): 135–143 143

Nekaris KAI. 2013. Family Galagidae (galagos). In: Mittermeier RA, Simpson GG. 1951. The species concept. Evolution 5: 285–298. Rylands AB, Wilson DE (eds), Handbook of the mammals of the Skinner JD, Chimimba CT. 2005. The mammals of the southern world, part 3: Primates. Barcelona: Lynx Edicions. pp 184–209. African subregion (3rd edn). Cambridge: Cambridge University Oxnard CE, Crompton RH, Lieberman SS. 1990. Animal lifestyles Press. and anatomies: the case of prosimian primates. Seattle: Skinner JD, Smithers RHN. 1990. The mammals of the southern University of Washington Press. African subregion (2nd edn). Pretoria: University of Pretoria Petter J-J, Petter-Rousseaux A. 1979. Classification of the Press. prosimians. In: Doyle GA, Martin RD (eds), The study of Smithers RHN. 1983. The mammals of the southern African prosimian behavior. New York: Academic Press. subregion. Pretoria: University of Pretoria Press. Pozzi L. 2016. The role of forest expansion and contraction in Smithers RHN, Tello JLP. 1976. Check list and atlas of the species diversification among galagos (Primates: Galagidae). mammals of Mozambique. National Museums and Monuments Journal of Biogeography 43: 1930–1941. of Rhodesia, Museum Memoir 8. Salisbury: Trustees of the Pozzi L, Nekaris KAI, Perkin A, Bearder SK, Pimley ER, Schulze National Museums and Monuments of Rhodesia. H, Streicher U, Nadler T, Kitchener A, Zischler H, Zinner D, Thomas O, Wroughton RC. 1907. The Rudd Exploration of South Roos C. 2015. Remarkable ancient divergences amongst Africa. VII. List of mammals obtained by Mr. Grant at Coguno, neglected lorisiform primates. Zoological Journal of the Linnean Inhambane. Proceedings of the Zoological Society of London Society 175: 661–674. 1907: 285–299. Roberts A. 1951. The mammals of South Africa. Pretoria: Trustees Wiley EO. 1978. The evolutionary species concept reconsidered. of “The Mammals of South Africa" Book Fund. Systematic Zoology 27: 17–26. Schluter D. 2001. Ecology and the origin of species. Trends in Zimmermann E. 1990. Differentiation of vocalizations in bush- Ecology and Evoloution 16: 372–380. babies (Galaginae, Prosimiae, Primates) and the significance for Schwarz E. 1931. On the African long-tailed lemurs or galagos. assessing phylogenetic relationships. Zeitschrift für zoologische Annals and Magazine of Natural History 10(7): 41–66. Systematik und Evolutionsforschung 28: 217–239.

Received 8 January 2016, revised 29 August 2016, accepted 1 September 2016 Associate Editor: Ara Monadjem