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Short Communication
A new genus name for pygmy lorises, Xanthonycticebus gen. nov. (Mammalia, primates)
expand article infoK. Anne-Isola Nekaris, Vincent Nijman
‡ Oxford Brookes University, Oxford, United Kingdom
Open Access

Abstract

Lorisiformes are nocturnal primates from Africa and Asia with four genera, with two (Arctocebus and Loris), three (Perodicticus) and nine (Nycticebus) recognised species. Their cryptic lifestyle and lack of study have resulted in an underappreciation of the variation at the species and genus level. There are marked differences between the pygmy slow loris Nycticebus pygmaeus and the other Nycticebus species and, in the past, several authors have suggested that these may warrant recognition at the generic level. We here combine morphological, behavioural, karyotypical and genetic data to show that these contrasts are, indeed, significantly large and consistent. We propose Xanthonycticebus gen. nov. as a new genus name for the pygmy slow lorises and suggest a common name of pygmy lorises. Based on analysis of complete mitochondrial DNA sequences, we calculate the divergence of pygmy from slow lorises at 9.9–10.0%. The median date, calculated for the divergence between Xanthonycticebus and Nycticebus, is 10.5 Mya (range 4.9–21.0 Mya). Xanthonycticebus differs from Nycticebus by showing sympatry with other slow loris species, by habitually giving birth to twins, by showing seasonal body mass and whole body coat colour changes (absent in other species living at similar latitudes) and a multi-male, multi-female social system. Pygmy lorises are easily recognisable by the absence of hair on their ears and more protruding premaxilla. Xanthonycticebus is threatened by habitat loss and illegal trade despite legal protection across their range and all slow lorises are listed on appendix 1 of CITES. The suggested nomenclatural changes should not affect their legal status.

Key Words

conservation, cytotaxonomy, Lorisidae, Lorisiformes, primate taxonomy, Strepsirrhini

Background

Lorisiformes are a group of nocturnal primates with two genera, Perodicticus Bennett, 1831 (three species) and Arctocebus Gray, 1863 (two species) occurring in west and equatorial Africa and two, Loris É. Geoffroy, 1796 (two species) and Nycticebus, É. Geoffroy, 1812 (nine species) occurring in south, east and southeast Asia (Groves 2001; Nekaris 2013; Rowe and Meyers 2016). In west-central Africa, Perodicticus edwardsi Bouvier, 1979 and Arctocebus occur in sympatry and in eastern Indochina, Nycticebus bengalensis (Lacépède, 1800) and N. pygmaeus Bonhote, 1907 occur in sympatry. All other species have allopatric distributions.

At a major international conference on nocturnal primates in 1993, Schwartz and Beutel (1995: 189), at a time when only two species of Nycticebus were recognised, commented that “N. coucang and N. pygmaeus are species that are remarkable for their variability”. Since then, a considerable amount of comparative research has been conducted on the slow lorises, including morphologically (e.g. Ravosa 1998; Groves 2001; Nekaris and Jaffe 2007; Munds et al. 2013; Xie et al. 2013 7), behaviourally (e.g. Fitch-Snyder and Ehrlich 2003; Nekaris et al. 2008; Nekaris et al. 2010; Streicher et al. 2012; Ni et al. 2020; Poindexter and Nekaris 2020) and genetically (e.g. Chen et al. 2006; Perelman et al. 2011; Pozzi et al. 2015; Munds et al. 2018; Munds et al. 2021). Combined, these studies allow us to gain a better understanding of the species and higher-level taxonomy. Recent molecular phylogenetic research has revealed the divergence between genera and between species and, from this, it is evident that one species, the pygmy slow loris N. pygmaeus is anomalous. In combination with karyotypical, behavioural and morphological data, this supports the conclusion that this species is best placed in its own genus.

Although under the Code (International Commission on Zoological Nomenclature 1999), Art. 13.1, we are not obliged to provide a description of a new taxon (it would suffice to provide a bibliographic reference to earlier descriptions), we feel that, in this instance, it may be opportune to give a generic diagnosis.

Order primates Linnaeus, 1758

Suborder Strepsirhini É. Geoffroy Saint-Hilaire, 1812

Family Lorisidae Gray, 1821

Xanthonycticebus gen. nov.

Diagnosis

Morphological synapomorphies to Xanthonycticebus include: (i) skull length consistently less than 55 mm, (ii) diastema between P2 and P3, (iii) long black ears, hairless at the tips (iv) relatively narrow interorbital distance compared to Nycticebus and (v) full seasonal coat colour change including almost complete loss of dorsal stripe (Fig. 1). The species is furthermore distinguished from Nycticebus species by giving birth habitually to twins, frequent sympatry with N. bengalensis (sensu lato) and more rapid locomotion. Regarding multiple births, this trait occurs with varying frequency in primates. Most of the marmosets and tamarins are polyovulatory and twins are the dominant litter size in the wild and most twins are considered dizygotic (Ward et al. 2014; Wahab et al. 2015). Old World monkeys, apes and humans are monovulatory species and while single births are the rule, multiple births do occasionally occur in various species, typically at a rate at, or below one percent (Geissmann 1990). Around two-thirds to three-quarters of these twins are estimated to be monozygotic (Geissmann 1990). This contrasts with twinning in strepsirrhines, as here all, or practically all, are dizygotic (Pasztor and Van Horn 1979). No other species of slow lorises are known to be sympatric, with their distribution similar to gibbons Hylobatidae Gray, 1870 and langurs Presbytina Gray, 1825, which, even though having more recent evolutionary histories, contain multiple genera (Rowe and Meyers 2016). Where nocturnal primate genera or species are sympatric, different locomotor strategies have evolved, allowing reduced competition (Charles-Dominique 1977). Additional differences, as well as those from Loris, are summarised in Table 1.

Figure 1. 

Characteristics of pygmy loris Xanthonycticebus pygmaeus gen. nov. A. Photograph of wild adult male X. pygmaeus from Mondulkiri District, Cambodia and skull from Li Chau, Vietnam (FMNH 32499), compared with Nycticebus javanicus from Garut Regency, Indonesia and skull (RMNH14563) from South Java, Indonesia; and with Loris lydekkerianus nordicus from Trincomalee District, Sri Lanka and skull (FMNH95029) from Jaffna District, Sri Lanka. Features distinctive to Xanthonycticebus include yellowish-orange colour, mid-broad snout with long premaxilla, M2 larger than M1 and ears hairless at the tips; B. Neighbour-joining tree of 175 cytochrome b sequences (alignment 1,068 bp) of Nycticebus, Xanthonycticebus and Loris; C. Neighbour-joining tree of complete mtDNA sequences of Nycticebus, Xanthonycticebus and Loris, with Perodicticus as outgroup, showing considerable divergence of Xanthonycticebus from Nycticebus. All photographs courtesy of K.A.I. Nekaris.

Etymology

The genus name Xanthonycticebus, masculine, refers to the species orange/ish overall colouration and their nocturnal activity pattern; Xanto, Gr. Yellowish-orange; nykt-, Gr., night; kêbos, Gr., monkey (Gainsford 2020). Currently, the most frequently used common name of this genus is pygmy slow loris, followed by the rarely used lesser slow loris or intermediary slow loris. For the common English name, we suggest pygmy loris in order to differentiate the new genus from the two other loris genera (slow and slender lorises). We acknowledge, however, that with the recognition of N. menagensis Munds, Nekaris and Ford 2013, from Borneo, with a minimum adult body mass of 265 g, the small size is no longer a unique feature of the pygmy loris. The most commonly-used name for pygmy lorises in Vietnamese is Cu li nhỏ, in Mnong, it is Tau kless, in Lao, it is Linh lom and in Chinese, it is 小懶猴 / Xiǎo lǎn hóu (Nijman and Nekaris 2016;Thạch et al. 2018).

Table 1.

Summary of key similarities and differences amongst the three Asian lorisiform genera.

Loris Nycticebus Xanthonycticebus Reference
Latitudinal range 6°N–20°N 8°S–28°N 10°N–25°N Ravosa (1998)
Altitudinal range (asl) 0–2,000 m 0–2,400 m 50–1,500 m Nekaris (2013)
Twins Rare but occasional Absent or very rare Habitually Fitch-Snyder and Ehrlich (2003)
Torpor Absent Present Present Streicher and Reinhardt (2020)
Venomous Absent Present, 68 volatile and semi-volatile components Present, 200 volatile and semi-volatile components Hagey et al. (2007)
Seasonal body mass change Absent Absent Present Streicher (2004)
Seasonal coat colour change Absent Dorsal stripe shortens in some species Full coat and dorsal stripe change Streicher (2004); Nekaris, unpubl. data.
Species Two Nine One, possibly two Rowe and Meyers (2016)
Body size, range 120–330 g 265–2200 g 360–580 g Nekaris (2013)
Ears Haired, larger than in Nycticebus or Xanthonycticebus Haired and small often with tufts Ear length intermediate and naked at tips Osman Hill (1953)
Multi-male, multi-female social system Present Absent Present Poindexter and Nekaris (2020)
Gestation 160–170 d 184–197 d 184–200 d Fitch-Snyder (2020)
Molar size M2 larger than M1 M1 larger than M2 M2 larger than M1 Osman Hill (1953)
Karyotype and nucleolus organiser regions (NORs) 2n = 62 2n = 50; NORs on chromosome 1, 6, 9, 15 and 23 2n = 50; NORs on chromosome 6, 9 and 15 Chen et al. (1993); Goonan et al. (1995)
Third hand pad Smallest Intermediate or small Largest Osman Hill (1953); Nekaris, unpubl data.
Snout Narrow and pointy Broader and more rounded Broader than Loris, but longer premaxilla than Nycticebus Osman Hill (1953)
Interorbit Narrowest Widest Intermediate Ravosa (1998)
Ocular axial and corneal diameter AD – 14.0 mm; CD – 12.0 mm AD – 15.7 mm; CD – 12.1 mm AD – 15.5 mm; CD – 12.3 mm Ross and Kirk (2007)

Contents

a single species, Xanthonycticebus pygmaeus (Bonhote, 1907) is currently recognised and Nycticebus intermedius Dao Van Tien, 1960 and the not formally described N. chinensis are treated as synonyms. There is clear clinal latitudinal variation in body size and craniofacial size (smaller in the north) (Ravosa 1998). Variation in pelage colourations, coupled with a considerable amount of genetic divergence between available sequences deposited in GenBank (e.g. up to 2.0% in cytb; Fig. 1), largely from specimens without exact geographic locality data, may lead to the recognition of additional species in the future. Pozzi et al. (2020), based on monophyletic northern and southern populations of pygmy lorises from Laos PDR, Cambodia and Vietnam, advocate more research to confirm if these are, indeed, two species.

Mein and Ginsburg (1997) tentatively described a single third upper molar M3 (T Li 41) from Li Mae Long in Lamphum Province, Thailand dated to the early Miocene, 17–18 Mya, as ?Nycticebus linglom Mein & Ginsburg, 1997. The small size (1.29 × 1.82 mm) shows affinities with X. pygmaeus, but absence of a hypocone and a metaconule on M3 on T Li 41 aligns it closer to N. bengalensis than to X. pygmaeus and Li Mae Long is situated west of the Mekong River, outside the current distribution range of X. pygmaeus. We suggest to retain ?Nycticebus linglom within the genus Nycticebus.

The holotype of X. pygmaeus is a juvenile male collected by J. Vassal on 13 November 1905 in Nha Thrang Vietnam [12.24, 109.19], that is currently stored in the Natural History Museum London under registration number 1906.11.6.2. It is described in detail by Bonhote (1907).

Divergence and molecular clock dates

Several molecular phylogenetic studies have been conducted that included samples of X. pygmaeus and two or more other Nycticebus species; in all analyses, X. pygmaeus is the first group to split, thus forming two distinct reciprocal monophyletic groups. Our own analysis, based on the complete mitochondrial genome sequences of Xanthonycticebus (X. pygmaeus GenBank Accession #: KX397281), two species of Loris (L. lydekkerianus KC757402 from India and L. tardigradus AB371094 from Sri Lanka), three Nycticebus (N. bengalensis KY436589 from China, N. c. insularis MG515246 from Malaysia and N. coucang AJ309867 from an unknown location) with P. edwardsi KC757407 from Cameroon as an outgroup, likewise shows a genetic distance of 9.9–10.0% between X. pygmaeus and the three other Nycticebus species (Fig. 1).

The divergence time between X. pygmaeus and the other Nycticebus species was estimated at between 6.4 Mya and 26.4 Mya (Table 2). Pozzi et al. (2015) commented that the gap of around six million years between the divergence of X. pygmaeus and the radiation of the other Nycticebus species may lend support to the distinction of X. pygmaeus at the generic level. Using data from Perelman et al. (2011), it is evident that the split between Nycticebus and Xanthonycticebus, by them estimated at 10.2 Mya (95% CI range 5.4–15.1 Mya), considerably predates several widely acknowledged generic splits within the Order primates, including those between geladas Theropithecus gelada and baboons Papio spp. / mangabays Lophocebus (4.1 Mya; 3.4–4.7 Mya), between Semnopithecus and Trachypithecus langurs (4.1 Mya; 2.9–5.4 Mya), between Mico and Cebuella marmosets (4.8 Mya; 2.9–7.2 Mya) and, indeed, between humans Homo and chimpanzees / bonobos Pan spp. (6.6 Mya; 3.4–7.7 Mya). Estimates of the split between the two genera, based on other Nuclear genes, nuclear, mitochondrial or both, are generally between 10 and 20 Mya, with some estimates exceeding 25 Mya (Table 2). Thus, in all likelihood, the Nycticebus and Xanthonycticebus split occurred by the Late to Middle Miocene and possibly as early as the Oligocene.

Table 2.

Estimates of the timing of the split between Nycticebus and Xanthonycticebus (in Million years ago, range is expressed as the 95% highest posterior density of divergence time estimates).

Type (bp) Nycticebus species included in calculation Split (mean, range), Mya Reference
Mitochondrial genes
Cytochrome b (1140) javanicus / bengalensis / coucang / menagensis 10.9 (7.6–14.5) Pozzi et al. (2015)
Cytochrome b + cytochrome oxidase subunit 1 (536) coucang 26.4 (13.1–39.7) Munds et al. (2018)
Nuclear genes
18 gene regions (9,500) coucang 6.4 (3.5–10.1) Horvath et al. (2008)
54 gene regions (34,927) bengalensis / coucang 10.2 (5.4–15.1) Perelman et al. (2011)
Melanocortin 1 receptor (729) bengalensis / coucang 12.0 Munds et al. (2021)
Recombinant activation gene 2 intron (716) coucang 14.5 (6.0–24.9) Munds et al. (2018)
Mitochondrial and nuclear genes
4 genes (cytb, co1, rag2, MC1R) (1983) coucang 18.4 (10.2–26.9) Munds et al. (2018)

Even the lower estimates of the divergence between Nycticebus and Xanthonycticebus, of around 8 Mya predate many acknowledged generic splits in a wide range of mammalian taxa. This includes, for instance, those within the Muridae (e.g. Beamys-Cricetomys, Parotomys-Arvicanthis, Microtus-Clethrionomys, Phyllotis-Calomys and Rhipidomys-Phyllotis/Calomys) (Steppan et al. 2004) and the Cetartiodactyla (e.g. Capra-Pseudois, Ovis-Nilgiritragus, Oryx-Addax, Bos-Bison, Cervus-Rusa and Mazama-Odocoileus) (Zurano et al. 2019). The same is true for other vertebrates, such as birds (e.g. babblers, white-eyes and bee hummingbirds: Cai et al. 2019; Licona-Vera and Ornelas 2017).

The marked difference between Nycticebus and Xanthonycticebus is also supported by hybridisation events. In captivity, hybrids (confirmed and suspected) have been recorded between N. bengalensis and N. coucang and N. coucang and N. hilleri (other Nycticebus species are rarely kept in zoological facilities). Despite being the most common of the slow lorises in captive settings – the Zoological Information Management System lists globally 191 Xanthonycticebus and 220 of four other slow loris species combined – there are no records of hybrids between Xanthonycticebus and any of the other species. Both Nycticebus and Xanthonycticebus have n = 50 chromosomes, but karyotypically, the former differs from the latter by having a secondary construction in the short arm of chromosome 1 and the additional presence of nucleolus organiser regions on chromosome pair 1 and 23 (Stanyon et al. 1987; Chen et al. 1993).

Status

Xanthonycticebus pygmaeus occurs naturally in Vietnam (historically south to the vicinity of Ho Chi Minh City [10.75, 106.66]), Laos PDR (west to Phôngsali [21.59, 102.25]), Cambodia (east of the Mekong River), China (historically north to Lüchun County [23.00, 104.67]) (Nekaris 2013). The species may have established itself in Thailand, west of the Mekong River, as a result of poorly planned release efforts (Osterberg and Nekaris 2015). Xanthonycticebus pygmaeus has been assessed as Endangered according to IUCN Red List Criteria, with the trade for medicinal purposes and as pets and habitat loss recognised as the main threats (Starr et al. 2011; Blair et al. 2020). The species is protected in all four of its range countries, but active enforcement of these laws is far from optimal (Nekaris and Starr 2015; Thạch et al. 2018; Ni et al. 2020). The species is the most common loris kept in accredited zoological collections (i.e. 43 in N America, 86 in Europe, 62 in Asia; Species360 2021). In addition, rescue centres in Vietnam, Laos, Thailand, China, United Arab Emirates and Japan have at least 79 individuals under their care (e.g. Kenyon et al. 2014; Khudamrongsawat et al. 2018; Yamanashi et al. 2021). The species is part of both American Zoo Association and European Association of Zoos and Aquariums breeding programmes, but birth rates are low.

The genus Nycticebus is listed in appendix I of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), precluding all commercial international trade (Nekaris and Nijman 2007). In the proposal, submitted by Cambodia in 2007, which was accepted by consensus, three species names were singled out, including Nycticebus pygmaeus (with N. intermedius and N. chinensis listed as synonyms). As such, with respect to international trade, there is no doubt that Xanthonycticebus gen. nov. continues to receive the same level of protection and regulation as other slow lorises.

Acknowledgements

We thank the following museums and staff for access to specimens under their care: Colombo Natural History Museum, Field Museum of Natural History-Chicago, Naturalis Leiden, Zoological Museum Amsterdam (now merged with Naturalis), Natural History Museum London and Natural History Museum Oxford. Funding was received from the Systematics Research Fund of the Linnean Society, The Royal Society and SYNTHESIS Project, financed by the European Community Research Infrastructure Action under the FP6 Structuring the European Research Area programme (NL-TAF 3491). Our long-term field projects on slow and slender lorises in Sri Lanka, Cambodia and Indonesia has been supported by People’s Trust for Endangered Species, Cleveland Zoological Society and Cleveland Metroparks Zoo and Disney Worldwide Conservation Fund. We thank Aconk Ahmad, Penelope Goodman, Zak Showell, Carly Starr and Ariana Weldon for support and three reviewers and the editor for constructive comments and suggestions for improvement.

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