Nasalis É. Geoffroy Saint-Hilaire, 1812

Harding Abstract, Lee E., 2015, Nasalis larvatus (Primates: Colobini), Mammalian Species 47 (926), pp. 84-99 : 84-92

Nasalis É. Geoffroy Saint-Hilaire, 1812

Simia Linnaeus, 1758:25 . Simia suppressed by Opinion 114 (International Commission on Zoological Nomenclature 1929).

Cercopithecus Linnaeus, 1758:26 . Type species Simia diana Linnaeus 1758:26 by subsequent designation (Stiles and Orleman 1926); Cercopithecus validated by Opinion 238 (International Commission on Zoological Nomenclature 1954).

Nasalis É. Geoffroy Saint-Hilaire, 1812:90 . Type species Cercopithecus larvatus von Wurmb (1781) by monotypy.

Hanno Gray, 1821:297. Replacement name.

Rhinolazon Gloger, 1841 :XXVII, 36. Replacement name.

Rhynchopithecus Dahlbom, 1856:91 . Type species Rhynchopithecus larvatus Dahlbom 1856:93 by monotypy; replacement name.

CONTEXTANDCONTENT. OrderPrimates,suborderHaplorrhini, infraorder Simiformes , superfamily Cercopithecoidea , family Cercopithecidae , subfamily Colobinae , tribe Rhinopithecini . Nasalis is monotypic.

Nasalis larvatus ( von Wurmb, 1781) Proboscis Monkey

Simia nasica Schreber, 1775:46 , plates 10B and 10C. Type locality not specified. Nomen oblitum (see “Nomenclatural Notes”).

Cercopithecus larvatus von Wurmb, 1781:145 . Type locality Indonesia, West Kalimantan, “Pontiana, West Borneo” ( Pontianak ).

S[imia]. Cercopithecus capistratus, Kerr 1792 :No. 56. Type locality not specified.

Simia nasalis: Shaw, 1800:55 . Name combination.

Cercopithecus nasica: Latreille, 1801:283 . Name combination.

Nasalis larvatus: É. Geoffroy Saint-Hilaire, 1812:91 . First use of current name combination. Nomen protectum (see “Nomenclatural Notes”).

Cercopithecus nasicus: Desmarest, 1817:574 . Name combination.

Cercopithecus (Nasalis) nasicus: Desmarest, 1820:55 . Name combination.

Semnopithecus nasicus: Desmoulins, 1825:570 . Name combination.

Nasalis recurvus Vigors and Horsfield, 1828:109 . Type locality “Borneo.” Based on a juvenile specimen of N. larvatus .

Semnopithecus larvata: Fischer, 1829:16 . Name combination.

Semnopithecus larvatus: Martin, 1841:453 . Name combination.

Rhynchopithecus nasalis: Dahlbom, 1856:93 , table II. Name combination.

Semnopithecus (Nasalis) larvatus: Anderson, 1878:42 . Name combination.

Nasalis larvatus orientalis Chasen, 1940:84 . Type locality Indonesia: East Kalimantan, “Bulungan, North-East Borneo.”

CONTEXT AND CONTENT. As for genus. Nasalis larvatus has contained 2 named subspecies, Nasalis larvatus larvatus von Wurmb, 1781 , stripe-naped proboscis monkey of Borneo except probably northeast Kalimantan and N. l. orientalis Chasen, 1940, plain-naped proboscis monkey of northeast Kalimantan ( Brandon-Jones et al. 2004). Neither is currently recognized ( Groves 2005).

NOMENCLATURAL NOTES. Several authors (e.g., Geoffroy Saint- Hilaire 1812; Lesson 1834; Martin 1837; Gervais 1854) refer to Louis Jean-Marie Daubenton’s description of “ le nasique,” read to the Institut National des Sciences et Arts sometime after 1766 and before 1781, as the basis for nasica , nasicus , and, ultimately, Nasalis . This paper was apparently never published, however (see Harding 2012 for a discussion of it) and the non-Linnaean name would not be available for nomenclatural purposes in any case. Von Wurmb (1781:145) misspelled Cercopithecus (“ Cercopheticus ”).

Geoffroy Saint-Hilaire (1812) and others ascribed the 1st description of “ Simia nasica ” to von Schreber (1775:46, plates 10B and 10C). Bowdich (1821:18), for example, remarked, “There is a large Guenon ( Simia Nasica, Schreber ) which is remarkable for an excessively long nose, in the form of a notched spatula. It is found in Borneo, ...Wurmb first transported this animal, of which Buffon was ignorant,…”

However, nasica may rank as a nomen oblitum under Article 23.9, Reversal of Precedence because (Article 23.9.1.1) it has not been used as a valid name since before 1899; and (Article 23.9.1.2) larvatus has been used as the presumed valid name in> 25 works, published by> 10 authors, in the past 50 years. This qualifies larvatus as a nomen protectum. Geoffroy Saint-Hilaire’s (1812) use of “ nasica ” as the root of Nasalis recognizes both von Schreber’s and Daubenton’s contributions.

Simia nasalis has been wrongly attributed to Linnaeus (1758), who did not mention this species. Likewise, Gmelin (1788), editor of the 13th edition of Linneaus’ Systema Naturae, is sometimes cited as the authority for S. nasali s, but this species is not mentioned in that edition. Similarly, S. nasica has been attributed to Lacépède (1799) and Audebert (1800), whose publications succeeded von Schreber’s (1775).

Kerr (1792:No. 55), a translation of Gmelin’s 13th edition of Linnaeus’ Systema Naturae, but enhanced with many additional species, described Simia (Cercopithecus) nasuus . However, “ nasuus ” appears to have been either a mistranslation or misprint from von Schreber (1775), as Elliot (1913) and others evidently assume when writing it as Simia (Cercopithecus) nasicus Kerr. Allen (1895) noted that Kerr (1792:No. 56) also listed a Cercopithecus capistratus as a synonym for S. (C.) nasutus [= larvatus ].

Vigors and Horsfield (1828:109) named a specimen Nasalis recurvus as a 2nd species of Nasalis , but Gray (1850:2) reported that “Capt. Sir Edward Belcher brought home a young specimen of this species [ Nasalis larvatus ], showing that N. recurvus is only the young of the common species.” Geoffroy Saint-Hilaire (1829) included Nasalis in Semnopithecus . Pryer (1881:398) is sometimes given as an authority for “ S [emnopithecus] nasalis ,” which he discusses with considerable uncertainty as to “... whether [he has] found a new species of Monkey or not...” and gives no detailed description.

Although Groves (1970) and others have included the simakobou, Simias concolor Miller, 1903 (endemic to the Mentawai Islands) in Nasalis, Groves (2001) and others restored Simias to generic rank. However, Whittaker et al. (2006), based on cytochrome b and adjacent RNA genes, conclude that the genetic differences between Nasalis and Simias are slight enough to warrant congeneric status, although they do not recommend this change for conservation reasons.

Its name is bekantan in Indonesian and rasong in Malay; in Malay, an obsolete name, orang belinda, referred to the similarity of its large nose to those of Dutch people—possibly to the amusement of von Wurmb.

DIAGNOSIS

Nasalis larvatus , the largest colobine, is also the most sexually dimorphic. Mean mass of females is 10.0 kg, n = 14 and for males is 21.2, n = 13 ( Oates et al. 1994). Both genders have uniquely large noses ( Fig. 1 ); the mature males, which is pendulous and hangs below the mouth, can reach 17.5 cm in length (Buffon and Sonnini 1799). It is the only Southeast Asian colobine with reddish-brown dorsal fur, a darker crown, creamy pale belly, and gray legs, hands, and tail ( Fig. 1 ). N. larvatus is the only cercopithecid in which the length of the femur plus tibia is longer than the skeletal trunk length ( Ankel-Simons 2000).

GENERAL CHARACTERS

Nasalis larvatus shares many cranial, dental, and postcranial features such as body size and limb proportions with snub-nosed monkeys ( Rhinopithecus ), duoc-langurs ( Pygathrix ), simakobou or pig-tailed langur ( Simias concolor ), and the fossil Eurasian colobine Mesopithecus , suggesting a common inheritance ( Peng et al. 1993; Peng and Pan 1994; Jablonski 1998). Pan et al. (2004) suggested placing these 5 genera into a tribe, the Rhinopithecini . Alternatively, they are referred to as the “odd-nosed” clade, the Rhinopithecus clade, or the Rhinopithecus complex ( Jablonski 1998; Sterner et al. 2006; Whittaker et al. 2006; Roos et al. 2011). These common features contrast with the analogous features of the surilis ( Presbytis ), lutungs ( Trachypithecus ), and south-Asian langurs (henceforth, langurs), Semnopithecus , collectively called the Presbytini ( Groves 2001) .

The skull dimensions (mm) of Elliot’s (1913) example, an adult male, were: total length 135, occipitonasal length 111, intertemporal width 45, zygomatic width 95, median length of nasals 24, palatal length 45, length of upper molar series 33, length of mandible 94, and length of lower molar series 45.5. Fitch (2000) found a maximum occipitonasal length of 143 mm in a sample of 33 adults and juvenile skulls. Relative brain size (cube root of brain volume divided by basicranial length) is 0.76 ( Spoor 1997). Mean cranial capacity is 102 cm 3 (n = 10) in adult males and 85 cm 3 (n = 15) in adult females ( Schultz 1942).

Head and body length is 660–762 mm for males and 533– 609 mm for females; tail length is 559–762 mm for both genders ( Nowak 1999). The mean relative length of the tail (as a percentage of trunk length) is 156.6% (range 143–167%, n = 10) for males and 152.3% (range 139–169%, n = 15) for females ( Schultz 1942). Bismark (2010) gives mean mass (kg) of subadults as 6.7, young 3.5, and infants 1.5. N. larvatus has a relatively stout chest, shorter tail, and longer upper limbs than langurs and the long-tailed macaque, Macaca fascicularis ( Schultz 1942) . The dark cap, which is flat with prominent whorls, together with swept-back cheeks, “frame[s] the flesh to terra-cotta face” (Chaplin and Jablonski 1998:89). The skin on the smallish ischial callosities and on the bottom of the hands and feet is black. The facial skin of infants is bluish and their skin and fur do not contrast with those of adults, as in the Presbytini ( Jablonski 1998) .

Not surprisingly, the skull of N. larvatus ( Fig. 2 ) has specialized features to support the huge nose, such as the external nasal cartilages ( Maier 2000). Nasalis is the only colobine genus with a narrow, cercopithecine-like interorbital pillar ( Delson 1994). Craniometrically, N. larvatus clusters separately from the other Asian colobines except for simakobou, mainly due to its long, narrow nasal structure, a long muzzle, and a back-tilted ascending ramus; and its sexual dimorphism pattern is different from the other odd-nosed colobines and more broadly similar to langurs (Groves and Thorington 1970; Pan and Groves 2004). Compared to snub-nosed monkeys, N. larvatus has narrower nasal bones, narrower premaxillae, reduced breadth of the bony elements of the hard palate, a longer aspect ratio of the molars, and greater depth of the mandible and the midface between the inferior margin of the orbit and the maxillary alveoli ( Jablonski 1998). Schultz (1942) gives the following metrics for adults: mean intermembral index 121.2 (range 119–125, n = 10) for males, 121.0 (range 119–124, n = 15) for females; crural index 88.1 (range 84–91, n = 10) for males, 87.7 (range 86–90, n = 15) for females; and brachial index 100.3 (range 98–102, n = 10) for males, 99.5 (range 94–102, n = 15) for females.

DISTRIBUTION

Nasalis larvatus is endemic to Borneo and small islands near the coast of Borneo and is distributed throughout in suitable habitat, that is, along lowland rivers, near-shore islands, and coastal mangrove swamps, except where populations have become extirpated ( Fig. 3 ).

FOSSIL RECORD

No fossils of Nasalis are known. Harrison (1996, 2000) and Harrison et al. (2006) note the absence of Nasalis material in both the paleontological and archaeological records of Sundaland. T. Harrison (in litt.) suggests that their absence, “... may be a question of sampling... [also] their preference for mangrove swamp and riverine environments may be a factor in their absence from Niah [Cave],” a mountain-side site with fossils of many other primate species including humans, Homo sapiens . Harrison et al. (2006) suggest that N. larvatus was probably already present on Borneo as an endemic taxon in the Late Pliocene and that the last common ancestor of it and simakobou had arrived in the Sunda islands by the early Pliocene. A recent find of Mesopithecus in Yunnan suggests this area as the center of evolution and radiation of the odd-nosed clade ( Jablonski et al. 2011).

FORM AND FUNCTION

Form. —The dental formula of Nasalis larvatus is i 2/2, c 1/1, p 2/2, m 3/3, total 32 ( Elliot 1913). The vertebral formula is 7 C, 12 T, 7 L, 3 S, 25 Ca, total 54 and shows a “remarkable scarcity of numerical variations among the presacral vertebrae [compared to] anthropoid apes” ( Schultz 1942:299).

Nasalis larvatus , a foregut fermenter, has the smallest stomach and largest small intestine of the colobines, implying a low need for fermenting capacity (compared to the more folivorous langurs) and higher absorbing capacity ( Chivers 1994). Like snub-nosed monkeys and duoc-langurs, N. larvatus has a distinct presaccus at the forestomach, giving the stomach 4 parts, in contrast to the tripartite stomach of the Presbytini ( Caton 1998) . The colon weight and surface area are high relative to other colobines ( Chivers 1994).

The placenta is bidiscoid with anterior and posterior lobes and the umbilical cord of one was 15 cm; the mother’s adrenal glands were larger than the kidneys, with an adrenal:kidney mass ratio of about 1.18 (Soma and Benirchke 1977).

Youlatos et al. (2012) found that the humeral elements of Nasalis and the other odd-nosed monkeys clustered separately in discriminant function analysis from the 3 species of Mesopithecus , which clustered together with the Presbytini . The humeri of duoc-langurs, simakobou, and Nasalis were “morphologically associated with a large globular head, enlarged subscapularis facet, long shaft, extended biepicondylar width, medial condyle directed more medially, and wide and low trochlea and capitulum” ( Youlatos et al. 2012:226–227). They interpreted this as reflecting more derived arboreal locomotion in the odd-nosed clade following divergence from Mesopithecus and the Presbytini .

The baculum is about 8 mm long (mean 7.9 mm, n = 3— Dixson 1987). The penis is long and red and the scrotum black, contrasting colors that may function as visual signals in sexual or dominance displays (Chaplin and Jablonski 1998). The mean (n = 5) mass of both testes in breeding condition is 14.7 g, or 0.07% of body mass ( Schultz 1938, not seen cited by Kenagy and Trombulak 1986).

Function. — Nasalis larvatus has large hands and feet ( Figs. 1 and 4 ) and swims well, a useful capability for its riverine and tidal habitats. Elliot (1913) recounts an observation of 1 individual swimming submerged for 28 min to avoid a hunter in a boat; and Bennett and Sebastian (1988) confirm that N. larvatus can swim underwater for up to 20 m to avoid avian predators. The enlarged nose is used for sexual display and to amplify vocalizations (Bennett and Gombek 1993).

In the odd-nosed colobines (including Mesopithecus ), several aspects of the scapula, such as the overall proportions and the inclination of the glenoid fossa, resemble those of hylobatids and suggest a high frequency of overhead suspensory locomotion (N. G. Jablonski, in litt.). Youlatos et al. (2012:227) classified duoc-langurs, simakobou, and Nasalis as “Arboreal Walking/Suspensory,” as opposed to snub-nosed monkeys, “Arboreal Walking/Terrestrial.” Its shoulder morphology “seems to accommodate extended arm movements at the shoulder level, favor a partially extended elbow and promote frequent forearm prono-supination” relative to the other colobini studied; these movements “occur frequently in forelimb dominated positional activities, such as arm swing, brachiation or vertical climb that are common in these monkeys” ( Youlatos et al. 2012:227).

Suspensory feeding in N. larvatus is common ( Fig. 5 ). Napier (1963:187) describes its leap ( Fig. 4 ): “...its hind limbs ... at the moment of take-off are extended at both knee and hip joints. In flight, the forelimbs are extended at the shoulder and reach out towards the landing site to arrest the progress of the leap. At the initial states of the horizontal leap, therefore, both sets of limbs are extended. Subsequently the hind limbs flex to assist the hands at the end of the leap.”

Nasalis larvatus walks upright, with the arms raised, when on land and wading (Bennett and Sebastian 1988). Contrary to some often-repeated reports, the hands and feet are not “webbed” per se, but the feet have a slight webbing at the base of the phalanges between toes 2 to 5 that may extend as far as the middle of phalanx 2 ( Schultz 1942). The metacarpus and metatarsus are long, both absolutely and relative to the digits ( Figs. 1 and 4 ), and these features no doubt give support when walking on soft mangrove swamp mud, and in swimming.

Nasalis larvatus individuals sometimes regurgitate and remasticate food, which allows for a higher food intake efficiency compared to days in which the same individuals do not regurgitate and remasticate ( Matsuda et al. 2011a). This and its high chewing efficiency—mean fecal particle size is small for its average mass and significantly smaller than for 2 sympatric colobines, silvered lutung ( Trachypithecus cristatus ) and red surily ( Presbytis rubicunda — Matsuda et al. 2014b)—may be evidence for regular use of rumination.

The robust mandibular corpora and symphyses, combined with other aspects of cranial morphology described above, reflect the highly folivorous diet of N. larvatus ( Ravosa 1996) . Linear enamel hypoplasia, a sensitive dental indicator of physiological stress, occurs at a low frequency in N. larvatus (e.g., 2 of 18, 11%— Guatelli-Steinberg 2000).

ONTOGENY AND REPRODUCTION

Ontogeny. — Hayssen et al. (1993) give the following ontogenic data for Nasalis larvatus : neonatal mass 454 g, mean number of embryos 1.5 (range 1–2), litter size 1 (occasionally 2), solid food at 6 weeks, and weaned at 7 months, although Zimmermann and Radespiel (2007) give the age at weaning as 246 days (8.2 months). Infants are born with thin, blackish hair and dark blue faces with the short, upturned noses typical of the odd-nosed clade. Murai et al. (2007) classified individuals with at least some dark skin on the face as infants and those that are noticeably smaller than adults, ≤ 1.5 years old, as juveniles.

Female N. larvatus normally become sexually mature at age 4 (Zimmermann and Radespiel 2007) to 6 years ( Afrilia 2011), after adult dentition is complete ( Schultz 1942). Age at 1st breeding is usually 3–5 years for females and 5–7 years for males ( Murai 2004). Maximum life span in captivity is 25.1 years (Zimmermann and Radespiel 2007). Maximum age of reproduction is assumed to be equivalent to life span since cessation of estrus is not known (cf. Murai 2004)

The tooth eruption pattern of N. larvatus differs markedly from that of other colobines and resembles a cercopithecine pattern in that there is no early eruption of the 2nd molar relative to the incisors in either the upper or lower jaw ( Hart 2007):

M1I1I2M2PP C M3 M1I1I2M2 [PP C] M3

Schultz (1942) gives detailed measurements of body and limb proportions (including hands and feet) and cranial capacity as N. larvatus grows from fetuses through infants and juveniles to adult males and females. Polydactyly has been reported (1 of 31 births, 3.2%— Schultz 1972).

Reproduction. —Reproduction is not seasonal ( Hayssen et al. 1993; Boonratana 2011). Based on progesterone and estradiol concentrations in feces, the estrus cycle lasts 22–23 days ( Astuti et al. 2011). Sexual swelling is evident in 77.4% of copulating females, with copulating subadult females showing the most distinct swelling ( Murai 2006). Gestation is 166 days ( Asdell 1964) and lactation lasts 1.5 years ( Afrilia 2011). Stark et al. (2012) used an interbirth interval of 2 years for population modeling purposes and calculated a sex ratio at birth of 41.7% males from data given by Boonratana (1993, 2000). From available data for 3 groups in different habitats, the proportions of females breeding were calculated as 45.8% to 64.1% per group and “male monopolization” (= proportion of males that breed) as 74% to 100% ( Stark 2012). The ratio of young infants to adult females can range from 0 to 0.65 ( Boonratana 2011).

ECOLOGY

Population characteristics. — Sha et al. (2008) estimated a minimum of <6,000 Nasalis larvatus individuals in 5 highly fragmented populations in Sabah and smaller groups elsewhere. Almost all were in coastal marshes and estuaries, although some were far inland on major rivers. Population estimates are <300 in 1 population in Brunei ( Bennett 1986) and about 1,000 in Sarawak (Yeager and Blondal 1992). The population in Central, West, and East Kalimantan was estimated at 9,200 in 2005 ( Manansang et al. 2005). The total population may therefore be as high as about 16,000, although current, quantitative estimates are not available.

Space use. — Nasalis larvatus occurs mainly along rivers, coastal deltas, and islands, rarely more than 200 km inland from the coast, usually at elevations <200 m (Meijaard and Nijman 2000a) to a maximum of about 350 m ( Medway 1977). Its habitat is mainly riparian or riverine dipterocarp forest and coastal or inland mangrove forest. Dipterocarp forest has taller trees than mangrove forests and provides better predator-avoidance cover, especially the taller trees used for sleeping ( Matsuda et al. 2009b; Bismark 2010). It is often at highest densities at ecotones and being able to exploit 2 or more forest types may give it a greater variety of food and cover throughout the year (Bennett and Sebastian 1988).

Typical habitat of N. larvatus in Sarawak is mangrove-nipa forest along the saline-brackish portions of rivers, with Avicennia and Sonneratia close to the river mouth giving way upstream to Rhizophora and, further upriver, to Brugiera and Nypa fruticans ; further up, where the water is fresh, the riparian forest is often taller than the surrounding lowland dipterocarp forest (Bennett and Sebastian 1988). Vegetation types that dominate its habitat at Nipah Panjang, West Kalimantan, include Rhizophora apiculata , R. mucronata , Bruguiera gymnorrhiza , and B. parviflora ( Kartono et al. 2008) . In western Sabah ( Bernard 2009), N. larvatus habitat is dominated (top 6 species by frequency in decreasing order) by: Excoecaria indica (Euphorbiaceae) , Cerbera odollam (Apocynaceae) , Ficus binnendykii (Moracreae) , B. gymnorrhiza (Rhizophoraceae) , Psydrax (Rubiaceae) , and Symplocos celastrifolia (Symplocacecae) . In eastern Sabah, along the Kinabatangan River, the predominant tree species in N. larvatus habitats are Mallotus muticus , E. indica , Dillenia excelsa , Croton oblongus , Nauclea subdita , Xylosma sumatrana , Pternandra galeata , Vitex pinnata , Vatica rassak , and Antidesma thwaitesianum ; predominant vines are Lophopyxis maingayi , Croton caudatus , Dalbergia parvifolia , Hydnocarpus sumatrana , Entada rheedei , Bridelia stipularis , Albizia corniculata , Artabotrys suaveolens , Bauhinia diptera , and Millettia nieuwenhuisii (Matsuda 2008) . N. larvatus can adapt to human presence and will use rubber plantations adjacent to riverine and lowland forest that provides food and cover but avoids areas of intense human activity ( Soendjoto 2005).

Nasalis larvatus is nonterritorial ( Yeager 1989; Boonratana 2000; Matsuda et al. 2009b), home range sizes vary from a mean of 130 ha (range 25–138 ha— Yeager 1989), to 221 ha in riverine forest and 315 ha in coastal mangrove forest, with up to 100% overlap among groups ( Boonratana 2000), to 900 ha in mixed mangrove and lowland forests (Bennett and Sebastian 1988). In good habitat with little disturbance, however, home ranges can be much smaller. For example, at Kutai National Park, East Kalimantan, home ranges of 3 groups was 18, 19, and 21 ha with 20–62% overlap (Bismark and Iskander 2002). Food availability is the main determinant of home range size in N. larvatus (reviewed by Matsuda et al. 2009b).

Daily activity is allocated 1st to resting, 2nd to feeding, and 3rd to traveling; for example, Matsuda et al. (2009a) found a daily budget of 76.5% resting, 19.5% feeding, and 3.5% moving. In both genders, feeding activity peaks in the late afternoon at 1500–1700 h, shortly before sleeping, with differences among the seasons reflecting fruit availability ( Yasaningthias 2010; Matsuda et al. 2014a).

After foraging during the day, N. larvatus groups habitually return to well-developed, riverside tree patches for sleeping. For example, groups sleep mainly in patches of tall Sonneratia alba (Lythraceae) and Bruguiera (Rhizophoraceaa) in the bends in the Kinabatangan River, rather than along the smaller tributaries where they range during the day ( Boonratana 2000; Matsuda et al. 2009b). Areas near the sleeping sites and river crossing sites also tend to be foraging sites when fruit is abundant, but in times of low fruit abundances they forage farther away from sleeping sites ( Matsuda et al. 2009b). Along the Mananggul River in Sabah, N. larvatus spends significantly more time away from the river (> 50 m) than near the river (<50 m) in all months except during June–August, when the foraging time allocation is reversed; the higher use of riverine habitats is associated with greater availability of fruits and flowers and lower availability of young leaves in these months ( Matsuda et al. 2011b).

Daily movement ranges from about 500 m ( Bismark 2010) to an average of 910 m (range 370–1,810, n = 53 full-day follows— Boonratana 2000). In a study near Nipah Panjang Village, Kalimantan, linear distances between main activity sites averaged 158 m ± 75 SD and daily range of groups averaged 904 m / day ± 117 SD, or a maximum radius of 371 m ± 47 SD ( Kartono et al. 2008). Sleeping site positions are shifted daily (e.g., 192 m ± 65 SD on subsequent nights— Kartono et al. 2008).

Availability of fruit, but not of flowers or young leaves, is the main determinant of daily path length: N. larvatus groups travel farther to search for fruit when it is less abundant ( Matsuda et al. 2009b). A minor determinant is rain, during which they travel a little less ( Matsuda et al. 2009b).

In a riverine forest with a maximum canopy height of 30 m, N. larvatus climbed up to 21 m high, although most feeding, resting, and traveling were between 10 and 17 m high ( Boonratana 2000). These groups occasionally swam across the Kinabatangan River, which might be about 150 m wide at crossing places but much wider elsewhere, and almost daily across 20–25 m wide tributaries.

Choice of sleeping trees depends on tree size (diameter, height, and number of branches) and proximity to the river, and not on the tree species; sleeping trees are near other trees with overlapping branches, creating good arboreal connectivity for escape ( Bernard et al. 2012). However, at Sungai Tolak, West Kalimantan, N. larvatus preferred to sleep in large, emergent trees with few canopy connections located along rivers, consistent with the authors’ hypotheses that such sites would decrease molestation by mosquitoes and reduce potential entry routes for terrestrial predators (Feilen and Marshall 2014). The selection of sleeping sites in tall trees on the river bank in the angle of bends in the river and where the river is narrow is also thought to be a predator-avoidance strategy: when danger approaches from land, N. larvatus can leap into the river and swim across ( Yeager 1991a; Boonratana 1993; Bismark 1994; Matsuda et al. 2008a; Matsuda et al. 2011b). When the forest is flooded, however, the predation risk is less and they are more likely to select interiorforest sleeping sites ( Matsuda et al. 2010a).

Since home range size and daily movement distances are influenced by food (especially fruit) availability, it follows that biomass of N. larvatus is influenced by vegetation types. Biomass of N. larvatus ranges from 45 to 500 kg /km 2 (Bennett and Sebastian 1988; Yeager 1989; Boonratana 2000). Density ranges from about 8 to 60 individuals/km 2 (summarized by Bismark 2010). For example, Yeager and Blondal (1992) reported 9 individuals/km 2 in the most severely degraded habitat, 25/km 2 in habitat with severe destruction, 33/km 2 with moderate degradation, and 62/km 2 with low degradation. In the Garama River area of the Klias Peninsula, Sabah, population density was 1.85 groups/km 2 or 14.07 individuals/km 2; the population there, 10 groups with 76 individuals, was unchanged since a previous survey in 2005 and included some groups outside of the protected area ( Ridzwan Ali et al. 2009). In Brunei Bay, the population density in 1995 was 4.78 individuals/km 2 ( Yeager 1995).

Diet. — Nasalis larvatus is a folivore–frugivore specializing in seeds, fruits, and young leaves ( Yeager 1989; Matsuda et al. 2009 a, 2009b). Although it consumes a high diversity of plant species (e.g., 188 species— Matsuda et al. 2009a), it is an extremely selective feeder in terms of plant parts: mature leaves comprise only about 3% of the diet (Bennett and Sebastian 1988). The degree of folivory varies widely. For example, it has a mainly folivorous diet at Kutai National Park, East Kalimantan, of 81.1% leaves, 8.38% fruit, 7.68% flowers, 2.8% other including bark, insects, and crabs ( Bismark et al. 1994). Similarly, at Tanjung Puting National Park, Central Kalimantan, N. larvatus diet is comprised of 79% leaves, 18% fruit, and 3% flowers ( Purba 2009). On the Kinabatangan River, young leaves (65.9%) and fruits (25.9%) account for the majority of feeding time, with most (> 90%) fruit eaten being flesh and seeds of unripe fruits ( Matsuda et al. 2009a). The diet there includes 7.7% flowers, 0.03% mature leaves, and 0.5% other (Matsuda 2008). By contrast, in Samunsam, Sarawak, N. larvatus eats only 47% leaves, with 3% flowers, 35% fruit, and 15% seeds ( Bennett 1986).

On the Kinabatangan River, of the 48 dominant plant species, 16 had fruits and flowers that N. larvatus did not eat at all, in some cases because the seeds were too hard or the fruits too big, although orangutans ( Pongo pygmaeus ) and long-tailed macaques ate fruits of at least 5 of those species (Matsuda 2008). Predominant species of Croton were avoided completely despite their abundant fruits and flowers, which produced a strong smell (to observers), suggesting toxic or repellent chemicals (Matsuda 2008).

By comparing availability of various foods over an entire year, Matsuda (2008) showed that, although leaves were a constant dietary component, fruits varied seasonally, becoming more important in seasons of high availability of preferred fruits; hence, despite its being commonly described as primarily a folivore, this is an oversimplification. N. larvatus eats the calyx and flesh as well as seeds when the seeds are unripe, but often discards the calyx and flesh when the seeds are ripe, although this varies according to the phenology of ripening fruits (Matsuda 2008). N. larvatus also consumes bark of certain trees and nests of a species of arboreal termite, both of which vary seasonally for females but not males; termites evidently supplement mineral nutrients, absorb toxins, and assist digestion, rather than serving as a protein source (Matsuda 2008).

Nasalis larvatus adapts to a variety of diets, according to what is available and seasonal changes in plant nutrients and digestibility. In the Klias Peninsula, Sabah, N. larvatus eats at least 17 plant species, with preference for Ficus binnendijkii , B. gymnorrhiza , Hibiscus tiliaceus , and E. indica ( Bernard 2009) . At Labuk Bay, Sabah —a limited mangrove habitat surrounded by oil palm plantations—its food is mainly young leaves of R. apiculata (fruits, shoots, and mature as well as young leaves), Bruguiera parviflora , Acrostichum aureum (only the spores of this fern are eaten), S. alba , Ficus benjamina , Ipomoea pescaprae , Tetrastigma glabratum , and Sphenodesme stellata (Agoramoorthy and Hsu 2005a) .

In Tanjung Puting National Park, N. larvatus uses at least 55 plant species and prefers Eugenia , Ganua motleyana , and Lophpetalum javanicum; although these are the most frequent and most dominant tree species there, differences between availability and the species eaten indicated that N. larvatus selects particular plant species ( Yeager 1989). At the same national park, swamp forest habitats provide twice the diversity of food plants as lowland forest ( Purba 2009). Bismark and Iskander (2002) list 20 plant species that N. larvatus consumes (always the leaves, plus the flowers or fruits of 4 species), out of 55 available. At Pulau Kaget, South Kalimantan, until it was extirpated, N. larvatus ate leaves, fruits, or flowers of Limnocharis flava , Agapanthus africanus , Hymenachne amplicaulis , and Vittis trifolia ( Bismark 1997, not seen cited by Bismark 2010). In Samboja Kuala, East Kalimantan, N. larvatus eats Mangifera caesia , Garcinia mangostana , Durio zibethinus, Sondaricum koetjapi, Hevea brasiliensis , and Sonneratia caseolaris ( Alikodra et al. 1995 cited by Bismark 2010).

Leaves from species consumed are higher in protein, phosphorus, and potassium and lower in fiber, calcium, and manganese than those available but not consumed, similar to other colobine diets that are typically high in protein and low in protein inhibitors ( Yeager et al. 1997). Within the category of high protein-low fiber young leaves, abundance is also a factor in selection, suggesting that N. larvatus optimizes both leaf quality and intake per unit time ( Matsuda et al. 2013b). Although N. larvatus inhabits riverine forests with higher-quality leaves than other available forest types, including primary lowland forest, its habitat may still be protein-limited because of the requirements of its large body size; on the other hand, the high quality of foods available in these habitats may be a factor in the larger body size of N. larvatus relative to other colobines ( Matsuda et al. 2013b).

Agoramoorthy and Hsu (2005b) gave the ash, crude fibre, protein, and mineral content of these foods and noted the high sodium content in their study area—a small patch of mangrove forest adjacent to the ocean and surrounded by a sea of oil palm plantations—compared to other dietary studies, a consequence of limited vegetation heterogeneity.

Bismark (2010) calculated that an 8.84 kg N. larvatus would consume 900 g fresh weight (270 g dry weight) of food per day, equivalent to 1,066 kcal or 120.68 kcal/kg of body weight. The leaves, fruits, flowers, and seeds eaten by wild N. larvatus are lower in protein and higher in lignin, relative to 9 other colobine species, suggesting a poor quality diet ( Nijboer et al. 2006). However, some riparian plant species’ leaves and aerial roots have higher mineral content than the same plants grown in soil, suggesting a nutritional advantage of their habitat ( Bismark 2010). Certain foods are consumed in small amounts but contribute a disproportionate amount of nutrients because they are high in potassium, zinc, calcium, or copper; these include Alophyllus cobbe , the flowers of R. apiculata and Avicennia officinalis , and the bark of R. apiculata ( Bismark et al. 1994) . As a seed disperser N. larvatus helps forest regeneration: intact small seeds of Ficus and other tree and vine species are commonly found in fecal samples ( Matsuda et al. 2013a).

Interspecific interactions. —Ascaris and Trichiuris egg worms are common in Nasalis larvatus feces (Bismark 1994; Bismark 2010). Hasegawa et al. (2003) describe a new species of nematode, Enterobius (Colobenterobius) serratus , from N. larvatus .

Predators of N. larvatus include Neofelis diardi , clouded leopard ( Davis 1962; Matsuda et al. 2008b; Nowell and Jackson 2010), Tomistoma schlegeli , false gavial ( Galdikas 1985; Yeager 1991a), Ophiophagus hannah , king cobra, and Varanus salvator , monitor lizard ( Bismark 2010). Populations of monitors increase following forest clearing and this is thought to affect N. larvatus populations; N. larvatus is also hunted for bait to catch the lizards ( Bismark 2010).

After documenting predation on the banded surili ( Presbytis femoralis ) by the changeable hawk-eagle ( Nisaetus [formerly Spizaetus ] cirrhatus) and using data on the relative size of sympatric Nisaetus hawk-eagles and colobines, Fam and Nijman (2011) predicted that N. larvatus would be little threatened by Niseatus hawk-eagles, 3 species of which occur on Borneo. However, larger eagles occur on Borneo, such as the black eagle, Ictinaetus malayensis , which is known to take mammals ( Myers 2009). Crested serpent eagle ( Spilornis cheela ), a large raptor that I saw frequently in N. larvatus habitat on the Kinabatangan River in 2011, primarily preys on reptiles ( Myers 2009). As with other larger primates of Southeast Asia (cf. Hart 2007), N. larvatus seemingly has little to fear from avian predators.

Nasalis larvatus is commonly sympatric with silvered lutungs and long-tailed macaques and often encounters other primates such as surilis, Bornean orangutans ( P. pygmaeus ; henceforth, orangutans), and gibbons ( Hylobates ). Agoramoorthy and Hsu (2005a) described wild male and female orangutan nesting near and interacting with groups of N. larvatus , but without obvious conflict or competition for food. In 2011, I observed N. larvatus feeding in the same trees as Bornean gibbons, Hylobates muelleri , and silvered lutungs, but separated temporally by a few hours, along the Kinabatangan River; and I have seen N. larvatus groups aggregating for sleeping within sight of silvered lutungs nighttime aggregations along the Kinabatangan and Klias Rivers. In the Mananggul River, tributary to the Kinabatangan River, Matsuda et al. (2011b) observed long-tailed macaques about as frequently as N. larvatus in riverine habitats (<50 m from water), but infrequently at inland sites (> 50 m from water); and they observed pig-tailed macaques, M. nemestrina, Bornean gibbons, and silvered lutungs much less often overall, but still far more frequently in riverine habitats than inland sites. They observed orangutans about as frequently as N. larvatus overall, but more frequently at inland sites than riverine.

Figures

Fig. 1.—Nasalis larvatusfemale (above)and male (below).Photographs by Lee Harding.

Fig. 2.—Dorsal, ventral, and lateral views of skull and lateral view of mandible of an adult male Nasalis larvatus. Occipitonasal length is 133mm. Photographed by Phil Myers, Museum of Zoology, University of Michigan; used with permission of the photographer. First published by http://animaldiversity.org.

Fig. 3.—Nasalis larvatus is endemic to the island of Borneo in Brunei, the Malaysian states of Sarawak and Sabah and the Indonesian states of Daerah Tingkat I Kalimantan Barat, Kalimantan Tengah, Kalimantan Selatan, and Kalimantan Timur, collectively shown as Kalimantan. Some place names mentioned in the text are shown. Based on Meijaard and Nijman (2000a) and Sha et al. (2008).

Fig. 4.—Leaping style of Nasalis larvatus. Photograph by Lee Harding.

Fig. 5.—Nasalis larvatus juvenile showing single-arm suspensory feeding. Photograph by Lee Harding.