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Mammalian Species 47(926):84–99
Nasalis larvatus (Primates: Colobini)
Lee E. Harding
SciWrite Environmental Sciences Ltd., 2339 Sumpter Drive, Coquitlam, British Columbia, Canada V3J 6Y3; [email protected]
Abstract: Nasalis larvatus (von Wurmb, 1781), proboscis monkey, is the only member of its genus and is the largest colobine monkey. It has a uniquely large nose in males. It occurs in lowland riverine forests, peat swamps, and mangrove swamps of Borneo. It is
a strong swimmer and can swim underwater. A folivore, it lives in single male-multifemale troops or all-male groups, in a multilevel
social system. Male dispersal is routine and females commonly transfer among groups. It is listed as “Endangered” by the International
Union for Conservation of Nature and Natural Resources and is included in Appendix 1 of the Convention on International Trade in
Endangered Species of Wild Fauna and Flora.
Key words: bekantan, Borneo, colobine, odd-nosed, proboscis monkey, Pygathrix, Rhinopithecini, Rhinopithecus
© 2015 by American Society of Mammalogists
Synonymy completed 2 July 2012
DOI:10.1093/mspecies/sev009
Nomenclatural statement.—A life science identifier (LSID)
number was obtained for this publication: urn:lsid:zoobank.
org:pub:25D283FD-2FB1-450A-B483-7B2AE10345C4 www.mammalogy.org
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.
Context and Content. Order Primates, suborder Haplorrhini,
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).
Fig. 1.—Nasalis larvatus female (above) and male (below). Photographs
by Lee Harding.
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47(926)—Nasalis larvatus
mammalian species85
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 SaintHilaire 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 Naturæ,
is sometimes cited as the authority for S. nasalis, 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 Naturæ, 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).
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mammalian species47(926)—Nasalis larvatus
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 cm3 (n = 10) in adult
males and 85 cm3 (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,
Fig. 2.—Dorsal, ventral, and lateral views of skull and lateral view of
mandible of an adult male Nasalis larvatus. Occipitonasal length is
133 mm. Photographed by Phil Myers, Museum of Zoology, University
of Michigan; used with permission of the photographer. First published
by http://animaldiversity.org.
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)
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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).
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
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mammalian species47(926)—Nasalis larvatus
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
Fig. 4.—Leaping style of Nasalis larvatus. Photograph by Lee Harding.
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,
Fig. 5.—Nasalis larvatus juvenile showing single-arm suspensory feeding. Photograph by Lee Harding.
47(926)—Nasalis larvatus
mammalian species89
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):
M1 I1 I 2 M 2 PP C M3
M1 I1 I 2 M 2 [ 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
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mammalian species47(926)—Nasalis larvatus
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/km2 (Bennett
and Sebastian 1988; Yeager 1989; Boonratana 2000). Density
ranges from about 8 to 60 individuals/km2 (summarized by
Bismark 2010). For example, Yeager and Blondal (1992)
reported 9 individuals/km2 in the most severely degraded habitat,
25/km2 in habitat with severe destruction, 33/km2 with moderate
degradation, and 62/km2 with low degradation. In the Garama
River area of the Klias Peninsula, Sabah, population density was
1.85 groups/km2 or 14.07 individuals/km2; 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/km2 (Yeager 1995).
Diet.—Nasalis larvatus is a folivore–frugivore specializing in
seeds, fruits, and young leaves (Yeager 1989; Matsuda et al. 2009a,
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).
47(926)—Nasalis larvatus
mammalian species91
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.
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mammalian species47(926)—Nasalis larvatus
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.
HUSBANDRY
Nijboer et al. (2006) provide data on chemical composition
including minerals of native plant foods eaten by Nasalis larvatus and note that their natural foods are low in protein and contain much higher levels of indigestible fiber than most zoo diets.
In captive N. larvatus with a total average feed intake of 12% of
body mass, dry matter and plant cell wall material disappearance
exceeded 80%; passage marker studies revealed a transit time of
14 h, mean passage time of 49 h, and 5–80% retention after 52 h
(Dierenfeld et al. 1992). In that study, digestion coefficients and
retention times were greater than expected based on body size.
In captivity, the problem of surplus males arises because
avoidance and dispersal are not possible (Mulder 2012). A solution is to establish all-male groups in zoo environments which
Sha et al. (2012) showed, can be accomplished with development of affiliative behaviors, a dominance hierarchy, and little
contact aggression after the first few weeks.
BEHAVIOR
Grouping behavior.—Nasalis larvatus is typically found
in 1 male-multifemale groups, but with overlapping home
ranges, as well as all-male and predominantly male nonbreeding groups (Bennett and Sebastian 1988; Yeager 1991b, 1992,
1995; Boonratana 2002).
Male dispersal is routine (solitary males and all-male groups
are often seen) and females commonly transfer among groups
(Bennett and Sebastian 1988; Murai et al. 2007). Transferring
females are usually subadults (Murai et al. 2007). Over the course
of a year or more, group stability is low, with large fluctuations
in both male and female members (Rajanathan and Bennett
1990). Aside from dispersing individuals, however, groups are
relatively stable (Yeager 1990b). For example, in 16 months of
observation, Bennett and Sebastian (1988) never saw a harem
split into smaller parties, even when members were scattered
over > 100 m.
Some groups associate more than others and select sleeping
sites close together: a multilevel social organization of a band
comprising several groups (Yeager 1991b; Boonratana 2002;
Grüter et al. 2012). However, Matsuda et al. (2010b), using a
Bayesian analysis of N. larvatus density in relation to environmental factors, suggest that the previously reported multilevel
hierarchy might instead result from temporary aggregations of
groups around clumped food resources.
Group size varies by habitat quality, size, and degree of disturbance, ranging from 3 to 32 (Kawabe and Mano 1972; Yeager
1989; Kartono et al. 2008). In Tanjung Puting National Park,
Kalimantan, which has a mixture of mangrove, riverine, and
lowland dipterocarp forest, Yeager (1989) reports a mean group
size of 12.1 for all groups (n = 145 individuals). Group sizes
in Kutai National Park are 12.0–17.4 in riverine forest along
the Sangata River and 21.0 in a mangrove forest (Bismark and
Iskander 2002). In a mixed riverine–mangrove forest of Batu
Ampar District, West Kalimantan, mean group size varies by the
amount of riverine habitat available, e.g., 19 individuals ± SD 2
in narrow strips of riverine habitat and 16 individuals ± SD 2 in
broader strips with double the amount of riverine habitat available (Kartono et al. 2008).
The proportional amount of resting, feeding, and moving
varies with forest type, with feeding activity peaking at 1300
to 1500 h (Salter et al. 1985). For example, in mixed riverine–
mangrove forest of the Sangata River, daily activity budgets are
allocated to resting 42.3% of observation time (5.50 h), moving 25.2%, feeding 23.2%, grooming 1.1%, and playing 8.2%
(Bismark et al. 1994). In riverine forests along the Kinabatangan
River, N. larvatus rests more, feeds less, and moves much less:
76.5% resting, 19.5% feeding, and 3.5% moving (Matsuda et al.
2009a).
Nasalis larvatus has a polygynous mating system with
a single or alpha male, several adult females, and young of
various ages. N. larvatus societies are female-centered, males
remaining aloof from most social interactions (Matsuda et al.
2012a).
Allomothering behaviors include handling and grooming
of infants by adult females other than the mother, who easily
retrieves her infant (Gorzitze 1996; Matsuda et al. 2012a); however, allonursing has not been observed (Kohda 1985).
Copulation is infrequent (e.g., 0.01% of 4,966 scan observations—Boonratana 2011). Females and, less often, males solicit
copulation, which involved 1 mount of mean duration 25 and
27 s in 2 studies (Murai 2006; Boonratana 2011), although up
to 6 mounts have been observed; however, males do not always
accede to female solicitations (Yeager 1990a; Murai 2006;
Boonratana 2011). Females solicit copulation by using a pouting
47(926)—Nasalis larvatus
mammalian species93
facial expression (pursing or pouching the lips) to get the male’s
attention, followed by head-shaking and presenting the hindquarters; she also shakes her head during copulation (Hollihn
1973; Yeager 1990a). Males use a similar pouting expression
when soliciting and both may use this expression after copulation (Hollihn 1973). Females solicit and mate during interestrus
and pregnancy, as well as during estrus (Hollihn 1973).
Non-copulatory mounting also occurs between females,
between females and infants or juveniles, among juveniles, and
between juveniles and infants; those between adult females may
occur shortly after failed solicitations toward males (Yeager
1990a; Murai 2006; Boonratana 2011). Females compete for
mating and may harass a mating pair (Yeager 1990a). Infants and
juveniles may also harass copulating pairs (Boonratana 2011).
In captivity, neonates immediately become the center of
attention, with others of the group huddling around the new
mother and observing the infant (Hollihn 1973). Hollihn (1973)
also notes that, in captivity, females other than the mother carry
new infants and a male held 1 momentarily; the mothers retrieve
their infants without difficulty. After 2 wild births, both females
resumed copulating with the alpha male soon after; in one of the
births that occurred in the daytime, other group members watched
the parturition but were not otherwise involved (Gorzitze 1996).
Both females consumed the placentas.
Nasalis larvatus individuals are less intensely social than
other colobines, displaying relatively fewer intraunit interactions (Matsuda et al. 2012b). For example, in 1 study N. larvatus devoted < 0.5% of total observation time to grooming,
while other direct affiliative interactions were not observed at all
(Matsuda et al. 2012a). It exhibits a low level of aggression, which
is rarely seen in intergroup interactions (Bennett and Sebastian
1988; Yeager 1991b). Boonratana (1993) saw agonistic behavior
involved in only 0.7% (n = 5) and 0.8% (n = 34) of total activity
time in 2 groups, none of which interactions entailed physical
contact; instances included an alpha male chasing away a female
from another group and an alpha male chasing away a male from
another group. Similarly, in 1,968 h of focal observations on the
adult male and 1,539 h on the 6 females, Matsuda et al. (2012a)
recorded just 39 agonistic interactions: 26 were displacements
from sleeping places, 6 were the alpha male threatening others
to mediate quarrels among females and juveniles, and 7 were
displacements from feeding sites. The alpha male’s main role,
besides protection from predators, is to maintain group cohesion
by policing agonistic behaviors of others (Matsuda et al. 2012a).
The low level of aggression is common to the Rhinopithecini
(Yeager 1990b; Matsuda et al. 2012b; Mulder 2012).
There is no clear, linear dominance hierarchy, although specific individuals are more dominated than others (Matsuda et al.
2012a). Most grooming is by females grooming females or juveniles; males rarely or never groom females but females occasionally groom them (Yeager 1990b; Matsuda et al. 2012a).
Although infanticide is rarely observed or suspected in
N. larvatus, 1 case has been reported after an adult male took
over a group (Agoramoorthy and Hsu 2005b); however, this
occurred in disturbed habitat in a semi-wild population that
is provisioned by a tourism operator in Labuk Bay Sanctuary,
Sabah (Agoramoorthy and Hsu 2005a) and may not represent
natural behavior. Murai et al. (2007:121), commenting on this,
noted that “...we never observed infanticide in our study site,
whereas male replacements were observed three times.”
Communication.—The most frequently heard vocalizations are resonant, drawn-out goose-like calls, the female a
little softer than the male’s. Based on multiparametric analysis,
Röper et al. (2014) identified acoustic features of the 4 most
common call types: “shrieks,” “honks,” “roars,” and “brays.”
Of these, 3 are “loud calls” that could be used for noninvasive,
vocalization-based monitoring (Röper et al. 2014). They also
described “choruses” in which multiple callers produced mixed
vocalizations.
During acts of aggression or when alarmed, they make a
very high frequency tonal call, or shriek, the maximum pitch
of which, 1.4–6.8 kHz, is higher than expected based on a comparative study of large primates (Srivathsan and Meier 2011).
The high frequency may be an adaptation for predator avoidance (crocodiles) and intragroup contact in dense vegetation
(Srivathsan and Meier 2011).
Miscellaneous behavior.—Groups swim rivers to avoid
investigators more frequently when naïve than after they
become accommodated, further evidence that swimming can
be a strategy to avoid terrestrial predators (Boonratana 2000).
To cross rivers, Nasalis larvatus selects crossings with narrow bank-to-bank or branch-to-bank distances (Yeager 1991a;
Matsuda et al. 2008a). Groups leap from heights of 5–15 m,
land “with a great splash” and after surfacing, swim directly to
the far shore (Boonratana 2000:11).
The selection of riverside sleeping places also appears to be
mainly a predator-avoidance strategy because neither temperature nor food availability differs between riverside and inland
sites where N. larvatus feeds during the day (Matsuda et al.
2011b).
Adult males may confront intruders while the others depart,
except for humans to which they are habituated (Kern 1964).
I observed (Kinabatangan River, May 2011) that, when a female
and infant were surprised at close range, the infant instantly
dropped to the ground followed quickly by the female and both
escaped to another tree under cover of the understory.
GENETICS
Cytogenetics.—Unlike other colobines (e.g., African colobines, surilis, lutungs, langurs, duoc-langurs, and snub-nosed
monkeys) in which the diploid chromosome number (2n) = 44,
the diploid number in Nasalis larvatus is 48 (Chiarelli 1966;
Chen et al. 1979). Chiarelli (1966) defined 4 groups of chromosomes with similar dimension and morphology: (a) 7 pairs
of metacentric chromosomes, of which pairs 6 and 7 are of
the same size and distinctly smaller than pair 5; (b) 9 pairs all
submetacentric; (c) 7 pairs of small chromosomes, all submetacentric; and (d) 1 pair marked by a large achromatic region on
94
mammalian species47(926)—Nasalis larvatus
one of the arms. The karyotype of N. larvatus is derived (not
basal as previously thought), nested within Asian colobines and
shares a common period of descent with other odd-nosed colobines after the divergence of duoc-langurs (Bigoni et al. 2003).
A pericentric inversion links Nasalis (and presumably the other
Rhinopithecini) with the lutungs (Stanyon et al. 2008).
Molecular genetics.—Nasalis occupies a monophyletic
clade of odd-nosed monkeys, or Rhinopithecini, that also
includes simakobu, duoc-langurs, and snub-nosed monkeys
(Sterner et al. 2006; Whittaker et al. 2006). Based on noncoding nuclear genes and the mitochondrial genome (mtDNA),
Nasalis and snub-nosed monkeys form a sister clade to duoclangurs and the odd-nosed group as a whole forms a sister
taxon with surilis (Zhang and Ryder 1998; Liedigk et al. 2012;
Wang et al. 2012). The odd-nosed clade including the ancestors
of Nasalis diverged from the Presbytini (langurs, lutungs, and
surilis—Groves 2001) about 7–10 million years ago (Sterner
et al. 2006; Md. Zain et al. 2010; Meyer et al. 2011; Roos et al.
2011). Age of divergence estimates based on mtDNA suggest
that the lineages leading to snub-nosed monkeys, duoc-langurs,
and Nasalis+simakobu originated in the late Miocene, about
7.3 million years ago, Nasalis+simakobu split from duoc-langurs 6.3 million years ago, and Nasalis and simakobu diverged
in the early Pleistocene, 2.5 to 1.75 million years ago (Liedigk
et al. 2012; Wang et al. 2012).
Population genetics.—Salgado-Lynn et al. (2010) found
little genetic structure in microsatellite markers among 33 samples from around Sabah: a mean of 6.25 alleles per locus and
a mean expected heterozygosity of 0.674; all but 1 locus were
in Hardy–Weinberg equilibrium, and there is no evidence for
linkage disequilibrium between loci. There is also no identifiable population structure within populations, based on mtDNA
control region analysis of Klias River subpopulations (MunshiSouth and Bernard 2011). However, the haplotypes of the mitochondrial control region in 5 captive N. larvatus in Japan were
well differentiated from the haplotypes previously reported in
wild populations from northern Borneo, indicating a greater
amount of genetic diversity in proboscis monkeys than previously reported (Ogata 2014).
CONSERVATION
Nasalis larvatus is listed as “Endangered” by the
International Union for Conservation of Nature and Natural
Resources (Meijaard et al. 2008) and is on Appendix I of CITES
(Convention on International Trade in Endangered Species of
Wild Fauna and Flora 2012). By 1986, 40% of N. larvatus habitat had been lost (International Union for Conservation of Nature
and Natural Resources data cited by McNeely et al. 1990). This
figure reached 49% lost by 1995, continuing at a rate of 2% lost
per year (Bismark 2010). In 1997–1998, forest fires, the result
of a disastrous project to convert peat-swamp forest to rice
cultivation in Kalimantan, burned about 400,000 ha of forest
(Tisdell and Nantha 2007) and destroyed the greatest proportion
of remaining N. larvatus habitat of any primate in Kalimantan
(Meijaard et al. 2008).
Logging and conversion of forest to oil palm plantations are
the major threats and both continue to accelerate in many areas.
Along the Kinabatangan River, the effect of habitat loss is exacerbated by tourism, which disturbs N. larvatus in the few stands
of tall riverine trees that are left (Boonratana 2013). Population
viability analysis predicts that, in the absence of further management efforts, a population in a protected area in Sabah will
remain fairly stable, while 2 populations in protected areas in
Kalimantan will decrease by more than half, the smaller going
effectively extinct in 30 years (Stark et al. 2012). In that study,
fire associated with land clearing for agriculture has the greatest
impact and hunting the next greatest impact.
At least 1 population (in Pulau Kaget Nature Reserve) has
recently become extirpated and others are likely to follow at
current rates of habitat loss and hunting (Meijaard and Nijman
2000b). Indeed, maps of its current distribution (e.g., Meijaard
and Nijman 2000b; Sha et al. 2008) show large stretches of
coastline and major rivers with seemingly suitable habitat but no
recent observations. Sha et al. (2008:113) found that only 15.3%
of the population in Sabah occurred within protected forest
reserves and urged “greater efforts ... to restoring remnant habitat patches as well as re-establishing corridors along fragmented
river systems, ... linking major populations through a protected
area network.” In Kalimantan, unfortunately, there is no difference in deforestation rates between non-protected and protected
areas, which consequently provide little security for N. larvatus
(Curran et al. 2004). By modeling mangrove habitat use in Kutai
National Park, Suwarto (2015) showed that N. larvatus selected
areas of dense vegation, presence of particular food tree species
and proximity to water, while avoiding roads and settlements,
limiting them to only 18.8% of the park, of which just 1.35%
was high suitability habitat.
Nasalis larvatus can adapt to certain developments, such as
rubber plantations, as long as heterogeneity of vegetation types
and access to water are maintained (Soendjoto 2005). Another
example is the private 162 ha Labuk Bay Sanctuary, where a
population last counted at 89 persists within an oil palm plantation where only high-saline mangrove plants are available
(Agoramoorthy and Hsu 2005a). N. larvatus damages crops
by feeding on young leaves and flowers of rubber trees and the
young leaves of coconut (Soendjoto et al. 2003). It can utilize
logged forest as long as it has suitable tree cover, security, and
food, but illegal gold mining in the headwaters is a threat in
some areas (e.g., Kendilo River, East Kalimantan—Rachmawan
2006). Hunting is significant in some areas, mainly by inland
Dyak and Iban ethnic groups, because monkey meat is prohibited to Muslims, who are mostly ethnic Malays and predominate
along the coast (Meijaard and Nijman 2000a).
Manansang et al. (2005:3) noted that, “Although ...the proboscis monkey in the wild probably numbers > 10,000 individuals, the species still has an unacceptable risk of extinction...
because of unsustainable (and largely illegal) rates of deforestation that devastate proboscis monkey habitat, because existing
47(926)—Nasalis larvatus
mammalian species95
populations are almost entirely too small to be viable in the long
term and are highly isolated from each other, and because forest fires are becoming more frequent and severe—due mostly to
anthropogenic factors.”
Despite recent conservation initiatives, to prevent N. larvatus from declining further will require greater efforts to close
the gap between policy and implementation, establish more (and
more effective) community-based reserves, increase community awareness, reinforce traditional laws protecting monkeys,
reconnect isolated habitat through reforestation, and improve
law enforcement (Tisdell and Nantha 2007; Kartono et al. 2008;
Nijman and Meijaard 2008; Sha et al. 2008; Soendjoto et al.
2008; Purba 2009; Ridzwan Ali et al. 2009; Bismark 2010; Hon
2011; Stark et al. 2012). Ex situ conservation may also play a
role if captive breeding can obviate the need for N. larvatus to
be captured in the wild for zoos and to augment or restore wild
populations (Manansang et al. 2005).
ACKNOWLEDGMENTS
T. Harrison, Ir. A. P. Kartono, J. Krigbaum, I. Matsuda,
J. Munshi-South, V. Nijman, K. Röper, and E. Sargis provided
research material. P. Gomez and staff of the Bibliothèque nationale de France and A. Lemaire and staff of the Muséum national
d’Histoire naturelle, Paris, facilitated access to many of the rare
books cited herein. C. Groves reviewed an earlier version of the
synonymies. P. Myers photographed the skull.
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Associate Editor and Editor of this account was Meredith J. Hamilton.