Systematic review of the Taiwanese macaque, Macaca cyclopis, Swinhoe, 1863

78 Pages·2001·3.4 MB·English

by  Fooden, Jack, 1927-

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FIELDIANA
Zoology
NEW
SERIES, NO. 98
Systematic Review of the Taiwanese Macaque,
Macaca cyclopis Swinhoe, 1863
Jack Fooden
Adjunct Curator
Division ofMammals
Department ofZoology
FieldMuseum ofNatural History
1400 South Lake Shore Drive
Chicago, Illinois 60605-2496
U.S.A.
Wu
Hai-Yin
AIsnsstiisttuatnetoPfrNoafteusrsaolrResources H'"d^JUMWAVRWyfQVFJTT!H<E>
National Dong Hwa University
Hualien, Taiwan J^U ? 2002
R.O.C. 974
Accepted February 16, 2001
Published November 30, 2001
Publication 1515
PUBLISHED BY FIELD MUSEUM OF NATURAL HISTORY
2001 Field Museum of Natural History
ISSN 0015-0754
PRINTED IN THE UNITED STATES OF AMERICA
Table of Contents Neonatal Sex Ratio, Twinning, Birth Weight
30
Infant Mortality 30
Abstract 1 Nursing; Longevity 31
Introduction 1 Population Growth Rate 31
Geographic Distribution; Island-wide Fossils 31
Taxonomy 32
Population Estimate 2
Pelage 2 Synonymy 32
General Characterization 2 Type Series 32
Age and Sex Variation 2 Type Locality 33
Remarks 34
Seasonal and Geographic Variation 3
Evolution and Dispersal 36
Albinism 3
External Measurements and Proportions Acknowledgments 38
Literature Cited 38
3
Cranial Characters 3 Note Added in Proof 45
Appendix Specimens Examined 46
Molecular Biology and Genetics 9 1:
Mitochondrial DNA 9 Appendix 2: Gazetteer of Macaca cyclopis
Nuclear DNA 12 Localities 47
Blood Proteins 14
Karyology 15
Parasites 17
List of Illustrations
Protistans 17
Flagellates 17
Amebas 17
Malaria 17 1. Locality records ofMacaca cyclopis 4-5
2. External characters in Macaca cyclopis 10
Ciliate 18
3. Tail length vs. head and body length in
Trematodes 18
Macaca cyclopis 12
Cestodes 19 4. Skull of adult female Macaca c>'c/o;j/5 14
Nematodes 19
5. Skull of adult male Macaca cyclopis 15
Leech 20
6. Map of southwestern Taiwan showing col-
Lice 20 lecting localities of fossil monkey teeth 34
Viruses 20 7. Fossil monkey teeth collected in southwest-
B Virus 20 em Taiwan 35
Reovirus 20
Simian Foamy Virus 20
Simian Virus 40 21
Natural History 21 List of Tables
Habitats 21
22
Terrestriality/Arboreality
Group Size and Composition 22 1. External measurements and proportions in
Home Range Area and Population Density ... 23 Macaca cyclopis 11
Diet 23 2. Mean birth weight reported in laboratory-
Predators 26 born Macaca cyclopis 12
Intergroup Dispersal 26 3. Cranial measurements and proportions in
Reproduction 26 Macaca cyclopis 13
Seasonality 26 4. Local variation in greatest length of skull
Sexual Skin 26 in wild-collected Macaca cjc/op/5 16
Polythelia 28 5. Sister groups and divergence ages ofMa-
Menstrual Cycles 28 caca cyclopis as determined in five stud-
Sexual Maturation 29 ies of mtDNA infascicularis-group spe-
Copulation 29 cies 16
Gestation and Parturition 29 6. Allele frequencies at blood-protein loci in
Reproductive Rate 29 samples ofMacaca cyclopis 17
m
7. Incidence oftrypanosome infections 15. Incidence of simian virus 40 infections
(Trypanosoma cf. conorhini) detected in detected in Macaca cyclopis 21
samples of natural populations ofMacaca 16. Elevational distribution ofMacaca cyclo-
cyclopis 17 pis locality records 22
8. Incidence ofameba species detected in 17. Geographic variation in group size in Ma-
unlocalized fecal samples ofMacaca cy- caca cyclopis populations 23
clopis 18 18. Ratio of sexually mature males to sexual-
9. Incidence of natural malarial infections ly mature females reported in Macaca cy-
detected in surveys ofMacaca cyclopis clopis groups 24
populations 18 19. Home range area and population density
10. Incidence oftrematode parasite infections reported in Macaca cyclopis 24
detected in Macaca cyclopis samples 19 20. Foods reported eaten by Macaca cyclopis .. 25
11. dIentceicdteendceinoffecceasltsodaempplaersasoitfeMiancfeacctaioncsy- 2221.. OMsobensnaeslrtivrtauytailinoncMsyacclceoancdcuaerracntyiicnolgnopriienspcraopdtuicvteivMeasceaa-- 27
clopis 19 ca cyclopis 28
12. Incidence ofnematode parasite infections 23. Annual reproductive rate in natural popu-
detected in samples of natural populations lations ofMacaca cyclopis 30
ofMacaca cyclopis 20 24. Neonatal sex ratio in natural populations
13. Incidence ofanti-B virus antibodies de- ofMacaca cyclopis 31
tected in/aidcM/am-group macaques 21 25. Taiwanese fossil monkey teeth: measure-
14. Incidence of simian foamy virus, type 1 ments and collection information 33
and type 2, detected in samples of natural 26. Dental measurements in wild-collected
populations ofMacaca cyclopis 21 specimens ofMacaca cyclopis 36
IV
Systematic Review of the Taiwanese Macaque,
Macaca cyclopis Swinhoe, 1863
Wu
Jack Fooden and Hai-Yin
Abstract
The Taiwanese macaque, Macaca cyclopis Swinhoe, 1863 ("1862"), is systematically re-
viewed, based on examination of 237 museum specimens, survey of relevant literature, and
observation ofnatural populations. This review includes analyses ofpelage characters, external
measurements and proportions, cranial characters, molecular biology and genetics, and para-
sites. Information also is presented concerning natural history, reproduction, fossils, and tax-
onomic history. A hypothetical interpretation of the evolutionary history of this species is
proposed. In an appendix, an annotated gazetteer lists 429 localities at which M. cyclopis has
been collected or observed.
Introduction AMNH American Museum of Natural History,
New York (3)
Macaca cyclopis is endemic to Taiwan and is ANSP Academy ofNatural Sciences, Philadel-
the only species of nonhuman primate native to phia (1)
this subtropical island, which is situated 140 km bm(nh) British Museum (Natural History), Lon-
offthe coast ofmainland China. The existence of don (3)
monkeys on Taiwan became known to Western JMC Japan Monkey Centre, Inuyama, Japan
science as a result of a visit there in 1715 by the (45)
Jesuit missionary Pere J.-A.-M. de Moyria de KUPRi Kyoto University Primate Research In-
Mailla (Du Halde, 1735, pp. xxxiv, 162; Camp- stitute, Inuyama, Japan (53)
bell, 1903, pp. 504, 506). The first scientific spec- Mcz Museum of Comparative Zoology, Har-
imens of M. cyclopis were collected ca. 1862 by vard University, Cambridge, Massachu-
Rn.amSewionfhotehe(1s8p6e3c,ieps.,35w0h)o, awuathsorthoefnthtehetecBhrniitciaslh NMNS Nseatttison(1a)l Museum of Natural Science,
vmlaseniyucdcsst,ete-eedcmpuoarmntfosirbucsoalpbmselatcyusnidsamiiateegsusnnrseaaoldfhctatpoohvonieptsshueelssqapuuitebesicsnlioeacennqessdu,.ehn(RartAevellpleyaapttebiibnevveedeeelnilnyyxpcffuoee1bl)ww--, SNTMUTZD TmSNtaaeaitnacittholunoinafcglh,ZeosTToaaliioMwwguayas.nneT(uUa1nim6pi)eviefri(isr7i)tyT,ierDkeupnadret,-
lished (see Synonymy, below). Dresden (1)
The present review of M. cyclopis is based on TESRi Taiwan Endemic Species Research In-
the study of237 museum specimens (62 ofwhich stitute, Chichi, Taiwan (14)
were collected at known localities), survey ofrel- TM Taiwan Museum, Taipei (12)
evant literature, and observation of natural popu- UMMZ Museum of Zoology, University of
lations. Specimens examined are preserved in in- Michigan, Ann Arbor (2)
stitutions listed below, which hereafter are cited USNM National Museum of Natural History,
by means ofthe indicated abbreviations; the num- Washington, D.C. (41)
ber of M. cyclopis specimens in each institution Yio Yamashina Institute for Ornithology,
is indicated by a parenthetical notation. Abiko, Japan (2)
FIELDIANA: ZOOLOGY, N.S., NO. 98, NOVEMBER 30, 2001, PP. 1-70
ZMB Zoologisches Museum des Humboldt- ivaceous) to golden brown; more caudally, on the
Universitiit. Berlin (25) lumbosacral region, the color gradually brightens
Private collections (11) to a richer golden brown. In individual hairs on
the dorsal thoracic region, the basal two-thirds is
grayish brown and the distal one-third is conspic-
uously marked by 1-3 bands of pale golden (cf.
Geographic Distribution, Island-wide Inagaki. 1996. p. 91). On the lumbosacral region,
Population Estimate the base of individual hairs is paler than in hairs
on the dorsal thoracic region, and the distal bands
Locality records ofM. cyclopis are widely dis- are more erythristic. The crown generally is
tributed in the mountainous eastern two-thirds of somewhat paler than the dorsal thoracic region,
Taiwan Island (Fig. 1): questionnaire and field but it is not as brightly colored as the lumbosacral
surveys indicate that this species currently inhab- region. The skin of the thinly haired face is pink-
its 111 of270 townships (41.17f) in Taiwan (Hai- ish to reddish. Surrounding the face, on the fore-
Yin Wu. Ling-Ling Lee. and Shih-Wei Chang, head and cheeks, is an indistinct fringe of some-
2001. unpublished report). Prior to intensive hu- what elongated blackish hairs. The lateral facial
man settlement and agricultural exploitation ofthe crest, which is pale grayish brown, is restricted to
western lowlands, macaques probably also were the posterior mandibular region (infrazygomatic
fairly common there, judging from Pere de Mail- crest; Fooden, 1995, p. 19). The proximodorsal
la's observations in western Taiwan in 1715 (Du surface of the limbs is approximately the same
Halde. 1735. pp. xxxiv. 162). Local disappearance color as the adjacent dorsal surface of the trunk;
ofmacaques in western Taiwan was noted in 1862 more distally, the dorsal surface ofthe limbs grad-
by Swinhoe (1863. p. 351). The natural geograph- ually becomes somewhat more grayish. The prox-
ic distribution ofM. cyclopis apparently does not imal one-third of the dorsal surface of the tail is
extend to any of the small islands that surround approximately the same color as the lumbosacral
Taiwan Island (Fig. 1). region; the distal two-thirds of the dorsal surface
Introduced feral populations of M. cyclopis ofthe tail is dark grayish brown to clearly defined
have become well established at four localities in blackish. The ventral surface of the trunk, limbs,
Japan: (1) Oshima, a small island south ofTokyo, and tail is pale grayish. For a discussion ofsexual
M. cyclopis population introduced sometime be- skin coloration, see Reproduction below.
tween 1942 and 1953: (2) Nojima, a small island Dorsal pelage color in M. cyclopis is generally
south of Nagoya, population introduced in 1958: similar to that in many specimens of M. fascicu-
(3) Wakayama Prefecture, south of Osaka, popu- laris (Fooden, 1995. p. 3), but the color contrast
lation introduced ca. 1960: and (4) Shimokita between the dorsal thoracic region and the lum-
Hanto (= Peninsula), at the northern tip of Hon- bosacral region is greater in M. cyclopis. Dorsal
shu (near the northern limit of distribution of M. pelage color in M. cyclopis is generally darker
fuscata), population introduced in 1971. For fur- than that in M. mulatta (Fooden, 2000, p. 7), and
therdetails concerning these feral populations, see the color contrast between the dorsal thoracic re-
Appendix 2: Gazetteer. gion and the lumbosacral region is less in M. cy-
Based on an ongoing survey conducted since
clopis.
1996 by Ling-Ling Lee. Shih-Wei Chang. G. Hair stream patterns on the trunk and extremi-
Agoramoorthy. and Hai-Yin Wu. the total extant ties ofM. cyclopis have been studied in detail by
population ofM. cyclopis in Taiwan has been es- Yasugawa (1960, p. 330).
timated to be ca. 250.000 100.000 individuals
in ca. 10,000 5.000 groups.
Age and Sex Variation
Pelage Neonatal pelage is dark gray to blackish (Hor-
ikawa, 1932. p. 69; Kuroda, 1940, p. 269; Hsu.
General Characterization 1990. p. 66). In older infants (usnm 294177, Ml
(Fig. 2) not erupted, age ca. 9 months), pelage color is
approximately the same as that in adults, but hairs
The dorsal surface of the thoracic region in are shorter and finer than in adults. Pelage color
postinfantile M. cyclopis is yellowish brown (ol- is generally similar in females and males, but the
FIELDIANA: ZOOLOGY
dark dorsal surface of the distal two-thirds ofthe Jachowski (1968, p. 1 1) asserted that body size is
tail is more blackish in fully adult males than in greater in northern M. cyclopis than in southern
fully adult females (H.-Y. Wu, pers. obs.)- M. cyclopis, no external measurement data are
available to test this statement (cf. Cranial Char-
acters below). A brief summary of crown-rump
Seasonal and Geographic Variation length measurements in 116 wild-collected but
unlocalized specimens has been reported by Satoh
&
Although evidence ofmolting was not detected et al. (1956, p. 42; cf. Setoguti Sakuma, 1959,
in M. cyclopis skins examined, Namiye (1914, p. p. 158; Lin, 1976, p. 75).
214) has reported that winterpelage is darkerthan Relative tail length (T/HB) apparently is similar
summer pelage. Based on observation at several in adult females and males, varying from approx-
localities in Taiwan, Jui-Hua Chu (ntuz; pers. imately 0.65 to 0.95 (Fig. 3). In pooled samples
comm., 16 Apr. 2000) confirms that annual molt- (Table 1), mean relative tail length is0.82 0.058
ing occurs in M. cyclopis during the period May- (SD) in 24 adult females and 0.85 0.089 in 8
August. adult males. This ratio apparently remains rela-
The available sample of wild-collected skins is tively constant from late fetal life to adulthood.
insufficient to determine whether or not pelage The hind foot apparently grows more slowly
color varies geographically in M. cyclopis. than the head and body from infancy to adulthood
(Table 1). The same probably also is true of the
ear, but data are ambiguous on this point.
Albinism Body weight (Table 1) is 8.12 kg in one wild-
&
collected adult male (cf. Setoguti Sakuma,
Two or three albino captives ofM. cyclopis re- 1959, p. 158) and varies from 6.30 kg to 18.50
pp1oe4rr1ti,eodd1l4y21;9o7Ar8ni-go1inn9ya8mt0eodu(Psio,nirHi1eu9r8a1l&,iepDn.a4vH7is)di,seoannn,ddua1rn9i7na9gl,biptnph.oe k7al5g.;,iP1no9i8nr4ii,neerp.c&a3p8tD6ia;vveSimdasidotunhl,t&m1a9Jl7ue9n,sgerp(.csf,.131L99i;9n7,M,a1pk9.i75t64,a4)pe..t
juvenile was captured by local residents at Wu- The female/male weightratio is 0.66 in 36 captive
shihkeng, Taichung Hsien, in the early 1990s adults. Mean birth weight is 402 g in 89 captives
(photograph in possession of H.-Y. Wu). Aber- born in colonies inTaipei and430g in 22 captives
rantly pale specimens of M. cyclopis previously born in a colony in Southboro, Massachusetts (Ta-
had been reported elsewhere inTaiwan by Kuroda ble 2).
(1940, p. 269) and Jones (1973, p. 370).
Cranial Characters
External Measurements and (Figs. 4, 5)
Proportions In wild-collected specimens examined of M.
cyclopis, the greatest length of the skull in adult
External measurements are available for only males (125.2 mm, n = 15) averages approximate-
ten wild-collected specimens of M. cyclopis (Ta- ly 13% greater than in adult females (1 10.4 mm,
ble 1); of these, two are adults one female and n = 12) (Table 3). Skull length in both sexes of
one male and eight are immatures. To supple- M. cyclopis tends to exceed that in M.fascicularis
ment these meager data, measurements ofcaptive and M. mulatta (cf. Fooden, 1995, p. 38; 2000, p.
specimens and specimens of unknown history 38). Available measurements of wild-collected
also are presented; however, these measurements specimens ofM. cyclopis are inadequate to indi-
probably are not directly comparable with those cate whether or not skull length varies geograph-
of wild-collected specimens. The following infer- ically in this species (Table 4). In captive speci-
ences are based on the limited avmaimlable data. mens of M. cyclopis, greatest length of the skull
Head and body length is 440 in one wild- tends to exceed that in wild-collected specimens
collected adult female and 650 mm in one wild- (Table 3; P < 0.02; cf. Komatsu, 1944. p. 18;
collected adult male (Table 1). The female/male Mouri, 1995, p. 189; Koppe et al., 1999, p. 78).
length ratio is 0.68 in the two wild-collected The rostrum is moderately projecting in M. cy-
adults, 0.86 in 25 captive adults, and 0.97 in six clopis, more similar to that in M.fascicularisthan
adults of unknown history. Although Bergnerand to that in M. mulatta (cf. Murie, 1873, p. 779;
FOODEN AND WU: SYSTEMATIC REVIEW OF MACACA CYCLOPIS
0)
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FIELDIANA: ZOOLOGY