Journal of Threatened
Taxa | www.threatenedtaxa.org | 26 September 2023 | 15(9): 23836–23842
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.8179.15.9.23836-23842
#8179 | Received 07
September 2022 | Final received 04 August 2023 | Finally accepted 20 August
2023
New localities and sexual
dichromatism in Blue-green eyed Spotted Cuscus Spilocuscus
wilsoni Helgen et
Flannery, 2004 (Mammalia: Marsupialia: Phalangeridae) from Biak Island, Indonesia
Aksamina Maria Yohanita
1, Kanthi Arum Widayati
2, Tri Atmowidi 3, Hiroo Imai 4 & Bambang Suryobroto
5
1-3,5 Department of Biology, IPB
University, Kampus IPB Dramaga,
Bogor, Indonesia.
4 Molecular Biology Section, Center
for the Evolutionary Origins of Human Behavior (eHUB),
Kyoto University, Inuyama, Aichi 484-8506, Japan.
1 a.yohanita@unipa.ac.id, 2 kanthiarum@gmail.com
(corresponding author), 3 atmowidi@apps.ipb.ac.id, 4 imai.hiroo.5m@kyoto-u.ac.jp,
5 suryobroto@apps.ipb.ac.id
Editor: Spartaco
Gippoliti, Socio Onorario Società Italiana per la Storia della Fauna “Giuseppe Altobello”,
Italy. Date of publication:
26 September 2023 (online & print)
Citation: Yohanita, A.M., K.A. Widayati, T. Atmowidi, H. Imai
& B. Suryobroto (2023).
New localities and sexual dichromatism in Blue-green eyed Spotted Cuscus Spilocuscus wilsoni
Helgen et Flannery, 2004 (Mammalia: Marsupialia: Phalangeridae) from
Biak Island, Indonesia. Journal of Threatened Taxa 15(9):
23836–23842. https://doi.org/10.11609/jott.8179.15.9.23836-23842
Copyright: © Yohanita
at al. 2023. Creative Commons Attribution 4.0
International License. JoTT allows unrestricted use,
reproduction, and distribution of this article in any medium by providing
adequate credit to the author(s) and the source of publication.
Funding: This
study was funded by Penelitian Disertasi
Doktor contract number 1967/IT3.L1/PN/2021 from the
Ministry of Research, Technology, and Higher Education to KAW. JSPS Kakenhi 21KK0130 (Fund for the Promotion of Joint
International Research (Fostering Joint International Research (B)) and Future
Development Funding Program of Kyoto University Research Coordination Alliance
to KAW.
Competing interests: The authors declare no competing interests.
Author details: Aksamina Maria Yohanita has studied small mammals in Papua for approximately 15 years since joining as a lecturer at the University of Papua, Manokwari. Currently, she is registered as a student in the animal biosciences doctoral program at Bogor Agricultural University. Dr. Kanthi Arum Widayati is working as a lecturer in the Department of Biology, Bogor Agricultural University. She is specialized in primatology and focuses on experimental biology and human biology. Dr. Tri Atmowidi is the head of the Animal Bioscience study program, Bogor Agricultural University (IPB University). He is specialized in Entomology and focuses on the Insect pollinator biology. Prof. Hiroo Imai is a professor in molecular and cellular biology at the Molecular Biology Section, Center for the Evolutionary Origins of Human Behavior (eHUB), Kyoto University. Bambang Suryobroto is working as a senior lecturer in the Department Biology, Bogor Agricultural University. He
is specialized in the life history and focuses on symmetry/asymmetry. He is also supervising PhD scholar in the field of anthropology, mammalogy, and developmental biology.
Author contributions: AMY: field work, conceptualization, and manuscript writing; KAW: conceptualization, manuscript writing, and review; TAW, HI, and BS: review.
Acknowledgements: The authors would like to thank the field guide and
assistants for the cuscus survey. We also thank the Head of the Biak Bird and
Orchid Park for the permission to access the cuscus in captivity.
Abstract: Spotted cuscuses are
medium-sized tree-dwelling mammals native to tropical forests of Australo-Papua that primarily feed on fruits and leaves.
They belong to the phalangerid genus Spilocuscus (Gray,
1862). The difference in pelage color between male and female Spilocuscus wilsoni has
not yet been well described morphologically. In the present study, we describe
the coat color of four S. wilsoni individuals:
a male adult, a sub-adult male, a sub-adult female, and a juvenile female.
Dorsal, lateral, and ventral body section images were captured on camera, and
body weight & length, tail & ear length were measured. The adult
male S. wilsoni had
brown spot and blotch patterns on the dorsal and lateral regions, and the
ventral region was plain beige. The sub-adult male had distinct spot
patterns without blotches on the dorsal and lateral regions, while the ventral
region was plain with a cream base color. The sub-adult female had a mottled
pattern that blended with the base color, making a silvery appearance. The female
juvenile was spotless throughout, with a foundation hue ranging from creamy to
somewhat yellow.
Keywords: Biak Island Spotted Cuscus, coat
color, medium-sized tree-dwelling mammal, morphologically describe.
INTRODUCTION
Spotted cuscuses are medium-sized
tree-dwelling marsupials that primarily feed on fruits and leaves and are
native to tropical forests of Australo-Papua. They
belong to the phalangerid genus Spilocuscus (Gray,
1862). Previously, Biak Island’s Spotted Cuscus was considered belonging to the
group S. maculatus (Flannery 1995b), but later it
was separated as a new species Spilocuscus wilsoni Helgen et
Flannery, 2004. Among all the species of Spilocuscus,
this is the only one that possesses blue-green eyes. S. wilsoni is one of the smaller species from
genus Spilocuscus that coexist with S.
maculatus on Biak Island.
S. wilsoni is
found exclusively on the oceanic islands of Biak-Supiori,
located in the northern region of New Guinea. Biak-Supiori
Island has an area of 2,497 km2, located off the coast of Sahul,
which has no connection with mainland New Guinea. The endemicity and restricted
range of S. wilsoni make
it ‘Critically Endangered’ on the IUCN Red List (Aplin
& Helgen 2016). The description of S. wilsoni was based on two samples; a juvenile
male (holotype) and an adult male (paratype) from the Rijksmuseum van Natuurlijke Historie, Leiden,
Netherlands (RMNH) (now Naturalis) (Helgen &
Flannery 2004). Furthermore, an immature individual of unspecified sex,
residing as a domesticated animal within a family setting on Biak, was captured
in photograph by Flannery 1992, and constitutes an additional paratype (Helgen & Flannery 2004).
The description of S. wilsoni is based on craniodental characters and coat
color diagnosis of an adult male (paratype) on dry skin. The adult paratype has
a pure white coat dorsally and ventrally, shared only with S.m. maculatus of northern New
Guinea (Helgen & Flannery 2004). The immature
holotype is known to be male, however, there is no information about coat color
and body size (Helgen & Flannery 2004).
The pelage color description is
essential in the identification of species and individuals. Although the
identification of species involved adult individuals, immature individuals also
need to be known because the pelage colors of mammals are not necessarily fixed
throughout their lifetimes (Caro & Mallarino
2020). Baby marsupials, including cuscus, have pink skin and very little hair,
and most weigh less than 0.01% of the mother’s weight at birth (Hughes &
Hall 1988). The difference in pelage color between male and female S. wilsoni has not yet been well described
morphologically. We found that sub-adult S. wilsoni show sexual dicromatism
(mottled in females versus spotted and pale color in males), a limited
phenomenon among mammals (Caro 2009) but not unusual among cuscuses (Flannery
1995a,b; Caro 2013).
In this study, we describe the
coat color pattern of an adult male, sub-adult male, sub-adult female, and
juvenile female of S. wilsoni.
We also measured the body and marked the location where S. wilsoni was found for this distribution data.
MATERIAL AND METHODS
This study was conducted from
July 2021 to October 2021. Four individuals of S. wilsoni from Biak represented the age
categories of adult male, sub-adult male, sub-adult female, and juvenile
female, one individual, respectively. Information on the origin of the cuscus
habitat was obtained directly from a local resident for 1, 2, and 3 and from a
keeper in the Biak Bird and Orchid Park for 4 (Figure 1). The subjects were
recorded using Canon EOS 750D digital camera with Canon lens EF-S 18–55
mm/F3.5–5.6 (Canon, Tokyo, Japan) in the RAW format. Photographs of the dorsal,
lateral, and ventral areas are made in the same frame with a color checker
passport. S. wilsoni body
measurements include weight (W), head-body length (HBL), tail length (TL), and
ear length (EL). All length measurements are in centimeters and weight
measurements are in grams. This study has received approval from the IPB Animal
Ethics Commission (Number 207-2021 IPB).
RESULTS
Adult male
The adult male appears to have a
creamy base color and brown spotted and blotched morphs. The spotted and
blotched morphs dominate the dorsum and flank, spreading from the head, back,
limbs, and half of the tail. The blotch of the head is very dark, and the ears
are covered with hair. The muzzle is hairless and darker in color compared to
the chin area. The pelage on the foot is darker than the arms. Some ends of the
hair strands look blackish and silvery in the dorsum and flank areas, while the
ventral area does not. The ventral coat is creamy from the chin and belly to
the limbs. This individual has blue-green eyes. The body measurements are as
follows: W = 2,480 g; HBL = 46.5 cm; TL = 44 cm; and EL = 2.5 cm. This
individual was found in the secondary forest around Warsa
village, northern Biak (Image 1).
Sub-adult male
The sub-adult male appears to
have a more dominant creamy base color, and the spotted morph is brown. Spotted
morphs spread from the head, back, limbs, and half of the tail but is less than
that of adults. The blotch area of the head is brown, the area from the cheeks
to the chin is creamy, and the ears are covered with hair. The pelage on the
foot is dark. The ventral coat is creamy and a little orange in the chest area.
This individual has blue-green eyes. The body measurements are as follows: W =
1,300 g; HBL = 36 cm; TL = 35 cm; and EL = 2 cm. This individual was found in
the secondary forest around Makmakerbo Village,
eastern Biak (Image 2).
Sub-adult female
The whole body of this sub-adult
female is a mixture of creamy, light brown, and dark brown colors. The hair of
the head area is a mixture of light brown on the face and dark brown on the
head. The ears are covered with brown hair. The hair on the dorsum and flank
areas has a mottled pattern of creamy and dark brown, while the tail area is
light brown. The ends of the hair strands on the dorsum and flank areas appear
silvery-buff hairs. The pelage on the foot is darker than the arms. The
creamy-colored ventral area looks like a coat from head to legs. The belly part
has an unopened sac. This individual has blue-green eyes. The body measurements
are as follows: W = 1,100 g; HBL = 33 cm; TL = 30.7 cm; and EL = 1.5 cm. This
individual was found in the secondary forest around Swandiwe
Village, western Biak (Image 3).
Juvenile female
The whole body of this juvenile
female looks creamy and unspotted (dorsum, flank, and belly visible). The hair
on the head is thinner than that on the body. The muzzle is hairless and pink,
and the ears are covered with light yellow hair. The dorsum and flank parts,
including the legs, are creamy and look a little yellow in the upper back. Some
ends of the hair strand on the dorsum and flank areas appear blackish and
silvery. The belly part has an unopened sac. This individual has yellow-green
eyes. The body measurements are as follows: W = 825 g; HBL = 30 cm; TL = 28.5
cm; and EL = 1.5 cm. This individual cuscus was found in the secondary forest
around Warbekwan Village, northern Biak (Image 4).
DISCUSSION
Our observation of the coat
colors of four individual S. wilsoni showed
differences in pelage color patterns between males and females. The female had
a mottled pattern throughout the dorsal and lateral to ventral edges and
appeared to be wearing a coat. The male had a spotted and blotched
pattern on the dorsal and lateral areas, while the ventral area was unspotted.
We conclude that the sub-adult S. wilsoni shows
sexual dichromatism (mottled in females versus spotted and pale color in
males). Some cuscuses have spots or dorsal stripes; the spotted cuscuses S. maculatus and S. rufoniger show sexual dichromatism as females
lack spots (Flannery 1995a; Helgen & Flannery
2004; Caro 2013), except for S. papuensis in
which both males and females had spots (Table 1). The spotted cuscus has a
unique color, especially in females, and it is recorded that four species
inhabit the mainland and islands of Papua. The female S. maculatus in
the northern islands is plain yellowish-white, while in mainland Papua it is
yellowish-white with orange markings from mid-back to the abdomen. Furthermore,
the S. rufoniger female
displays black saddle markings that cover both the mid-back and hind limbs (Helgen 2007).
The sub-adult
and adult males in this study showed a brown spotted pattern.
Nevertheless, the spots on the sub-adult individual are smaller and more
discrete, so the beige base is more dominant. In adults, a blotch on the head
extends to the upper back to the forelimbs, and a blotch on the lower back area
to the tail and hind limbs; therefore, the brown blotch is more dominant. S. wilsoni juvenile female has a plain cream
coloration all over the body, and it seems that pale, plain colors are common
among juveniles of Spilocuscus. The colors of mammal
pelage may not remain constant over their entire lifespan (Caro & Mallarino 2020). Certain pigs and peccaries experience
age-related transformation; for example, they are born with spotted and striped
coats that eventually become consistent as their young become mobile (Caro et
al. 2018).
The immature S. wilsoni photographed by Flannery in 1992 was of
unknown sex and was used as additional paratype information (Helgen & Flannery 2004). We saw similar color patterns
between the photo and S. wilsoni in
this study (Image 3), and we conclude that its morphology belongs to the
sub-adult female individual. We also found differences in the iris color of
juvenile (yellow-green) and sub-adult or adult individuals (blue-green), but
this needs further investigation.
Table 1. Differences in pelage
coloration and iris color in Spilocuscus wilsoni compare to other Spilocuscus.
|
Species |
Pelage color |
Iris color |
|
|
Male |
Female |
||
|
S. wilsoni |
Adult males unspotted are
yellowish white (Helgen 2007). Sub-adult has a more dominant
creamy base color, and the spotted morph is brown. The adult male has a
creamy base color and, more brown blotch that are
dominant in the dorsum and flank (present study). |
Sub-adult female is red-spotted
(ZMB 91706) (Helgen 2007). The juvenile is creamy and
unspotted in the entire body (dorsum, flank, and belly visible). Sub-adults
have a mottled pattern that looks like a mixture of creamy, light brown, and
dark brown colors (present study). |
Blue-green (Helgen
& Flannery 2004). Yellow-green (juvenile) and
blue-green (sub-adult and adult). |
|
S. papuensis |
The complete lower surface and
base color of the dorsum are creamy in apperance,
while the spots covering the back, head, and limbs are dark brown or
blackish. Frequently, the upper surface of the body is washed with a
yellowish hue and commonly exhibits lighter patches of yellow and brownish
speckles, while the tail is typically characterized by gold or red-brown
spotting. The markings are more prominent and blotchy
in males (Helgen 2007). |
The female has the same basic
coloration and spot pattern all over the body as the male. However, the spots
are smaller and more discrete (Helgen 2007). |
Carmine-red (Jentink 1885); as either brown or hazel (Flannery 1994,
1995b; Gray, 1862). |
|
S. maculatus from
northern and western New Guinea |
Mature males typically have a
yellowish-white or orange hue, often featuring substantial orange and white
spots or blotches on their mid-back (Helgen 2007). |
Mature females exhibit colors
ranging from yellowish-white to orange, and some may have yellowish-white
coats with orange markings (Helgen 2007). |
Brown to hazel (Flannery, 1994,
1995a, 1995b; Gray, 1862). |
|
S. rufoniger |
The dorsum of the animal has a
creamy base-color with a superimposed pattern of intensely blackish (ranging
from jet-black to maroon) spots or blotches on the mid-back and hind legs.
The face, head, nape, shoulders, hands, feet, and sometimes the body of the
limbs are covered in a vibrant red-orange or golden fur. The tail can be
either golden or whitish, and the underside of the throat and chin is
typically white fur that often extends as a crescent shape to the cheeks and
ears, creating a striking contrast with the intense color of the head (Helgen 2007). |
The female displays a
coloration identical to that of the male, with the exception of the absence
of black spots on the back. Instead, they have a black saddle marking that
extends over the mid-back and hind limbs (Helgen
2007). |
Brown to hazel (Flannery 1994,
1995a, 1995b; Gray 1862). |
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