New record of Melomys burtoni (Mammalia, Rodentia, Murinae) from Halmahera (North Moluccas, Indonesia): a review of Moluccan Melomys
Author
Fabre, Pierre-Henri
Author
Fitriana, Yuli S.
Author
Semiadi, Gono
Author
Pagès, Marie
Author
Aplin, Ken
Author
Supriatna, Nanang
Author
Helgen, Kristofer M.
text
Mammalia
2018
Warsaw, Poland
2017-06-22
82
3
218
247
http://dx.doi.org/10.1515/mammalia-2016-0137
journal article
254249
10.1515/mammalia-2016-0137
4bd98a0c-6261-4a2e-8fb1-7df5f3241dfd
1864-1547
7837666
Melomys burtoni
from Halmahera
Referred specimens
Ten
specimens of
Melomys burtoni
from
Halmahera
were caught
near the Gemaf and Sagea villages
on
June 2010
and
September 2013
(
MZB 33533
,
33537
,
33539
,
33540
,
33225
,
36359
,
36360
,
36361
,
36362
,
36363
)
,
and
eight specimens
were collected on the
South
(
MZB 33538
) and
North Ake Jira
(
Sake River
;
MZB 33223
,
33224
,
33226
,
33534
,
33536
,
33541
,
33552
) in
January
2010
, 19 km
NW of
Gemaf
and
26 km
NW of Sagea
at the GPS coordinates
00°37′23.8″N
,
127°55′12.6″E
(
South Ake Jira
) and 00°38′49.9″N, 127°56′01.2″E (North Ake Jira);
Ake Sake
(
Sake River
),
5 km
NW of the village of
Gemaf
and
12 km
NW of the village of
Sagea
,
Central Halmahera
,
Halmahera Island
,
Indonesia
, at an altitude of
22 m
, at the GPS coordinates
00°29′14.6″N
,
127°59′15.7″E
(see
Figure 1
).
Their
current altitudinal range is 0 from
250 m
.
Seventeen specimens
are prepared as study skins with accompanying skulls.
Figure 7: Ventral view of study skins representing six
MelomyS
species.
From right to left:
M. fUlgenS
(Seram, BMNH 20.7.26.19),
M. aeroSUS
(Seram, BMNH 20.7.26.21),
M. fratercUlUS
(Seram, BMNH.20.7.26.27),
M. paVeli
(Seram MZB 35961),
M. talaUdiUm
(Pulau Lirung (
=Salibabu), Talaud, BMNH.12.2.9.3),
M. caUrinUS
(Talaud, BMNH.12.2.9.3),
M. obienSiS
(Obi, AM M24392) and
M. bUrtoni
(Halmahera, MZB 33552). Scale bar 0 1 2 cm.
Distribution
Currently,
Melomys burtoni
from Halmahera is known only from the south-central region of the North Moluccan island of Halmahera (
Figure 1
). The species has been collected in lowland forest and forest edge habitats, at elevations between 0 and
250 m
.
We suspect that it may occur more broadly in other regions in the tropical lowland evergreen rain forest (
Whitmore et al. 1984
) in Halmahera, and on neighbouring islands such as Morotai and perhaps Bacan, but little is yet known of its biology and distribution. Previous efforts to survey the rodent fauna of Halmahera and adjacent islands (specimens deposited at AM, AMNH, MZB, USNM), which have documented two native rodent species (
Rattus morotaiensis
and
Halmaheramys bokimekot
) and several non-native rodents (
Rattus exulans
,
R. tanezumi
/
R. rattus
, and
Mus
), have not yet documented
Melomys
in other areas of Halmahera or on Morotai or Bacan. However, rodent collecting efforts in the North
Moluccas
have been very limited to date. Sampling was done at higher elevation in Halmahera by us (
900– 1000 m
, cf. boki mekot locality
Fabre et al. 2013
) and also other mammalogists (
Flannery 1995a
,b), but
M. burtoni
were never collected above
250 m
.
Table 4: Selected external and cranial measurements (mm) and body mass (g) of adult
MelomyS bUrtoni
from Halmahera and Moluccan species of
MelomyS
(
M. obienSiS
) as well as related Australo-Papuan species
(
M. frigicola
,
M. lUtillUS
,
M. bUrtoni
) (means, measurement ranges, and sample sizes provided).
|
Halmahera
burtoni
a
|
Obi, Bisa
obiensis
b
|
Montane New Guinea
frigicola
c
|
Lowland New Guinea
lutillus
d
|
Australia
burtoni
e
|
| HBL |
117 110–141 (13) |
127 123–129 (3) |
118 237–267 (18) |
110 190–246 (23) |
104 174–243 (21) |
| Tail length |
121 110–140 (13) |
162 148–175 (2) |
129 122–136 (18) |
110 85–135 (23) |
111 90–122 (21) |
| Hindfoot length |
24 20–27 (13) |
28 27–29.0 (4) |
26 25–28 (18) |
24 23–26 (23) |
23 21–25 (21) |
| Ear length |
18 15–21 (13) |
15 14–17 (4) |
13 12–14 (18) |
13 11–14 (6) |
13 12–15 (21) |
| GLS |
29.7 29.8–31.3 (13) |
34.1 33.4–34.4 (3) |
28.31 27.19–30.03 (10) |
28.31 27.19–30.03 (10) |
28.4 27.8–29.1 (6) |
| ZB |
15.6 15.1–16.3 (13) |
17.4 17.3–17.6 (3) |
14.26 13.6–15.19 (10) |
14.26 13.6–15.19 (10) |
14.2 13.8–14.21 (6) |
| Mass |
56 37–95 (13) |
71 68–74 (2) |
NA NA |
NA NA |
NA NA |
aMZB
33223-26; 33533-34; 33536-41; 33552.
bBMNH
.3.4.10.1; AU 24391-92.
cAMNH
151204-215; 151217; 151223-227.
dAMNH
105754-760; 105762-771; 105866; 105964-965; 105967-969.
eAMNH
154116; 154120; 154123; 154125-126; 154128-129; 154131; 154133; 154135; 154136-138; 154140-141; 154144; 154149-153.
Table 5: External and cranial measurements (mm) and body mass (g) of adult specimens of additional species of
MelomyS
endemic to the Moluccas (means, measurement ranges, and sample sizes provided).
|
Seram
paveli
a
|
Seram
fraterculus
b
|
Seram
aerosus
c
|
Seram
fulgens
d
|
Talaud
caurinus
e
|
Talauds
talaudium
f
|
| HBL |
124.5 123–126 (2) |
115 115–115 (2) |
153 150–160 (5) |
150 150–150 (2) |
176 176 (1) |
174 173–174 (2) |
| Tail length |
133 128–138 (2) |
154 153–155 (2) |
132 125–138 (8) |
203 200–205 (2) |
137 136–137 (2) |
171 150–183 (3) |
| Hindfoot length |
24 22.4–26.2 (2) |
26 26–26 (2) |
33 31–34 (8) |
34 34–34 (2) |
30 30–30 (2) |
NA NA |
| Ear length |
15 14.6–15.4 (2) |
17.5 17–18 (2) |
17.4 16–18 (8) |
18 17–19 (2) |
15 15 (1) |
14.7 13–16 (3) |
| GLS |
33.6 33.6 (1) |
32.4 31.7–33.0 (2) |
36.6 35.0–37.4 (7) |
39.3 39.3–39.4 (2) |
38.6 38.6 (1) |
38.3 36.9–39.7 (6) |
| ZB |
15.0 14.7–15.3 (2) |
16.1 15.9–16.4 (2) |
18.6 18.0–19.8 (8) |
21.1 20.2–22.0 (2) |
20.0 20.0 (1) |
19.6 18.1–20.8 (6) |
| Mass |
55 45–65 (2) |
NA NA |
110 97–123 (2) |
NA NA |
NA NA |
NA NA |
aMZB
35961; AU 31923.
bBMNH
.20.7.26.26-27.
cBMNH
.20.7.26.21-25; BMNH.20.7.26.22.
dBMNH
.20.7.26.19-20.
eBMNH
.21.2.9.2.
fBMNH
.21.2.9.3.
Measurements
See
Tables 4–6
.
Diagnosis
Melomys burtoni
from Halmahera can be distinguished from congeners by the following external characters: (1) relatively small body size, e.g. as compared to
M. aerosus
and
M. fulgens
of Seram (
Helgen 2003
) (
Tate 1951
, Menzies 1996, see also
Figures 6
and
7
;
Tables 5
and
6
); (2) head-body length is nearly equal to the tail length (103 % of the body length, but see also
Figures 6
and
7
) compared to the long-tailed
M. obiensis
(127 % of the body length); (3) dorsal fur dark brown or red-brown with dark gray bases; (4) ventral fur pure white along mid-ventral region of underparts and grayish on the sides; (5) dorsal surfaces of the forefeet and hindfeet pale brown with scattered rufous hairs; (6) tail usually dark above and below (some specimens have a paler underside), with three hairs per tail scale; (7) brown ears relatively long and large.
Table 6: Cranial and dental measurements (in mm) of
MelomyS bUrtoni
(Halmahera)
.
|
M. burtoni
(Halmahera)
a
|
|
Male (n
=
6)
|
Female (n
= 6)
|
| Mean ± SD |
Range |
Mean ± SD |
Range |
| GLS |
32.78 ± 2.01 |
(30.56/34.6) |
29.99 ± 0.59 |
(28.84/30.90) |
| IB |
4.88 ± 0.02 |
(4.69/5.2) |
4.815 ± 0.03 |
(4.51/4.97) |
| ZB |
16.37 ± 0.51 |
(14.96/17.65) |
14.97 ± 0.2 |
(14.57/15.84) |
| LR |
9.42 ± 0.06 |
(9.14/9.7) |
8.68 ± 0.11 |
(8.02/8.93) |
| BR |
6.01 ± 0.09 |
(5.40/6.94) |
5.48 ± 0.06 |
(5.22/5.92) |
| BBC |
13.35 ± 0.04 |
(12.98/13.71) |
13.00 ± 0.11 |
(12.62/13.39) |
| HBC |
9.66 ± 0.01 |
(9.51/9.78) |
9.60 ± 0.02 |
(9.45/9.78) |
| BZP |
4.54 ± 0.2 |
(3.83/5.49) |
3.92 ± 0.08 |
(3.56/4.34) |
| LD |
8.93 ± 0.39 |
(7.88/9.7) |
7.93 ± 0.07 |
(7.64/8.34) |
| PPL |
11.61 ± 0.28 |
(10.83/12.58) |
10.08 ± 0.36 |
(9.09/10.76) |
| LBP |
6.09 ± 0.04 |
(5.78/6.56) |
5.89 ± 0.04 |
(5.75/6.14) |
| BBPM1 |
2.75 ± 0.06 |
(2.38/3.25) |
2.49 ± 0.02 |
(2.36/2.78) |
| BBPM3 |
4.25 ± 0.02 |
(4.03/4.58) |
4.02 ± 0 |
(3.94/4.08) |
| LIF |
5.82 ± 0.01 |
(5.53/6.55) |
5.35 ± 0.07 |
(5.12/5.85) |
| BIF |
1.92 ± 0.02 |
(1.77/2.10) |
1.80 ± 0.02 |
(1.68/2.01) |
| LB |
4.53 ± 0.04 |
(4.33/4.83) |
4.50 ± 0.05 |
(4.08/4.67) |
| CLM13 |
6.03 ± 0.03 |
(5.84/6.25) |
5.84 ± 0.05 |
(5.65/6.15) |
| clm13 |
5.79 ± 0.10 |
(5.64/6.03) |
5.72 ± 0.01 |
(5.58/5.90) |
| BM1 |
1.83 ± 0.10 |
(1.74/1.98) |
1.77 ± 0.10 |
(1.68/1.81) |
| bm1 |
1.68 ± 0.10 |
(1.61/1.73) |
1.61 ± 0.10 |
(1.52/1.71) |
| bm2 |
1.92 ± 0.10 |
(1.89/1.97) |
1.90 ± 0.10 |
(1.82/1.93) |
| bm3 |
1.48 ± 0.10 |
(1.46/1.51) |
1.43 ± 0.10 |
(1.39/1.46) |
aMZB
33224-26; 33533-34; 33536-41; 33552.
Craniodental features diagnostic in combination include (1) a long rostrum, topped by broad nasals and slightly convex at the premaxillary tips (
Figures 5
,
8
and
9
); (2) a narrow interorbital region with concave borders (
Figure 8
); (3) large palatine foramina (
Figure 10
), (4) long incisive foramina that extend posteriorly to the start of the molar rows (
Figures 4
,
5
and
10
), (5) relatively longer incisive foramina and shorter tympanic bullae compared with all other species sampled here (
Figures 4
,
5
and
10
). Following
Menzies (1996)
,
Melomys burtoni
from Halmahera belongs within the “
cervinipes
division” and more specifically is a member of the
M. burtoni
species group that includes
M. burtoni
of
Australia
,
M. lutillus
and
M. frigicola
of New
Guinea
, and four insular taxa distributed both west and east of New
Guinea
(
M. bannisteri
,
M. cooperae
,
M. howi
,
M. paveli
). Six species (
M. aerosus
,
M. caurinus
,
M. fulgens
,
M. obiensis
,
M. fraterculus
,
M. talaudium
) from the Moluccan region should not be included in this group due to lack of data as well as their relative morphological divergence.
Description
Melomys burtoni
from Halmahera (
Figures 6
,
7
, and 11) is relatively small in body size (head-body length
110–141 mm
) with short, dense, and soft pelage. Dorsal fur ranges from dark-brown to red-brown; the hairs are bicolored, uniformly gray to blackish at the bases (the proximal 1/4 of the length) and brightly rufous distally. Dorsal guard hairs are soft, short, and pliable, project up to
7 mm
beyond the overfur, and are glistening black for most of their length with some reddish tips. The ventral coat is pure white the length of the midventral region and grayish towards the flanks. We detect major chromatic differences between the pelage of an old adult (n = 1), and other adults (n = 15). The old individual MZB 53533 has an overall darker coat and large body size, but is molecularly identical to all other
M. burtoni
specimens from Halmahera. The studied juvenile (n = 1) display a finer and duller colour tone and a more greyish fur compared to the adults.
The snout of
Melomys burtoni
from Halmahera is reddish-brown to yellowish above, and white on the sides and underside. The rhinarium and lips are unpigmented. The eyes are small (diameter about
5 mm
). Vibrissae are dark gray. Mystacial and superciliary vibrissae are moderately long, extending slightly beyond the ears. The pinnae are relatively small and brown, with a sparse covering of reddish brown hairs on both the inner and outer surfaces.
The tail is nearly equal in length to the combined head and body length (only exceeding HBL in the specimen MZB 33533) (
Tables 4
and
6
). The tail is dark brown to blackish on the entire surface, except for the proximal portion (
10–25 mm
), which is unpigmented in some specimens (MZB 33533, 33552). Tail scales are smooth and less raised compared to those in species of the
M. rufescens
Division (
Menzies 1996
), and moderately large (14–15 rows/cm). There are three hairs per tail scale (each
1–2 mm
long), which is characteristic of the
M. cervinipes
Division, as described by
Menzies (1996)
. Tail hairs are dark brown.
Figure 8: Dorsal view of crania of various
MelomyS
species.
Top to bottom:
M. bUrtoni
(Halmahera, MZB 33552 young adult and MZB 33533 old adult),
M. obienSiS
(Obi, AM M24392),
M. bUrtoni
(Australia, BMNH 61.360),
M. lUtillUS
(Papua New Guinea, BMNH 47.1186),
M. talaUdiUm
(Talaud, BMNH 12.2.9.3),
M. caUrinUS
(Talaud, BMNH 12.2.9.3),
M. fratercUlUS
(Seram, BMNH 20.7.26.27),
M aeroSUS
(Seram, BMNH 20.7.26.21),
M. fUlgenS
(Seram, BMNH 20.7.26.19),
M. paVeli
(Seram MZB 35961). Scale bar 0 1 cm.
Dorsal surfaces of the forefeet and hindfeet are pale brown or unpigmented (
Figures 6
) and sparsely covered with short reddish or brownish hairs on top of the metapodials and laterally on the digits. At the base of each claw, long white hairs form ungual tufts. The pollex is very short and bears a flat nail. The other front digits are longer and broader with curved, sharp, white claws. Each palmar surface is hairless, unpigmented, and displays three interdigital pads and two large metacarpal pads. The hindfeet of
Melomys burtoni
from Halmahera are shorter than those of
M. obiensis
and those of
M. frigicola
(
Tables 4
and
5
). Digits are elongated and broad, and each bears a pale claw that is short, sharp, and recurved. The hallux extends past the middle part of the medial digits. The 5th digit is slightly shorter than the medial digits and has a large associated interdigital pad. The plantar surface is naked and unpigmented, with four large interdigital pads, an elongate thenar pad, and a very small hypothenar pad.
Figure 9: Lateral view of crania for various
MelomyS
species.
Top to bottom:
M. bUrtoni
(Halmahera, MZB 33552 young adult and MZB 33533 old adult),
M. obienSiS
(Obi, AM M24392),
M. bUrtoni
(Australia, BMNH 61.360),
M. lUtillUS
(Papua New Guinea, BMNH 47.1186),
M. talaUdiUm
(Talaud, BMNH 12.2.9.3),
M. caUrinUS
(Talaud, BMNH 12.2.9.3),
M. fratercUlUS
(Seram, BMNH 20.7.26.27),
M aeroSUS
(Seram, BMNH 20.7.26.21),
M. fUlgenS
(Seram, BMNH 20.7.26.19),
M. paVeli
(Seram MZB 35961). Scale bar 0 1 cm.
Figure 10: Ventral view of crania for various
MelomyS
species.
Top to bottom:
M. bUrtoni
(Halmahera, MZB 33552 young adult and MZB 33533 old adult),
M. obienSiS
(Obi, AM M24392),
M. bUrtoni
(Australia, BMNH 61.360),
M. lUtillUS
(Papua New Guinea, BMNH 47.1186),
M. talaUdiUm
(Talaud, BMNH 12.2.9.3),
M. caUrinUS
(Talaud, BMNH 12.2.9.3),
M. fratercUlUS
(Seram, BMNH 20.7.26.27),
M aeroSUS
(Seram, BMNH 20.7.26.21),
M. fUlgenS
(Seram, BMNH 20.7.26.19),
M. paVeli
(Seram MZB 35961). Scale bar 0 1 cm.
Figure 11: (Left) Skulls of
M. bUrtoni
(Halmahera, MZB 33552).
(Right)
M. bUrtoni
(Halmahera, MZB 33533), shown in dorsal (top), ventral (2nd row), and left lateral (3rd row) views of crania, lateral views of left mandible (4th row), and medial views of right dentary (bottom).
As in all
Melomys
species
, it has only two pairs of inguinal teats (0 + 2 = 4).
The skull of
Melomys burtoni
from Halmahera (
Figure 11
) is smaller than most Moluccan species of
Melomys
and similar to
M. burtoni
and allies in most dimensions (
Figures 4
,
8–10
). In dorsal view, the rostrum is narrow and short (
Figure 11
). The interorbital region is moderately narrow and defined by concave borders. The postorbital region is elongate and the inflated braincase has a rounded outline. The temporal ridges that extend from the supraorbital region to the dorsolateral surfaces of the braincase are slightly developed. Robust zygomatic arches bow out from rostrum and braincase.
In lateral view (
Figures 9
and
11
), the dorsal profile of the skull is broadly convex from the slightly depressed nasal tips to the top of the frontals, straight over the frontals and parietals to the apex of the domed braincase, and sloping abruptly downward over the length of the interparietal. Nasal bones are short with sloping sides that give an angular shape to the tip of the rostrum. The posterior portion of the nasals are flat with nearly no concavity at the junction with the proximal end of the frontal. The zygomatic plate is narrower and the zygomatic notch shallower than in other Moluccan
Melomys
. The dorsal root and anterior portion of the zygomatic arch are slightly broadened. The squamosal root of the arch is positioned at the medial portion of the braincase. A subsquamosal fenestra is not present. Each auditory bulla is small (
Figures 4
,
5
,
10
, and 11) and separated from the squamosal by a small postglenoid vacuity and from the alisphenoid by a narrow middle lacerate foramen. The lambdoid crest is poorly developed.
The ventral view of the skull (
Figures 10
and
11
) shows long incisive foramina (
Figures 4
and
5
) that project posteriorly beyond the anterior margins of the first molars. The palate is narrow (BPPM1 and BPPM3) and short (LBP). Each palatine foramen is large, positioned between the anterior and posterior roots of the M2, and opens anteriorly into a well-defined palatal sulcus that runs forward to the posterolateral margin of the incisive foramina. The mesopterygoid fossa is moderately broad. The lateral pterygoid fossae are shallow and contain large sphenopterygoid vacuities. The skull exhibits bony landmarks consistent with the primitive pattern of cephalic arterial circulation found in most murine rodents (
Musser and Heaney 1992
), as in other
Melomys
(
Menzies 1996
)
.
The upper and lower molars of
Melomys burtoni
from Halmahera are brachydont and broader compared to
M. lutillus
from Papua and
M. burtoni
from
Australia
(
Figures 12
and
13
;
Tables 6
and
7
). Each molar overlaps with its neighbour. The first upper and lower molars form nearly half of the entire toothrow, the second about onethird of the row, with the last molar much smaller than the others (
Figures 12
and
13
). The transverse laminae of the upper molars (rows 1 and 2 of M1 and row 2 of M2) display a posteriorly oriented, angular U-shape with a typically acuspidate chevron pattern (characteristic of
Melomys
,
Paramelomys
and
Uromys
). The first row is formed by a medium-sized cusp t1 slightly separated from a wide central cusp t2, which in turn is broadly fused with a smaller cusp t3. The second row is composed of a large backward-directed lingual cusp t4 that is attached to a wide and narrow central cusp t5 and a large labial cusp t6, which is smaller than t4. The third row is formed by a large, angular cusp t8 joined to a cusp t9 that projects straight to the labial side. The second molar consists of two laminae with a medium-sized cusp t1. The first lower molar has an oblong outline and three rows of cusps (
Figure 13
). The anterior 2/3 of the molar is formed by small anterolingual and anterolabial cusps that are slightly separated in unworn teeth from the second cusp row (metaconid, protoconid). The metaconid and protoconid are large, with a triangular shape, and fused in specimens displaying worn teeth (e.g. MZB 33533;
Figure 13
). A large entoconid and hypoconid comprise the third cusp row, behind which is a broad but anteroposteriorly narrow posterior cingulum. The subsquare second lower molar has two cusp rows and a posterior cingulum. The pattern and shape of the lamina are similar in cusp shape and pattern to first lower molar. There is a small anterolabial cusplet on the anterolabial margin of the second lower molar close to the protoconid. The small third lower molar displays a rounded shape and a simple occlusal surface with two laminar cusp rows and a posterior cingulum. The molars of
Melomys burtoni
from Halmahera have multiple roots, which were identified by a µCT scanner. Below each first upper molar, we found one large anterior root, two smaller lingual anchors, one labial root and one large posterior root. Four roots anchor each second molar, there are two anterior roots and two posterior anchor. Three roots anchor each third molar, there are two anterior roots and one posterior anchor. One anterior and posterior roots coupled with smaller labial and lingual anchors attach to each first lower molar. The second lower molars are anchored by two anterior and two posterior roots. The third lower molars are anchored by two anterior and one posterior roots. The alveoli patterns of upper and lower molar roots seen in
Melomys burtoni
from Halmahera are similar to the patterns found for
M. lutillus
from Papua and
M. burtoni
from
Australia
.
Figure 12: Occlusal views of right maxillary upper molar rows.
Left: Specimen of
M. bUrtoni
(Halmahera, MZB 33533), Middle and Right:
M. bUrtoni
(Halmahera, MZB 33552; MZB 33537).
Figure 13: Occlusal views of right lower molar rows.
Left: Specimen of
M. bUrtoni
(Halmahera, MZB 33537), Middle and Right: Specimens of
M. bUrtoni
(Halmahera, MZB 33552; MZB 33533).
Each dentary of
Melomys burtoni
from Halmahera is moderately long and stocky (
Figure 11
), with a short but stout coronoid process, robust condylar process and strong angular process. There is a concave curvature of the posterior margin of the dentary. The capsular process forms a prominent ridge parallel to the coronoid and anterior part of the condylar process. A prominent masseteric crest extends between the ventral margin and the labial part of the dentary just before the mental foramen. The mandibular foramen is located above a narrow ridge that runs caudally from the molar platform to the base of the condylar process.