Journal of Mammalogy, 99(1):187–208, 2018

DOI:10.1093/jmammal/gyx160
Published online December 21, 2017
Version of Record, first published online December 21, 2017, with fixed content and layout in compliance with Art. 8.1.3.2 ICZN.

A new species of Halmaheramys (Rodentia: Muridae) from Bisa

and Obi Islands (North Maluku Province, Indonesia)

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Pierre-Henri Fabre,* Andrew Hart Reeve, Yuli S. Fitriana, Ken P. Aplin, and Kristofer M. Helgen
Institut des Sciences de l’Evolution (ISEM, UMR 5554 CNRS-UM2-IRD), Université Montpellier, Place E. Bataillon - CC 064 -
34095 Montpellier Cedex 5, France (PHF)
Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013, USA (PHF, KPA)
Center for Macroecology Evolution and Climate at the Natural History Museum of Denmark, University of Copenhagen,
Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark (AHR)
Museum Zoologicum Bogoriense, Research Center For Biology, Indonesian Institute of Sciences (LIPI), Jl.Raya Jakarta-Bogor
Km.46, Cibinong 16911, Indonesia (YF)
Wildlife Conservation Society, Goroka, Papua New Guinea (KPA)
School of Biological Sciences, Environment Institute, and Australian Research Council Centre of Excellence for Australian
Biodiversity and Heritage, University of Adelaide, Adelaide, SA 5005, Australia (KMH)
South Australian Museum, Adelaide, SA 5000, Australia (KPA, KMH)
* Correspondent: [email protected]

We describe a new species of murine rodent from a skull collected on Bisa Island and 3 specimens from Obi
Island, North Maluku Province, Indonesia. Molecular and morphological data indicate a close relationship with
Halmaheramys bokimekot (Fabre et al. 2013). The new species is characterized by its combination of large size;
short tail with large scales; spiny, coarse, dark dorsal pelage with long black guard hairs; and a dark gray ventral
pelage that contrasts slightly with the dorsum. The Bisa specimen displays unusual zygomatic arch morphology,
which may be a disease-related deformity, or potentially a sexually dimorphic trait. The new species shares
several external and cranio-mandibular features with its sister species from Halmahera that differ from those of
Rattus species, including a spiny pelt, deep palatine sulci, a high rostrum and relatively flat dorsal profile, short
incisive foramina, short palatal bridge, and molars with simple occlusal patterns. Although certain morphological
characteristics of the new taxon suggest an affinity with the taxonomically diverse and geographically widespread
Rattus, in other respects it clearly fits into the Wallacean clade containing Bunomys, Paruromys, and Taeromys, as
indicated by molecular phylogenetic analyses. Along with the recent discovery of Halmaheramys, recognition of
this new species from Bisa and Obi Islands underscores the north Moluccan region’s high endemism, conservation
importance, and the urgent need for a better inventory of its biodiversity.

Kami mendeskripsikan tikus jenis baru berdasarkan satu spesimen tengkorak yang dikoleksi dari Pulau Bisa
dan 3 spesimen dari Pulau Obi, Propinsi Maluku Utara, Indonesia. Data molekuler dan morfologi menunjukkan
adanya hubungan yang erat dengan Halmaheramys bokimekot (Fabre et al. 2013). Jenis baru ini dicirikan dengan
kombinasi berbagai karakter yaitu ukuran tubuh besar; ekor pendek dengan sisik besar; rambut kasar, berduri,
di bagian dorsal berwarna gelap dengan rambut-rambut penjaga panjang berwarna hitam; dan rambut di bagian
ventral berwarna abu-abu tua, sedikit kontras dengan bagian dorsal. Pada “zygomatic arch” spesimen tengkorak
dari Pulau Bisa terlihat berbeda, hal ini mungkin merupakan kelainan bentuk akibat penyakit atau berpotensi
sebagai ciri seksual dimorfisme. Jenis baru ini memiliki beberapa ciri eksternal dan cranio-mandibular yang mirip
dengan spesies sejenisnya dari Halmahera yang diketahui berbeda dari jenis-jenis Rattus antara lain kulit tertutup
rambut berduri, sulkus palatum dalam, rostrum tinggi dengan profil datar di bagian dorsal, foramen incisifum
pendek, rigi palatum pendek, dan pola oklusi sederhana pada gigi geraham. Meskipun karakteristik morfologi
tertentu dari jenis baru ini menunjukkan kemungkinan afinitas dengan genus Rattus yang secara geografi
jenisnya beragam dan terdistribusi luas, namun berdasarkan hasil analisa filogenetik molekuler, spesies baru ini

© 2017 American Society of Mammalogists, www.mammalogy.org

187
188 JOURNAL OF MAMMALOGY

jelas berada dalam satu klade dengan klaster Wallacean yang terdiri dari Bunomys, Paruromys, dan Taeromys.
Seiring dengan penemuan Halmaheramys baru-baru ini, pengenalan spesies baru dari Kepulauan Bisa dan Obi
menggarisbawahi tingginya endemisitas dan pentingnya konservasi di Maluku Utara, serta urgensi inventarisasi
keanekaragaman hayati yang lebih baik.

Key words: anatomy, biogeography, Moluccas, Murinae, Rattus division, taxonomy, Wallacea

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The Moluccan islands, part of Wallacea, host a highly en- the Margaretamys genus; the Maxomys + Crunomys clade,
demic mammal fauna that remains poorly known (Helgen and potentially the genus Haeromys (Achmadi et al. 2013;
2003; Fabre et al. 2013; Fabre et al. 2017a). Highlighting Rowe et al. 2016). The Moluccan murines, however, have
this is the recent discovery of a new genus of murine rodent mixed Asian and Australo–Papuan origins. For example,
from Halmahera Island (Halmaheramys bokimekot, Fabre molecular phylogenetic studies (Fabre et al. 2013, 2017a)
et al. 2013). Taxonomically, Halmaheramys is part of the illustrate a pattern of murine arrivals on Halmahera both
Rattus division (Musser and Carleton 2005), and belongs to a from the west (H. bokimekot) and from the east (R. moro-
clade comprising taxa from the Sunda Shelf (Sundamys), the taiensis and Melomys burtoni).
Philippines (Bullimus), and Sulawesi (Bunomys, Paruromys, In January 1990, T. Flannery and Boeadi discovered
and Taeromys). The Rattus division was initially defined mor- the badly decomposed carcass of a large, distinctive rat on
phologically by Musser and Carleton (2005), and delineated as the small island of Bisa (North Maluku Province, ­eastern
one of many taxonomic “divisions” among murines. More re- Indonesia; localities illustrated in Fig. 1). They collected
cent authors have tended to use clades identified via molecular the head. Flannery (1995:162) subsequently reported his
phylogenetic comparisons, which we recognize as tribes herein ­observations on the external appearance of the carcass under
(Lecompte et al. 2008; Pagès et al. 2010, 2016; Fabre et al. the epithet “Bisa Rat Rattus sp.”, providing a ­photograph
2013). Until recently, the Australo–Papuan tribe Hydromyini of the cleaned skull, and noting the peculiar anatomy of the
(Lecompte et al. 2008; Pagès et al. 2016) was thought to be the ­zygomatic arches. Local people suggested that the s­pecies
most diverse rodent group in the Moluccas. This interpretation also occurred on the larger neighboring island of Obi
was based largely on a modest mammal collection from Seram (Flannery 1995; T. F. Flannery, The University of Melbourne,
made almost a century ago (Thomas 1920), and material from a Melbourne, Victoria, pers. comm., August 2014) but no further
few other expeditions (Flannery 1995; Kitchener and Maryanto specimens were obtained from either island in the f­ollowing
1995; Helgen 2003). Along with Hydromyini, the tribe Rattini 2 decades. In 2013, we visited Obi Island to collect mam-
is now recognized as an important second component of the mal and bird specimens, and confirmed the presence of the
Moluccan and Australo–Papuan murine fauna (Lecompte et al. distinctive rat on Obi, obtaining 3 female specimens. Here,
2008; Rowe et al. 2011; Fabre et al. 2013). Five independent we re-examine Flannery and Boeadi’s “Bisa Rat,” together
Rattini lineages are currently recognized from Wallacea: with the 3 Obi specimens, within the context of the Moluccan
1) an old endemic lineage H. bokimekot; 2) Rattus elaphinus mammal fauna (Helgen 2003; Aplin and Helgen 2010; Fabre
Sody (1941) from the Sula archipelago, possibly closely re- et al. 2013, 2017a, 2017b). Using anatomy, molecular phylo-
lated to Rattus hoffmanni from Sulawesi (Musser and Holden genetics, and geometric morphometrics, we assess the distinc-
1991); 3) Rattus morotaiensis Kellogg (1945) from the north tiveness, as well as the relationships of this taxon. We find it
Moluccas, closely related to Australo–Papuan Rattus spp.; is more distinctive than hitherto suspected and describe it as a
4) the taxonomically ambiguous Rattus feliceus Thomas (1920) new species of Halmaheramys.
from Seram; and 5) the incertae sedis genus Nesoromys ceram-
icus Thomas (1920) from Seram (Fabre et al. 2013).
Study of these murine lineages is yielding new Materials and Methods
­biogeographical clues about the Wallacean transition zone Taxon sampling.—Specimens of Bullimus, Bunomys,
between Asia and Australo–Papua (Wallace 1860, 1902). Halmaheramys, Paruromys, Sundamys, and Taeromys were
Previous phylogenetic results (Fabre et al. 2013; Rowe obtained for examination from the following institutions: the
et al. 2016) indicated 3 key periods in terms of timing of Australian Museum, Sydney (AM M); American Museum
­colonization: 1) arrival in the Philippines (Phloeomyini) dur- of Natural History, New York (AMNH); Natural History
ing the Late Miocene; 2) dispersal of both the ­Sahul-Philippine Museum, London (BMNH); Australian National Wildlife
Hydromyini and the S ­ ulawesi-Philippine Rattini during the Collection, Canberra (ANWC); Museum Zoologicum
late Miocene; and 3) multiple ­Plio-Pleistocene colonizations Bogoriense, Cibinong (MZB); Nationaal Natuurhistorisch
by the Rattini into the ­Indo-Pacific area (at least 6 events). Museum Naturalis, Leiden (RMNH); National Museum of
Sulawesi’s murine fauna is inferred to be of Asian origin Natural History, Smithsonian Institution, Washington, D.C.
(Rowe et al. 2008, 2016; Fabre et al. 2013; Pagès et al. (USNM); Museum Victoria, Melbourne (NMV); South
2016), as there are no ­representatives in Australo–Papua of Australian Museum, Adelaide (SAM M); and Western
major Sulawesian lineages: the Echiothrix + Melasmothrix Australian Museum, Perth (WAM M). Specimens obtained
clade; the diverse Taeromys + Paruromys + Bunomys clade; during the Obi Expedition (November–December 2013) were
 FABRE ET AL.— A NEW SPECIES OF HALMAHERAMYS 189

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Fig. 1.—(A) Distribution map of endemic species belonging to the Rattus division in the Moluccas. (a) Rattus morotaiensis, (b) Halmaheramys
bokimekot, (c) Rattus elaphinus, (d) Rattus feliceus, (e) Nesoromys ceramicus, (f) Halmaheramys wallacei sp. nov. (B) Type locality of H. bokime-
kot (Boki-mekot, Halmahera, 1), and localities of occurrence for Halmaheramys wallacei sp. nov.: Air Durian, Bisa Island (2), Cabang Sumbali,
Obi Island (3), and Gunung Sere, Obi Island (type locality, 4). Maps were produced using the SRTM open database (http://www.cgiar-csi.org/data/
srtm-90m-digital-elevation-database-v4-1) in the open source QGIS software (http://www.qgis.org/en/site/index.html).

prepared in the field by representatives of Institut des Sciences length of the auditory bulla (LB), crown length of the maxillary
de l’Evolution de Montpellier (ISEM) and MZB. Rodents molar row (CLM1-3), and breadth of first upper molar (BM1).
were captured and handled following guidelines approved by All measurements are expressed in millimeters (mm). Molar
the American Society of Mammalogists (Sikes et al. 2016). cusps and cranial structures are generally named according to
A complete specimen list, with museum abbreviations, catalog the conventions established by Musser in numerous publica-
numbers, and locality information, is in Appendix I. tions (e.g., Musser 1981; Musser and Holden 1991; Musser
The holotype and 1 paratype skull of the new taxon were et al. 2008).
photographed. Images of the holotype were also produced Molecular taxon sampling.—Tissue samples preserved in
using a µCT scanner. Measurements of head + body length 95% ethanol were obtained from MZB, Montpellier University
(HB), tail length (TL), hind foot length (including claws; HF), (UM) and the Centre de Biologie et Gestion des Populations,
ear length from the notch (E), and weight in grams (WT) were Montpellier (CBGP), and Museum National d’Histoire
taken from a field catalog (Table 1). Hair lengths from the pelt Naturelle, Paris (MNHN). DNA was extracted from tissue with
were also measured for the description. These measurements a DNEasy Tissue Kit (QIAGEN), in accordance with the manu-
were taken either with a digital ruler graduated to 1 mm, or with facturer’s instructions. We sequenced the whole cytochrome b
Pesola scales graduated to 1 g. External measurements were (Cytb), breast cancer susceptibility 1 (Brca1), growth hormone
reported only for adult animals (males displaying descended receptor (Ghr), and interphotoreceptor retinoid-binding protein
testes and females with enlarged nipples). Using a dial caliper (Rbp3), according to protocols described elsewhere (Irwin et al.
graduated to 0.01 mm, we took the following cranial and dental 1991; Poux and Douzery 2004; Lecompte et al. 2008; Pagès et
measurements, as described by Musser and Newcomb (1983), al. 2010). Brca1, Ghr, and Rbp3 were obtained in 2 overlapping
for adult and subadult specimens (Table 2): greatest length of fragments. Genes were amplified and sequenced using the fol-
skull (GLS), greatest zygomatic breadth (ZB), least interorbital lowing primers: 1) Cytb (1,242 bp): L14723 (5′ ACC AAT GAC
breadth (IB), length of the rostrum (LR), breadth of the rostrum ATG AAA AAT CAT CGT T 3′) and H15915 (5′ TCT CCA TTT
(BR), breadth of the braincase (BBC), length of the braincase CTG GTT TAC AAG AC 3′); 2) Rbp3 1 (786 bp): I1-Rattus
(HBC), breadth of the zygomatic plate (BZP), length of the dia- (5′ ATT GAG CAG GCT ATG AAG AG 3′) and J2-Rattus
stema (LD), postpalatal length (PPL), length of the bony pal- (5′ TAG GGC TTG CTC YGC AGG 3′) and Rbp3 2 (893 bp):
ate (LBP), breadth of the bony palate at first molar (BBPM1), I2 (5’ ATC CCC TAT GTC ATC TCC TAC YTG 3’) and J1
breadth of the mesopterygoid fossa (BMF); length of the inci- (5′ CGC AGG TCC ATG ATG AGG TGC TCC GTG TCC TG
sive foramen (LIF), breadth across the incisive foramina (BIF), 3′); 3) Ghr1 (~ 690 bp): Ghr EXON10-fw (5′ GGR AAR TTR
190 JOURNAL OF MAMMALOGY

Table 1.—Measurements for lengths of head and body (HB), tail (TL), hind foot (HF), and ear (E), in mm, and weight in grams (WT), in
Halmaheramys wallacei sp. nov., H. bokimekot, Paruromys dominator, and selected species of Bunomys and Taeromys. Mean ± SD, observed
range (in parentheses), and size of sample are provided. Mean values were used to compute tail length (TL)/head–body length (HB). Samples of
Bunomys, Taeromys, and Paruromys contain males and females, and are from Sulawesi. Data listed here and in Table 2 for the Sulawesi genera are
extracted from Musser (The American Museum of Natural History, New York City, New York, pers. comm., June 2014).

Species HB TL HF E WT TL/HB (%)

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Halmaheramys
H. bokimekot ♀ 153.2 ± 12.33 121.6 ± 1.55 28.1 ± 0.48 18.4 ± 1.12 89.3 ± 15.04 71–82
(143–167) 3 (120–123) 3 (27–28) 3 (27–28) 3 (72−99) 3
H. bokimekot ♂ 149.0 ± 2.71 126.0 ± 9.02 29.6 ± 0.49 18.9 ± 0.94 89.7 ± 8.50 78–88
(145.9–151.1) 3 (119.6–132.3) 3 (29.2–30.1) 3 (18.1–19.9) 3 (81–98) 3
H. wallacei ♀ 223.7 ± 18 185.3 ± 7.1 45.5 ± 4.4 20.7 ± 0.5 266.7 ± 30.5 81–87
(205–241) 3 (168–210) 3 (42–50) 3 (20–21) 3 (240–300) 3
Bunomys
B. chrysocomus 161.5 ± 8.23 137.4 ± 10.75 35.9 ± 1.25 23.3 ± 0.96 93.3 ± 15.09 67–91
(133–180) 147 (90–165) 139 (33–39) 147 (21–26) 146 (55–135) 147
B. andrewsi 177.4 ± 11.62 150.1 ± 9.92 40.5 ± 1.33 24.7 ± 1.00 154.6 ± 33.43 82–86
(157–195) 17 (130–161) 15 (38–42) 17 (23–26) 17 (98–222) 17
B. penitus 184.0 ± 10.45 162.5 ± 8.63 41.4 ± 1.30 26.1 ± 0.91 133.3 ± 15.42 76–89
(155–242) 82 (138–185) 76 (38–44) 82 (23–28) 82 (95–170) 76
Taeromys
T. celebensis 224.0 ± 13.83 274.6 ± 16.64 50.1 ± 2.16 26.6 ± 0.73 252.7 ± 36.68 119–138
(201–249) 22 (244–306) 22 (47–56) 22 (25–28) 22 (190–345) 22
T. callitrichus 233.8 ± 8.17 253.2 ± 7.79 52.6 ± 1.14 27.2 ± 0.84 318.6 ± 26.88 110–131
(220–240) 5 (240–260) 5 (51–54) 5 (26–28) 5 (290–363) 5
T. hamatus 197.9 ± 12.03 192.0 ± 11.07 43.6 ± 1.43 24.7 ± 0.48 181.8 ± 24.50 95–101
(180–213) 10 (177–205) 9 (42–46) 10 (24–25) 10 (145–220) 10
Paruromys
P. dominator 249.1 ± 11.62 284.3 ± 14.10 54.3 ± 1.64 29.1 ± 1.22 324.9 ± 48.92 110–135
(225–275) 22 (256–316) 22 (51–60) 22 (27–32) 22 (220–425) 22

GAG GAG GTG AAC ACM ATC TT 3′) and Ghr 8-rev (5′ et al. 2009, 2014; Balete et al. 2012; Fabre et al. 2013; Schenk
TTG GCA TCT GAC TCA CAG AAG TAG G 3′), Ghr2 (~ et al. 2013). Our analysis included additional sequences from
600 bp): Ghr 7-fw (5′ AAG CTG ATC TCT TGT GCC TTG the new taxon, as well as H. bokimekot and Kadarsanomys
ACC AGA A 3′) and Ghr2-rev (5′ GAT TTT GTT CAG TTG sodyi. Sequences were aligned using MAFFT (Katoh et al.
GTC TGT GCT CAC 3′); and 4) Brca1 (~ 2,710 bp): Brca1-fw 2002), and checked with the ED editor of the MUST package
(5′ GRG ACC MGC AGT TTA TTG TTC 3′) and Brca1-rw (Philippe 1993). From these individual alignments, we built a
(5′ GGA AGA ACA CAC CTG GTA G 3′). All amplifications nuclear + mitochondrial supermatrix (219 taxa and 5,742 sites),
were carried out in 25 µl reactions containing about 30 ng of in which 40% of data were missing.
extracted DNA, 100 µM of each dNTP, 0.2 µM of each primer, Molecular phylogeny.—Phylogenetic trees were recon-
1 unit of Taq polymerase (Qiagen), 2.5 µl of 10× buffer, 0.5 structed using both maximum likelihood (ML) and Bayesian
mM of extra MgCl2. Cycling conditions were as follows: 1 inference for the single gene matrices and concatenated
activation step at 94°C for 4 min followed by 40 cycles of dena- datasets independently. We used PartitionFinder 2 (Lanfear
turation at 94°C for 30 s, annealing at primer-specific tempera- 2012) to determine the best-fitting ML model of DNA
tures (Cytb, 50°C; Rbp3 1, 58°C; Rbp3 2, 52°C; Ghr 1, 58°C; sequence evolution as specified by the corrected Akaike
Ghr 2, 53°C; Brca1, 58°C) for 30 s, elongation at 72°C for Information Criterion (AICc). Topology and support values
1–1.5 min depending on the length of the target (1 min per kb), for all nodes were estimated upon each matrix (Cytb, Rbp3,
and a final extension at 72°C for 10 min. PCR products were Ghr, Brca1, and the supermatrix) using ML in RAxML ver-
processed by the sequencing centre Genoscope (Evry, France) sion 8.2 (Stamatakis 2006; Stamatakis et al. 2008). This
using an ABI 3730xl automatic capillary sequencer and the ABI software can implement a partitioned analysis by applying
BigDye Terminator v.3.1 sequencing kit. All sequences were to each partition either 1) a general time reversible (GTR)
analyzed with the CodonCode Aligner software (CodonCode model with rate heterogeneity accounted for by a gamma
Corporation, Dedham, Massachusetts). (Γ) distribution (GTR+Γ); or 2) a GTR+CAT model (gen-
We used the DNA dataset from Pagès et al. (2016) for 1 mito- eral time reversible model with rate heterogeneity accounted
chondrial gene (Cytb), and 3 nuclear genes (Ghr; Rbp3; Brca1). for by a number of discrete rate categories). For the parti-
This dataset (Supplementary Data SD1) contains 219 murine tioned dataset, we used the GTR+MIX option, which repre-
species (following the classification of Musser and Carleton sents a combination of these 2 approaches. The GTR+MIX
2005) from previous studies (Steppan et al. 2005; Jansa et al. option assumes the faster GTR+CAT model for topologi-
2006; Lecompte et al. 2008; Rowe et al. 2008, 2016; Heaney cal tree searches, and the GTR+Γ model when computing
 FABRE ET AL.— A NEW SPECIES OF HALMAHERAMYS 191

Table 2.—Descriptive statistics for cranial and dental measurements To account for the potential differences in DNA substitution
(mm) for 6 specimens of Halmaheramys bokimekot and 4 specimens rates in the combined matrices, Bayesian analyses were per-
of H. wallacei sp. nov. Mean ± 1 SD and observed range (in paren- formed under the CAT + G4 mixture model (Lartillot and Philippe
theses) are listed. Sexes are combined in the samples. Abbreviations: 2004) using Phylobayes 3 (Lartillot et al. 2009). For the super-
BBC, breadth of the braincase; BBPM1, breadth of the bony plate at
matrix, 2 chains were run for 100,000 generations and trees were
first molar; BIF, breadth of the incisive foramen; BM1, breadth of first
sampled every 100 generations subsequent to the first 25,000
upper molar; BMF, breadth of the mesopterygoid fossa; BR, breadth
cycles. Convergence was assumed when the maximum difference

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of the rostrum; BZP, breadth of the zygomatic plate; CLM1–3, crown
length of the maxillary molar row; HBC, height of the braincase; IB, of each bipartition frequency between the 2 chains was < 0.1.
least interorbital breadth; LB, length of auditory bulla; LBP, length of Geometric morphometric procedures.—To explore variabil-
bony palate; LD, length of the diastema; LIF, length of the incisive ity in skull shape, we examined 181 specimens from 25 spe-
foramen; LR, length of the rostrum; ONL, occipitonasal length; PPL, cies from the previously cited museums (see Supplementary
postpalatal length; ZB, greatest zygomatic breadth. Data SD1). Besides the new taxon, these included species of
Bullimus, Bunomys, Halmaheramys, Paruromys, Sundamys,
Variables Halmaheramys
and Taeromys. The palatal (ventral) views of the skulls were
H. bokimekota H. wallaceib H. wallaceic
photographed for geometric morphometric analyses. We
n Halmahera (6) Obi Island (3) Bisa Island (1) carefully checked all skins and skulls and associated meta-
ONL 38.3 ± 0.92 48.2 ± 0.18 48.2 data to confirm identifications and geographic provenances.
(36.9–39.2) (46.8–50.2) The extent of dental wear was used to distinguish adults and
ZB 16.9 ± 0.64 21.7 ± 0.05 22.3 juveniles. Landmark coordinates were taken from the palatal
(16.1–17.9) (21.2–22.2)
IB 6.3 ± 0.28 7.4 ± 0.06 7.3
side of the specimens, and shape was described by 25 land-
(5.9–6.7) (7.0–8.0) marks on the palatal view following the Procrustes proto-
LR 13.5 ± 0.56 18.6 ± 0.2 17.6 col published in Claude (2013) and Camacho-Sanchez et al.
(12.7–14.2) (17.6–21.0) (2017). All Procrustes analyses are described in greater detail
BR 6.4 ± 0.31 8.2 ± 0.03 8.1 in Supplementary Data S2. To visualize patterns of shape var-
(6.1–6.8) (7.9–8.2)
BBC 15.2 ± 0.36 17.6 ± 0.07 16.9
iation observed on the 2 main PC axes, we computed extreme
(14.8–15.7) (17.0–18.4) morphologies along each PC from Procrustes-corrected data. A
HBC 11.7 ± 0.36 12.8 ± 0.08 12.2 univariate linear model on centroid size (analysis of covariance
(11.3–12.3) (12.1–13.6) [ANCOVA]) was employed to test the potential effects of spe-
BZP 3.2 ± 0.22 4.3 ± 0.02 3.9 cies, genus, and sex. A multivariate linear model (multivariate
(2.9–3.5) (4.1–4.5)
LD 9.9 ± 0.42 13.4 ± 0.16 13.3
analysis of variance [MANOVA]) was also applied on the PCs
9.4–10.6) (11.8–15.0) of shape variation using non-zero eigenvalues. The species,
PPL 13.3 ± 0.45 17.9 ± 0.06 16.9 genus, and sex factors, the size variable, as well as the interac-
(12.8–13.9) (17.3–18.6) tions until the third order were taken into account as explana-
LBP 7.1 ± 0.30 9.3 ± 0.05 8.5 tory variables. These ANCOVA (for size) and MANOVA (for
(6.6–7.4) (8.9–9.8)
BBPM1 3.2 ± 0.21 4.5 ± 0.01 4.0
shape) analyses of variance were performed on the different
(3.0–3.5) (4.3–4.5) variances explained by the covariables and factors.
BMF 3.6 ± 0.18 4.8 ± 0.08 4.3
(3.3–3.8) (4.1–5.7)
LIF 6.0 ± 0.15 7.9 ± 0.03 6.9 Results
(5.8–6.1) (7.5–8.1)
BIF 2.3 ± 0.08 3.1 ± 0.01 3.0 Halmaheramys wallacei, new species
(2.2–2.4) (3.1–3.3)
LB 5.3 ± 0.16 6.6 ± 0.02 5.8 Wallace’s large spiny rat, tikus-duri besar Wallace
(5.2–5.6) (6.3–6.8)
CLM1-3 6.6 ± 0.16 8.3 ± 0.02 7.1 Bisa Rat Rattus sp.: Flannery 1995:162.
(6.4–6.8) (8.1–8.4)
BM1 2.0 ± 0.08 2.4 ± 0.01 2.1 Halmaheramys bokimekot: Fabre et al. 2013:418.
(1.9–2.1) (2.3–2.4)
Holotype.—MZB 38226, adult female, from Gunung Sere
a
MZB 33261–266 (i.e., Mount Sere), Obi Island, North Maluku (Maluku Utara)
b
MZB 38225–227 Province, Indonesia, collected on 26 November 2013 by P. H.
c
AM M24389 Fabre et al. The specimen consists of a dried skin and a cleaned
skull. The dentition is fully erupted, the skull sutures are fully
the likelihood value of each topology. All RAxML analyses fused, and the skin bears enlarged nipples.
implemented the default parameters and comprised 10,000
tree pseudoreplicates. Node stability of the partitioned super- Type locality.—The type locality, in southwestern Obi, is situ-
matrix was estimated using 10,000 nonparametric bootstrap ated on Gunung Sere above the villages of Tapaya and Wayaloar.
replicates. Bootstrap values were computed with RAxML The holotype was collected in secondary forest along a ridge at
using a GTR+MIX model. 970 m asl, near a campsite at 1.624°S, 127.709°E, 870 m asl.
192 JOURNAL OF MAMMALOGY

Paratypes.—In addition to the holotype, 1 paratype of Halmaheramys wallacei can be distinguished from other
H. ­wallacei (MZB 38225, adult female) was caught at the type known murine genera by the following combination of ecologi-
locality on 23 November 2013. A second paratype from Obi cal and morphological traits (see also Fabre et al., 2013): 1) ter-
(MZB 38227, adult female) was trapped by P. H. Fabre et al. on restrial habitus; 2) relatively large body size (Table 1); 3) dorsal
8 December 2013 in the north of Obi Island, inland from the vil- pelage covering head and body harsh, thick, rufous brown with
lage of Jikotamo, from Cabang Sumbali, at 1.378°S, 127.659°E, scattered bristly and spiny hairs (Fig. 2); 4) ventral spiny coat
40 m asl. This animal was taken in secondary forest near a river. coarse and dark gray, with slight contrast between upper- and

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underparts; 5) moderately long muzzle, with pale brown ears;
Referred specimen.—One specimen of the new species was 6) tail shorter than combined length of head and body (mean
collected by T. F. Flannery and Boeadi on 16 January 1990 from value of TL/HB is 82%, Table 1), epidermal scales large and
the island of Bisa, immediately adjacent to Obi: AM M24389, square (8−10 scale rings/cm near base of tail), their annuli
adult skull, sex undetermined (cranium and associated dentaries overlapping, and 3 short spiny hairs associated with each scale
with moderately worn molars), from Air Durian (Durian Creek), (Fig. 3); 7) digits and dorsal surfaces of carpal and metacarpal
2 km south of Madu Pob on Bisa Island, North Maluku (Maluku regions pink, palmar surface adorned with the usual number of
Utara) Province, Indonesia. This was the first exemplar reported tubercles in murines (3 interdigitals, a thenar, and a hypothenar),
in the literature (Flannery 1995:162), who correctly regarded hind foot elongate with full complement of plantar tubercles (4
it as a new species. This skull was removed from a badly rot- interdigitals, a thenar, and a hypothenar), front claws moder-
ted carcass discovered along a forest path (Flannery 1995; T. F. ately long and adorned with white eponychial hairs (Fig. 3); 8) 3
Flannery, in litt.). The cranium is missing the left jugal and both pairs of teats, 1 postaxillary and 2 inguinal (0 + 1 + 0 + 2 = 6);
pterygoid and lacrimal bones. Left dentary is missing the incisor. 9) rostrum tubular, stocky, moderately long and narrow with a
The skull from Bisa shows a very distinctive squamosal feature, small lachrymal notch (Figs. 4 and 5); 10) interorbital and post-
which is absent from all Obi specimens. Additional specimens orbital margins bounded by a reduced orbito–temporal ridge;
will be needed to determine the consistency of any morphologi-
cal differences between Obi and Bisa animals, including differ-
ences that might signal taxonomic distinction. However, Cytb
divergence between the 2 populations is low (< 2%, d(K81) <
0.005–0.012% of nucleotide divergence).
Distribution.—The new species is recorded so far from Bisa
and Obi Islands in the north Moluccas (Maluku Utara Province,
Indonesia; Fig. 1). We suspect that H. wallacei is present in for-
est habitats throughout most of Obi and Bisa Islands, as well as
on other small islands closely surrounding Obi.

Etymology.—The new species name honors the natural-

ist Alfred R. Wallace, who spent more than 10 years in the
Malay Archipelago, and passed by Obi in difficult sailing.
The presence of this rat in the Moluccas supports the concept
of the Wallacea zoogeographic pattern for rodents, highlighting
the mixed Asian and Australo-Papuan origins of murines in the
region (see discussion on biogeography).

Vernacular names.—We suggest common names for this

species both in English, “Wallace’s large spiny rat”, and in
Bahasa Indonesia as “tikus-duri besar Wallace.”

Nomenclatural statement.—A life science identifier (LSID)

number was obtained for the new species (Halmaheramys
wallacei):urn:lsid:zoobank.org:pub:8D9D5BA4-288A-
4D81-AA79-AFA735FA3541.

Diagnosis.—Based on molecular analyses, H. wallacei

belongs to the Rattini lineage (molecular tribe sensu Lecompte
et al. 2008; Aplin and Helgen 2010; Fabre et al. 2013), and Fig. 2.—External appearance of the holotype of Halmaheramys wal-
the Rattus division of subfamily Murinae, family Muridae (as lacei sp. nov. (MZB 38226) shortly after capture, in lateral (A), and
delimited by Carleton and Musser 1984; Musser and Carleton ventral (B) views. The long dorsal guard hairs are pictured in (C).
2005). Based on Cytb nucleotide divergence, this species is ≥ Photo credit: Pierre-Henri Fabre, ISEM, Montpellier University,
8% divergent from its sister species H. bokimekot. Montpellier.
 FABRE ET AL.— A NEW SPECIES OF HALMAHERAMYS 193

moderately deep palatine grooves, posterior palatine foramina

at mid-level of M2 with a well-developed sulci containing 3
pairs of posterior palatine foramina (Fig. 7); 21) sphenopalatine
vacuities moderately long and wide; 22) pterygoid plates wide,
with narrow and moderately deep pterygoid fossa, small sphe-
nopterygoid openings; 23) ectotympanic (auditory) bulla small
relative to skull size and basicranial area (seems to be embedded

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between the basisphenoid, the zygomatic, and the basioccipi-
tal); 24) ectotympanic capsule incompletely covering periotic,
posterodorsal wall of carotid canal formed by periotic and not
bullar capsule; 25) large stapedial foramen, no sphenofrontal
foramen or squamosal–alisphenoid groove, indicating a carotid
arterial pattern widespread within Murinae (character state 2 of
Carleton 1980; pattern 2 described by Voss 1988); 26) dentary
short and stocky, thick ramus between incisor and molar row,
high ascending ramus, large coronoid process, condyloid process
with a posteriorly-oriented articulation surface, and end of alveo-
lar capsule forming small labial bulge level with base of coronoid
process; 27) upper and lower incisors with orange enamel and
ungrooved anterior faces, uppers emerging from the rostrum at a
right angle or nearly (orthodont to slightly opisthodont configu-
rations), and each lower incisor stocky with short wear facets;
28) M1 with 5 roots, M2 with 4, and M3 with 3, each m1 with 4,
and m2 and m3 each with 3 (Fig. 8); 29) molars brachydont and
narrow, cusp rows forming simple cuspidate occlusal patterns,
M3 and m3 small relative to others in toothrow; 30) 1st and 2nd
lamina of cusps on M1 arcuate, cusps broadly coalesced within
each lamina, anterior lamina of M2 shaped like 2nd row of M1;
31) no cusp t7 or posterior cingulum on upper molars (a small
cusp t3 is present on M2 and M3 and no other accessory cusps or
ridges could be detected in our sample); 32) anteroconid formed
of large anterolingual and small anterolabial cusps broadly fused
into single reduced lamina oblong in cross-section, anterocentral
cusp absent, anterolabial cusp present on m2 and m3, posterior
labial cusplets present on m1, posterior cingulum elliptical in
Fig. 3.—Photographs of the (A) forefeet, (B) hind feet, and (C) tail cross-section of m1 and m2 (Fig. 8).
scales of Halmaheramys wallacei, taken from MZB 38226 just after
its capture. Photo credit: Pierre-Henri Fabre, ISEM, Montpellier Halmaheramys wallacei and H. bokimekot share vari-
University, Montpellier. ous important characters, including aspects of fur texture
and morphology (including spines), color, tail length pro-
11) zygomatic arches bow outward from sides of braincase, and portion (shorter than head and body), and mammary formula
rostrum with the zygomatic root situated posteriorly near the (1 + 2 = 6). However, the species are easily distinguished from
tympanic bulla area and inserted low on braincase (Figs. 5 and 6); one another. The body mass of H. wallacei is more than twice
12) braincase moderately wide and deep, occiput deep, no that of H. bokimekot (Table 1). The hind feet are proportionally
­cranial flexion; 13) zygomatic plate moderately wide, with a shorter in H. wallacei than in H. bokimekot (Table 1). The ears
prominent anterior spine that forms a conspicuous zygomatic of H. wallacei are smaller in proportion. All complete speci-
notch, its posterior edge not overlapping with the anterior part of mens of H. wallacei lack the white tail tip (Fig. 2) characteristic
M1; 14) squamosal intact, not perforated by a squamoso–mas- of H. bokimekot. Regarding skull morphology, both taxa share a
toid foramen; 15) rostrum high and nearly flat dorsally (espe- narrow tubular rostrum, similar glenoid cavities, similar palatal
cially distinctive in H. wallacei); 16) alisphenoid struts absent, foramina patterns, similar orientation of the condylar process
and both the anterior opening of the alisphenoid canal and the of the jaw, similar parietal and squamosal suture patterns, and
foramen ovale opening posteriorly close to the wall of the tym- lack an alisphenoid strut. Several skull characters distinguish
panic bulla (see Fig. 6); 17) incisive foramina short and wide, H. wallacei from H. bokimekot (Fig. 9 and Table 2): 1) the tem-
their posterior borders not overlapping with anterior alveolar poral ridge is more developed; 2) the zygomatic plate is ante-
margins of 1st upper molars; 18) molar rows slightly divergent rior of M1 rather than adjacent to it; 3) the skull top is nearly
posteriorly; 19) bony palate short, with its posterior margin flat; 4) the squamosal root of the zygomatic arch is closer to
even with the posterior margin of M3; 20) palatal surface with the tympanic bulla; 5) the main post-palatine foramina reaches
194 JOURNAL OF MAMMALOGY

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Fig. 4.—Skulls of Halmaheramys wallacei sp. nov. from Obi Island (A: MZB 38225) and Bisa Island (B: AM M24389), and Halmaheramys
bokimekot from Halmahera Island (C: MZB 38266), shown in dorsal (1st row), palatal (2nd row), left lateral (3rd row) views of crania. Fourth
row: lateral views of left mandibles.

M2; 6) the jugular process is longer; 7) the post-glenoid vacu- The anterior side of the dorsum is more rufous than the pos-
ity is separate from the middle lacerate foramen; 8) the incisive terior part. The fur of the venter and the ventro–lateral side of
foramen does not reach the level of the M1 (except on 1 side the head is shorter, spiny, and gray or white. The underfur hairs
of the Bisa specimen of H. wallacei); and 9) its tympanic bulla are filamentous, unpigmented, and are covered by the spiny
is shorter. Unlike H. bokimekot, H. wallacei has: 1) a cusp t3 overfur. The spines of the ventral overfur are slightly bicolored,
on M2 and M3; 2) a postero–labial cusplet on m1; and 3) an with a white base and pale gray tip. Some long, whitish guard
anterolabial cusplet on m1, m2, and m3 (Fig. 5). hairs are also found on the postero–lateral side of the venter (≤
20 mm long). The transition in color between the dorsum and
Description.—Female adults of H. wallacei are large (240– venter is weakly demarcated. The interramal vibrissae are black
300 g) and rufous brown colored, with a tail shorter than the from the base to the middle part, and unpigmented to the tip.
head-body length (79–87% of HB; Fig. 2, Table 1). The harsh, The submental vibrissae are unpigmented. All other vibrissae
long, and spiny dorsal coat is composed of underfur, overfur, are mostly black, with a short silver tip. The ears are short (E/
and guard hairs (Fig. 3). Underfur hairs are filamentous, unpig- HB = 9–10%); their skin is light brown, and covered with short,
mented, and covered by the spiny overfur and very long guard unpigmented hairs. It is brown on all surfaces in the 3 Obi spec-
hairs. The hairs in the overfur are of 2 types: spiny or harsh. imens. Large, brown overlapping annuli of squarish epidermal
The spiny overfur hairs are enlarged, dark-brown tipped, and up scales (as also reported for the Bisa specimen by Flannery
to 30 mm long, with a creamy or gray color to the shaft below 1995) and brown scale hairs color all surfaces of the tail (Figs.
the tip. The harsh hairs in the overfur are of 2 subtypes. The 2 and 3). Under each scale, 3 spiny hairs emerge, each about
first subtype has a length of 10–25 mm with a gray base, mid- equal to or slightly longer than a single scale; there are 8–9
dle black band, a rufous terminal band, and sometimes a tiny scale rings per cm near the base of the tail (Fig. 3). The front
black terminal tip. The 2nd subtype are long guard hairs (up to and hind feet are short and slender (Figs. 2 and 3). The upper
70 mm on the bushy rump), with a gray base, a middle black parts of the feet are pink to white, with short, silvery hairs. On
band, a long silvery–gray subterminal band, and a short rufous the front feet, a rounded, reduced pollex bears a prominent nail.
terminus. The pigmented bands of the different layers com- The sharp and moderately long claws are pink or unpigmented
bine to render the dorsal coat rufous, and speckled with black. (ivory-colored), and partly covered by silvery ungual tufts. The
 FABRE ET AL.— A NEW SPECIES OF HALMAHERAMYS 195

Relatively small incisive foramina are located on the palatal

midline, behind the incisor alveoli. The zygomatic plate is rel-
atively narrow; its posterior margin aligned with the front of
M1. The bony palate is thin, and appears only slightly thick-
ened along the midline suture; its posterior margin is thickened
and rugose. The posterior margin of the palate is convex anteri-
orly, terminating at the midline level with the rear of the tooth

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rows. The palatine sulci are characteristically broad, and extend
from the anterior palatal foramina to the rear of the molar
rows. Posteriorly, the sulci contain 3 pairs of posterior pala-
tine foramina. The anterior pair is level with the posterior roots
of each M2; the central pair is level with the anterior roots of
each M3; the posterior and smallest pair, not visible in ventral
view, is shielded by the thickened posterior margin of the pal-
ate, level with the rear of M3 (Figs. 5 and 7). The palatine–max-
illary suture passes along the lateral margin of the anterior of
these 3 foramina; the suture extends a short distance forward of
the foramen to meet its opposite at a point level with the front
of M2. This palatal morphology is characteristic of both spe-
cies of Halmaheramys. The infraorbital region of the skull is
broad and flattened, with poorly developed temporal ridges that
terminate at the point of greatest constriction. The zygomatic
arches, forming the lateral borders of the combined orbitotem-
poral fossae, are relatively robust structures. The jugal bone is
particularly robust in each zygomatic arch. The orbital fossa
has the usual murine form (Fig. 4, but see Musser [1981] and
Musser and Newcomb [1983] for further descriptions). The ali-
sphenoid is weakly grooved lateral to the accessory foramen
Fig. 5.—Micro-CT scan of the skull of Halmaheramys wallacei sp. nov. ovale, and lacks a bony strut. The foramen ovale and the ante-
(holotype: MZB 38226) from Gunung Sere (Obi, Indonesia). From top: rior opening of the alisphenoid canal form a deep groove, and
dorsal, palatal, and left lateral, views of crania. Bottom left: lateral view are placed posteriorly to the molar row, close to the tympanic
of left mandible. Bottom right: medial view of left mandible. bulla area. The pterygoid bones are well developed, with a long,
thin hamular process. The pterygoid fossae are relatively exten-
skin color of the ankles of the hind feet is pink. Palmar and sive laterally and posteriorly. The roof of each pterygoid fossa
plantar surfaces are naked and unpigmented. Females have 3 in H. wallacei is complete and rugose back to the level of the
pairs of teats: 1 postaxillary and 2 inguinal. foramen ovale. The mesopterygoid fossa is relatively broad and
The cranium is characterized laterally by a relatively elon- high, and has a U-shaped anterior margin. Large sphenopalatine
gate tubular rostrum; lachrymal capsules that are weakly vacuities penetrate the roof of the fossa; basisphenoid and pre-
inflated; upper incisors that are orthodont in configuration and sphenoid are narrow and sharply ridged between the vacuities.
relatively delicate for a murine of this size; a dorsally bulg- The foramen ovale is laterally hidden by the sphenoid wall (see
ing braincase; relatively small cheekteeth; and small auditory Fig. 6C). Postero–lateral to the foramen ovale, the alisphenoid
bullae (Figs. 4–6). All specimens have a flat dorsal profile, bears a broad groove that marks the course of the infraorbital
increasing only slightly in height from front to back. The inter- ramus of the stapedial artery, running between the middle ear
parietal is D-shaped, convex posteriorly, and relatively long and the posterior end of the alisphenoid canal. The auditory
and broad. The narial lamina of the premaxilla projects high bullae, formed by the ectotympanic bones, are relatively small
above the incisor gyrus, its dorsal edge in long contact with the and flattened; each bulla has a well-developed meatal process,
nasal. Nasal bones are broad anteriorly, and taper evenly to the an elongate and broad bony eustachian tube, and a short ante-
rear; anteriorly, they extend past the incisors to terminate in a rior process directed towards the pterygoid ridge. The middle
broadly rounded arc. A shallow zygomatic notch separates the lacerate foramen, located between the auditory bulla and pos-
rostrum from the dorsal root of each zygomatic plate. Ventrally, terior margin of the alisphenoid, is almost entirely occluded.
the bony palate is slender; the upper molars are proportionally The bony eustachian tube also largely obscures a ventral view
small, and set in widely separated, weakly divergent rows; the of the primary carotid foramen. The pars petrosa of the periotic
anterior palatal foramina are moderately long; both foramina is broadly exposed along the medial side of the bulla. The pos-
terminate well behind the anterior root of the zygomatic arches, terior surface of the auditory bulla fails to contact the knob-
but well forward of M3. The lateral margin of each foramen like postero–medial end of the caudal tympanic process of the
is bowed, and both anterior and posterior ends are rounded. petrosal. The latter structure stands free of the paroccipital
196 JOURNAL OF MAMMALOGY

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Fig. 6.—(A) Half skulls of Halmaheramys wallacei sp. nov. from Bisa Island (left: AM M24389) and Obi Island (right: MZB 38227). Arrows re-
spectively indicate anomalous squamosal (sqa) and normal squamosal (sq). (B) Halmaheramys bokimekot from Halmahera Island (MZB 33266),
with visible foramen ovale (fo). (C) H. wallacei sp. nov. (MZB 38226), with hidden foramen ovale (fo hidden).

Fig. 7.—Palatal views of the cranium in Halmaheramys wallacei sp. nov. (MZB 38227) and Rattus norvegicus (UM 24.4.65.53). Abbreviations:
bs, basioccipital bone; fo, foramen ovale; mlf, middle lacerate foramen; mx, maxillary bone; pa, palatal bone; ppfa, posterior palatine foramen
anterior; ppfc, posterior palatine foramen central; ppfp, posterior palatine foramen posterior; ps, presphenoid; psu, palatine sulci; pt, pterygoid;
spt, sphenopterygoid vacuity; sv, sphenopalatine vacuity; trc, transverse canal.
 FABRE ET AL.— A NEW SPECIES OF HALMAHERAMYS 197

and are directed postero–ventrally. The free-standing portion

of each process is formed entirely from the exoccipital bone;
the mastoid contributes only to the base. The mastoid exposure
of the periotic is extensive, and trapezoidal. The supramastoid
foramen notches the dorsal margin of the mastoid. The mastoid
does not contribute to the principal body of the temporo–mas-
toid crest, which instead runs along the squamoso–exoccipital

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suture as indicated above. However, a knob-like process on the
antero–ventral corner of the mastoid is aligned with and forms
the terminal portion of the temporo–mastoid crest.
The horizontal ramus is relatively shallow below the ­posterior
molars, but deepens anteriorly to support a robust mandibular
symphysis (Figs. 4 and 5). The lower incisor projects forward
at a relatively low angle and is typically short. The anterior
border of the ascending ramus arises at the level of the anterior
lamina of m2; it has a straight anterior margin that forms an
angle of 140° with the plane of the cheekteeth. The coronoid
process is large, recurved and rises well above the level of the
articular condyle. The incisor tubercle is gently rounded and
situated just behind the level of m3; it is continued posteriorly
by a low ridge that runs to the lower end of the articular condyle
and marks the lower limit of insertion of the deep masseteric
muscle. The condylar process is short, such that the articular
condyle does not project far beyond a line drawn between the
tips of the coronoid and angular processes. The angular process
is relatively deep, with a broadly rounded margin; it extends to
just behind the articular condyle. The mandibular foramen is
small, and located near the anterior end of the internal ptery-
goid fossa.
The upper incisors display an orthodont to slightly opistho-
dont orientation. The enamel is ungrooved, contains orange pig-
ment, and extends one third of the way down the buccal surface
of the tooth. The molars are relatively brachyodont, with weakly
inclined laminae; adjacent molars show a moderate degree of
longitudinal overlap. The M1 has 5 roots, 1 positioned anteri-
orly, and 2 on each side of the tooth. The anterior root exceeds
Fig. 8.—Occlusal views of the right maxillary upper and left lower
all others in bulk, and extends only slightly forward of the ante-
molar rows of a paratype and the holotype of Halmaheramys wallacei
sp. nov. (AM M24389 and MZB 38227; crown length of the maxil-
rior margin of the tooth crown. The M1 cusp pattern is simple
lary molar row, CLM1–3, 7.1 mm and 8.4 mm), and the holotype of and follows the general murine pattern (Fig. 8). The tooth is
Halmaheramys bokimekot (MZB 33266; crown length of the maxil- slightly, but conspicuously, wider across the anterior lamina than
lary molar row, CLM1–3, 6.5 mm). the middle lamina. The enamel is weakly punctate. The ante-
rior lamina is broadly arcuate, with poor definition of individual
process and probably represents the point of attachment of a cusps. The central cusp (t2) appears to exceed the labial (t1) or
stylohyal ligament and associated muscles. The tubular process lingual (t3) cusps in bulk (Fig. 8). Cusp t1 is positioned posterior
of the bulla surrounds a large, kidney-shaped external auditory to cusp t3; both cusps are rounded posteriorly, without acces-
meatus. Thickened lateral extensions (“meatal processes”) are sory ridging. The middle lamina is more cuspidate due to the
developed anterior and ventral to the meatus; a V-shaped notch presence on the anterior surface of the lamina of broad grooves
separates these. The posterior lamina of the ectotympanic is between the central cusp (t5) and each of the labial cusp (t6) and
unexpanded. The basioccipital is broad, and bears a distinct but lingual cusp (t4), both of which are positioned slightly behind
subdued anterior midline ridge, which joins a low transverse cusp t5. Cusp t6 is subequal in size to cusp t5, and is rounded in
ridge positioned just forward of the occipital condyles. The lat- occlusal shape (Fig. 8). Cusp t4 is more angular in form, with a
eral margins of the basioccipital are slightly elevated where they hint of a posterior ridge; it lies slightly posterior to cusp t6. The
meet the periotic. The occipital condyles are moderately large. posterior lamina consists of a large, rounded central cusp (t8),
The posterior surface of the cranium is gently bowed, and proj- and a smaller labial cusp (t9), which has the form of a broad
ects well behind the nuchal crest. The paroccipital processes ridge, directed antero–labially (Fig. 8). The 2 cusps are broadly
are relatively short; they stand well behind the auditory bulla united, but defined by a broad groove on the anterior surface of
198 JOURNAL OF MAMMALOGY

the lamina. Cusp t8 is considerably larger than cusp t5. Cusp t9 inflected posterior surface. The labial protoconid and lingual
is smaller than any other primary cusp. A shallow groove on the metaconid are subequal in size; the metaconid is more rounded
antero–lingual surface of cusp t6 marks the position of a weak than the protoconid, which has an angular posteriolabial cor-
enamel ridge that meets the posterior tip of cusp t4. There is no ner. The boundary between the 2 cuspids is clearly marked by a
trace of a posterior cingulum on M1. The occlusal surfaces of deep, but narrow, groove, midway across the posterior surface
the individual laminae on M1 and M2 dip only slightly relative of the lamina. There is no trace of an accessory labial cusplet
to the overall longitudinal plane of the upper molar row (Fig. associated with the anterior lamina. The posterior lamina of

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8). M2 is considerably shorter, and slightly narrower, than the m1 is almost identical in width to the anterior lamina, but it
M1. It is supported by 4 separate roots, 2 on each side of the has a more complex occlusal shape, with a broadly W-shaped
crown. M2 is slightly longer than wide, and subtriangular in out- anterior margin, and a broadly V-shaped posterior margin that
line, tapering posteriorly. The cusp pattern follows the typical lacks a deep groove. The labial and lingual cuspids are sub-
murine pattern, cusps t1 and t3 representing isolated elements equal in occlusal area; both are subrectangular in shape. A shal-
of the anterior lamina, followed by complete middle and poste- low groove on the labial surface of the hypoconid presumably
rior laminae that mirror the construction of M1. Cusp t1 of M2 marks the presence of a posterolabial cusplet that is united with
is a large, tear-drop shaped cusp that lies on a common occlusal the posterior lamina. The posterior cingulum is a broad, len-
plane with cusp t8 of M1; its anterior surface projects slightly ticular structure, positioned centrally at the rear of the tooth.
forward of the anterior surface of cusp t5. Cusp t3 is small and The occlusal surface of the posterior cingulum lies in the same
lies above the occlusal plane of the tooth, closely adpressed to occlusal plane as the anterior lamina of m2. The m2 is slightly
the antero–labial face of t5. The middle lamina on M2 is similar longer than wide, and slightly wider than the m1. Four roots
in structure to that on M1. It differs in the slightly less ante- support the crown, 1 beneath each of the 4 primary cuspids. The
rior position of cusp t4 and the presence of a stronger poste- anterior lamina of m2 has a broadly V-shaped posterior margin
rior ridge on cusp t4. The posterior lamina on M2 is dominated that separates the 2 primary cuspids; the subtriangular proto-
by cusp t8 that is slightly broader than its serial homologue on conid is bulkier than the sub-rectangular metaconid. A small,
M1. Cusp t9 is smaller and less well-defined than on M1, and but elevated anterolabial cuspid is located on the front of the
the anterolingual ridge on t8 is weaker. There is no trace of a protoconid. The posterior lamina is similar in structure to that
posterior cingulum. M3 is broader than long, and considerably of m1, but differs in having a broader U-shaped concavity on
shorter and narrower than the M2. Three roots are present, 2 the posterior surface. The posterolabial cusplet is united with
anteriorly and 1 supporting the rear lamina of the tooth. Cusp t1 the hypoconid. The posterior cingulum is relatively broader,
is smaller and more rounded than the equivalent cusp on M2; it but shorter in antero–posterior length than the equivalent struc-
is closely adpressed against the posterolingual surface of cusp ture on m1. The m3 is substantially shorter and narrower than
t8 of M2. A small cusp t3 is present on both left and right M3; it m2. The crown is lower than either anterior tooth. The anterior
is positioned more labial than the equivalent cusp on M2, but is lamina on m3 consists of subequal protoconid and metaconid,
similarly positioned above the occlusal plane on the teeth. The defined by a broadly V-shaped posterior fold. The anterolabial
middle lamina of M3 is an irregular structure comprised of a cuspid, its boundary marked by a labial groove, is substantially
relatively large central cusp t5, a narrow cusp t4 that extends lin- larger than on m1 or m2. The posterior lamina is a lenticular
gually from t5, and a hook-like posterolabial extension from t5 structure, rounded both anteriorly and posteriorly.
that presumably represents t6. The posterior lamina of M3 con-
sists of a single transversely ovate cusp that is broadly united to Morphological and morphometric geometric comparisons.—
cusp t6 and closely adpressed to, but still distinct from, cusp t4. Principal component analysis was performed on superimposed
The lower molars are moderately small in relation to the coordinates of our landmark dataset (Fig. 9). We plotted the
dentary; relatively brachyodont, with weakly inclined laminae extreme morphologies along the 2 first principal components
(Figs. 5 and 8). The m1 retains the usual murine arrangement (PC; Fig. 9). The projection of individuals on eigenvectors
of cusps (Fig. 8). The pattern of roots below m1 follows the for the full dataset (Fig. 9) shows that Halmaheramys spp. are
pattern observed in Rattus, with 1 large circular root situated poorly distinguished along PC1 and PC2. Positive values along
beneath the anterior cluster of cusps; 2 small circular roots PC1 indicate a large tympanic bulla, short zygomatic plate,
on either side and near the rear of the anterior lamina; and 1 long incisive foramina, and a long, narrow rostrum, that dis-
large, oval-shaped root below the posterior lamina. The central tinguish Bunomys (negative loadings) from both Paruromys
roots lie midway between the anterior and posterior roots. The and Sundamys (positive loadings). On the PC2 axis, Bullimus
anteroconid of m1 consists of 2 rounded cuspids, positioned and Halmaheramys are slightly separated by larger bulla, larger
side by side and separated by an anterior groove; the antero- M1, longer incisor teeth extension, and skull length and width
lingual cuspid is slightly larger in area and projects slightly (Fig. 9). Bullimus, Halmaheramys, and Taeromys share a close
further forward than the anterolabial cuspid. The anteroconid morphospace on both PC1 and PC2. “Species” and “genus”
is firmly adpressed against the anterior lamina, but isolated significantly differed in skull centroid size (P < 0.001), and a
from it by a deep, transverse embrasure. The anterior lamina significant interaction between “sex” and “species” was identi-
of m1 is slightly broader than the anteroconid. It is B-shaped fied, but not for “genus” (P = 0.19; Supplementary Data SD2).
in occlusal outline, with a straight anterior margin and deeply Based on our MANOVA results (Supplementary Data SD2),
 FABRE ET AL.— A NEW SPECIES OF HALMAHERAMYS 199

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Fig. 9.—Principal components of morphological variation of the palatal side of the cranium among Halmaheramys species and Indo-Pacific gen-
era Bullimus, Bunomys, Sundamys Paruromys, and Taeromys. Patterns of shape variation along PC1 and PC2 are illustrated on the left and below
the graphic. Light gray lines and circles correspond to minimal scores, and black lines and circles to maximal values. Symbols are proportional
to centroid skull size and correspond to different genera. Landmark locations on palatal side: 1) premaxillary bone between anterior margin of
upper incisors, 2) posterior margin of the palatal bone, 3) anterior margin of the foramen magnum, 4) posterior margin of the foramen magnum,
5) lateral margin of the right incisor, 6) lateral marginal of the lacrimal notch, 7) anterior margin of the incisive foramina, 8) lateral margin of the
incisive foramina, 9) posterior margin of the incisive foramina, 10) maxillary insertion of the zygomatic root, 11) anterior margin of the first upper
molar, 12) lingual margin of M1 at the level of the second lamina, 13) labial margin of M1 at the level of the second lamina, 14) anterior margin
of the orbit, 15) posterior margin of M1, 16) posterior margin of the posterior palatine foramina, 17) postero–lateral margin of M3, 18) posterior
margin of the temporal fossa, 19) suture between squamosal and sphenoid, 20) junction between bulla tympanica and eustachian tube, 21) lateral
tip of the eustachian tube, 22) junction between basioccipital and basisphenoid, 23) most internal point of the external auditory meatus, 24) con-
tact between bulla tympanica and jugular process, 25) lateral margin of the foramen magnum. Species list with voucher numbers in Appendix 1
and Supplementary Data S2.

“skull shape” significantly varied by “species” (P < 0.001), that of H. wallacei in several features (Figs. 3 and 4) including:
“genus” (P < 0.001), and “size” (P < 0.001), with significant a larger tympanic bulla, wider pterygoid plate, narrower skull,
interactions between “size” and “genus” (P < 0.001), “size” and wider rostrum, and longer incisive foramina; the temporal ridge
“species” (P < 0.01), as well as “sex” and “species” (P < 0.01). is absent; the skull roof can be convex instead of flat (e.g., B.
chrysocomus, B. prolatus); the zygomatic plate is closer to M1,
Comparisons with Bunomys.—Like H. wallacei, Bunomys whereas in H. wallacei, the zygomatic plate has a more anterior
spp. (see Musser 2014) are terrestrial, with tail length ratios position; the zygomatic arch bows close to the molar rows in
ranging from 67% to 102%, and elongate rostra (Table 1; lateral view; the squamosal part of the zygomatic arch is placed
Musser 2014). Compared to H. wallacei, the body size and high upon the tympanic bulla; the carotid canal is embedded
length in Bunomys is smaller; but hind feet and ears are propor- under the ectotympanic; the main post-palatine foramina is
tionally longer. The mammae formula of Bunomys differs from placed at the level of M3; in palatal view, the squamosal part of
Halmaheramys in lacking 1 postaxillary teat (0 + 0 + 0 + 2 = the zygomatic arch does not overlap with the tympanic bulla;
4). The pelage of Bunomys is shorter and softer, and without the eustachian tube is shorter; the post-glenoid vacuity is fused
long guard hairs. Bunomys spp. generally have a more grayish with the middle lacerate foramen; and the spheno–palatine
dorsal coat compared to the dark rufous pelt of H. wallacei. vacuity is absent in B. andrewsi and B. chrysocomus. The cusp
Unlike H. wallacei, the tail scales of Bunomys are small, with t3 on M2 and M3 of Bunomys occurred less frequently than
3 short, soft hairs associated with each scale, and sometime a in our sampling of H. wallacei (t3 on M2 and M3 is present
white tail tip. The skull morphology of Bunomys differs from in all our samples). The position of t1 on M1 is placed more
200 JOURNAL OF MAMMALOGY

posterior relative to cusp t2 and t3, which also differs from Data SD3); partitioning scheme has no impact on the results.
H. ­wallacei. The proportion of different lower molar cusps are H. wallacei belongs to the Rattini, within the Rattus division.
given in Fabre et al. (2013: Table 8) for both B. chrysocomus The Rattus division (Node A) is split into 4 main lineages:
and H bokimekot (but see also Musser 2014 for further details). 1) Srilankamys ohiensis; 2) Berylmys; 3) a clade containing the
Sulawesian Bunomys, Paruromys, and Taeromys, the Moluccan
Comparisons with Taeromys.—Taeromys spp. are medium to Halmaheramys, the Philippine Bullimus, and the Sundaic
large rats from Sulawesi, with both scansorial and terrestrial Sundamys (Node B; bootstrap (BP) = 99, Posterior Probability

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lifestyles (Musser 2014). Taeromys differs from H. ­wallacei (PP) = 1); and 4) a clade containing the Southeast Asian Rattus
in having softer and shorter fur without spines. The tail length (Node C; B; BP = 100, PP = 1), some closely related Philippine
ratio of Taeromys is greater (longer) than that of H. wallacei rats (Limnomys, Tarsomys) and the Javan Kadarsanomys, the
(Table 1); tail surfaces are smooth and glistening, with non- South-Southeast Asian Nesokia + Bandicota (BP = 100, PP = 1),
overlapping rings of short scales and very fine hairs. Several and a group containing the Japanese Diplothrix, the Moluccan
Taeromys spp. have a white-tipped or dorso-ventrally ­bicolored species R. morotaiensis, and the Sahul Rattus (Node D; BP = 99,
tail (with the exceptions of T. arcuatus and T. punicans). PP = 1). Node B displays a polytomy among the Halmaheramys
Mammary formulae vary among species of Taeromys, with some + the Sulawesian clade, Sundamys, and Bullimus. Within the
matching H. ­wallacei (T. callitrichus, T. celebensis, T. ­hamatus, Wallacean clade, we recovered a monophyletic Halmaheramys
T. ­microbullatus, T. taerae) and others matching Bunomys (Node F, BP = 100, PP = 1). Based on the K81 model, Cytb
(T. arcuatus, T. punicans). Despite having a similarly long divergence between H. bokimekot and H. wallacei is > 8%, and
­rostrum, skulls of Taeromys spp. are usually larger, with the zygo- population divergence between Obi and Bisa Islands is < 2%.
matic arch bowing laterally well beyond the braincase ­margins,
a broad rostrum, a larger tympanic bulla, a larger M1, and a Natural history of Obi specimens.—In 2013, the mam-
longer incisive foramen, often invading the margins of M1. The malogical team from MZB (Cibinong, Indonesia) and UM
postorbital ridge is usually more developed than in H. ­wallacei, (Montpellier University, France) trapped the first 3 speci-
but the temporal ridge is less pronounced. Additionally, mens of H. wallacei from Obi Island (Fig. 1). Two specimens
Taeromys skulls differ from those of H. wallacei in that: 1) the were caught on Gunung Sere, a montane area dominated by
squamosal part of the zygomatic arch is inserted high upon the laterite soils (Fig. 11). As on Halmahera and other Moluccan
tympanic bulla; 2) on the palatal side, the squamosal part of Islands, the highland rainforest (1,000–1,600 m asl) can reach
the zygomatic arch is inserted well beyond the level of 20–30 m in height, and is characterized by the angiosperm
the ­tympanic bulla; 3) the eustachian tube is short; 4) the families Fagaceae, Guttiferacea, Lauraceae, and Myrtaceae.
post-glenoid vacuity is connected with the middle lacerate
­ Gymnosperms, Podocarpaceae, tree ferns, Ficus, rattans,
­foramen. Molar cusp patterns of Taeromys spp. are contrasted bamboos, nonwoody climbers, orchids, epiphytes, and bryo-
in Fabre et al. (2013: Table 8). phytes are also present (Sidiyasa and Tantra 1984; Whitmore
Comparisons with Paruromys.—Paruromys dominator, the 1984; Edwards et al. 1990; Flannery 1995; Monk et al. 1997).
sole member of Paruromys, has both arboreal and terrestrial hab- Fieldwork was carried out in secondary forest that had under-
its, and a long hind foot relative to head-body length (Table 1). gone heavy selective logging 10–15 years previous (pers.
It has soft, dense fur, small epidermal tail scales, and a bicol- comm. local people). Leaf litter depth was sometimes in excess
ored tail with the proximal part being blackish brown and the of 30 cm. Several small streams ran through the area of study
distal one-half or two-thirds is white, a pattern similar to those (from which Hydromys chrysogaster was collected). The 2
of some Taeromys spp. Halmaheramys and Paruromys have the H. wallacei specimens (MZB 38225, 38226) were caught along
same mammary formulae (0 + 1 + 0 + 2 = 6). Compared to H. a forested ridge at 970 m asl, using snap-traps placed in run-
wallacei, the skull of P. dominator has a much larger and wider ways under logs, on fallen tree trunks, and among tree roots.
zygomatic plate inserted well in front of M1; its tympanic bulla The closest village is approximately 9 km straight line from
and zygomatic plate are smaller; its palate extends well beyond the trapping site. The 3rd specimen (MZB 38227; Fig. 1) was
M3; the rostrum is wider and shorter, with broad incisors; and the collected at Cabang Sumbali (40 m asl), inland from Jikotamo
incisive foramina is shorter. In P. dominator, the postorbital and (Fig. 11). It was caught in a live trap, in small shrubs at the
temporal ridges are well developed; the interparietal is small; the edge of logged secondary lowland forest, near a large river.
zygomatic arch is laterally inserted well upon the tympanic bulla; This specimen was an adult female with an inactive reproduc-
the palatine foramina is at the M3 level; the squamosal root of tive tract. H. wallacei may be frugivorous or herbivorous: stom-
the zygomatic arch does not overlap with the tympanic bulla; the ach contents (n = 1; MZB 38226) contained remains of small
postglenoid vacuity is fused with the middle lacerate foramen; fruits. Further trapping is needed to better understand its diet.
and the condyle is placed upward on the jaw ramus. Paruromys At the Gunung Sere locality, H. wallacei was trapped in associ-
molar comparisons were presented in Fabre et al. (2013: Table 8). ation with 4 other native Obi murines, H. chrysogaster (Fabre
et al. 2017b), Melomys obiensis, Rattus sp. (an undescribed
Molecular phylogenetics.—Our respective combined and taxon), and Uromys sp. (an undescribed taxon), as well as the
single gene datasets provide congruent topologies for the phy- shrew Crocidura nigripes (Cytb identification by J. Esselstyn;
logenetic position of H. wallacei (Fig. 9 and Supplementary species previously known only from Sulawesi) and the cuscus
 FABRE ET AL.— A NEW SPECIES OF HALMAHERAMYS 201

Phalanger rothschildi. At Cabang Sumbali, H. wallacei was reflect evolutionary relationships; this is made clear by our
trapped in association with H. chrysogaster, C. nigripes, and own results, as well other recent molecular phylogenetic analy-
M. obiensis; 2 commensal murine species, Rattus exulans and ses revealing the polyphyly of groups such as the Pithecheir,
Rattus tanezumi; and P. rothschildi. Dacnomys, Melasmothrix, and Micromys divisions (Jansa
et al. 2006; Rowe et al. 2008; Pagès et al. 2010; Fabre et al.
2013; Schenk et al. 2013; Pagès et al. 2016; Rowe et al. 2016).
Discussion A revised concept of a heavily reconfigured Rattus division—

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The phylogenetic relationships of Halmaheramys wallacei.— a genuine phyletic unit, rather than a simple morphological
Flannery’s (1995) tentative referral of the Bisa specimen of grade—is gradually emerging with support from molecular
H. wallacei, then known only by a skull, to the genus Rattus, systematics (Pagès et al. 2010; Fabre et al. 2013; Pagès et al.
was a reasonable first assessment of its taxonomic affinities. 2016). In our analysis, the Rattus division is supported, and
First, the skull and teeth of H. wallacei do broadly resemble includes all but a few of the genera listed by Musser and Heaney
those of many species currently included in the genus Rattus. (1992). However genera such as Anonymomys, Abditomys,
Second, at the time of Flannery’s 1st assessment, the known Palawanomys, Paulamys, and Tryphomys are not yet included,
native rodent fauna of the north Moluccas was otherwise owing to a lack of fresh tissues in collections. Our analysis,
limited to a single species of Rattus (R. morotaiensis), with as well as other recent studies utilizing both nuclear and mito-
slightly greater generic diversity present in the south Moluccas chondrial genes, support 4 major clusters within the Rattus
(endemic species of Rattus, “Stenomys”, Nesoromys, and division (Steppan et al. 2005; Rowe et al. 2008; Pagès et al.
Melomys). And 3rd, the genus Rattus has traditionally served 2010; Fabre et al. 2013; Thomson et al. in press). These include:
as a “catch-all” genus for relatively unspecialized Asian murine 1) the Berylmys lineage; 2) the monotypic genus Srilankamys
rodents (Ellerman 1941), and despite several decades of inten- (a former member of the Dacnomys division; Musser and
sive taxonomic study by Musser and colleagues, a number of Carleton 2005); 3) the Rattus clade containing Bandicota,
taxa still included within Rattus probably warrant generic sep- Diplothrix, Kadarsonomys, Limnomys, Nesokia, Rattus, and
aration (Musser and Holden 1991; Musser and Carleton 2005). Tarsomys; and 4) a large Indo–Pacific clade containing taxa
Our morphological and molecular analyses reveal that this from the Lesser Sundas (Komodomys, Papagomys), Moluccas
new taxon belongs not to Rattus, but rather to Halmaheramys. (Halmaheramys), Philippines (Bullimus), Greater Sundas
However, our results confirm that Flannery was correct in sus- (Sundamys), and Sulawesi (Bunomys, Taeromys). Certain Indo–
pecting that its affinities lie with the large cluster of taxa that are Pacific murine genera have yet to be included in modern molec-
more or less tightly associated with Rattus—members of what ular analyses: Abditomys, Nesoromys, Eropeplus, Lenomys,
we have hitherto referred to as the “Rattus division” (Musser Palawanomys, and Tryphomys; as well as several incertae sedis
and Carleton 2005). To date, the most explicit discussion of the “Rattus” spp. These new analyses (see also Camacho-Sanchez
Rattus division is found in Musser and Heaney’s (1992) review et al. 2017) invite reassessment of the limits of the Rattus divi-
of evolutionary relationships among the endemic murines of the sion; the Wallacean Bunomys clade (Fig. 10; Node B) is clearly
Philippine Islands. They distinguished the Philippine members well separated from the core Rattus group (Fig. 10), and may
of this group as “Division III (New Endemics).” In Musser and be best considered as a separate higher-level taxonomic entity
Heaney’s (1992:93–94) terms, the New Endemics are a “mor- in the future.
phological grade containing either Rattus or Rattus-like genera Biogeographic and faunistic context of H. wallacei.—The
that are identified as part of the endemic murine fauna” of the discovery of a new north Moluccan species within the Wallacean
Sundaic region, the Philippines, Flores, Timor, Sulawesi, the Bunomys clade (clade B in Fig. 10) fills a gap in our knowl-
Moluccas, New Guinea, and Australia. Although Musser and edge of murine zoogeography, confirming the presence of a 3rd
Heaney (1992:95–97) cite 4 putatively derived cranial features Rattini lineage in the north Moluccas. Along with H. bokime-
that potentially unite the members of this group, they express kot, H. wallacei represents a rat lineage with closely related
uncertainty as to whether these similarities are in fact synapo- representatives in Sulawesi (Bunomys, Paruromys, Taeromys),
morphies. The genera subsequently listed under the banner of the the Philippines (Bullimus), and Sundaland (Sundamys).
“New Endemics” include, aside from Rattus itself, Hooijeromys Discovery of a second Halmaheramys species reveals endemic
(an extinct taxon from Flores), Paulamys, Papagomys, and speciation of the genus in the north Moluccas, probably in the
Komodomys of the Lesser Sundas, Bunomys, Paruromys, early Pliocene (Fabre et al. 2013). This was likely due to a dis-
and Taeromys of Sulawesi, Abditomys, Bullimus, Limnomys, persal event, between Obi + Bisa and the Halmahera Islands.
Tarsomys, and Tryphomys of the oceanic Philippines, and Vicariance is unlikely, as Obi is situated between the Sula
Kadarsanomys, Palawanomys, and Sundamys of the Sunda Shelf and the Molucca part of the Sorong fault, separating it from
islands. As indicated above, Musser and Carleton (2005) include Halmahera and Bacan Islands (Hall et al. 1991; Ali et al. 2001;
a number of other genera with predominantly mainland Asian Watkinson et al. 2011; Hall 2013). The low degree of known
distributions (Bandicota, Berylmys, Diplothrix, Nesokia) in their murid diversity in this region may be symptomatic of undersam-
otherwise similarly founded concept of the Rattus division. pling by mammalogists, rather than lack of murine colonization
We now know that the groupings outlined by Musser and events (Helgen 2003). In view of the large number of islands in
colleagues (see also Watts and Baverstock 1995) do not strictly the Moluccas and the lack of previous biodiversity exploration
202 JOURNAL OF MAMMALOGY

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Fig. 10.—A maximum-likelihood topology for the Rattus division produced from the combined analysis of mitochondrial and nuclear sequences.
Labeled clades are discussed in the text. Numbers at nodes represent maximum-likelihood bootstrap support values > 70%, followed by Bayesian
posterior probabilities from Phylobayes. Rattus division clades are highlighted using the full ML topology on the figure. Colors on the tree indi-
cate geographical occurrences.
 FABRE ET AL.— A NEW SPECIES OF HALMAHERAMYS 203

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Fig. 11.—Field photographs at collection localities for Halmaheramys wallacei sp. nov. (A) View of the mountain Gunung Sere, Obi Island, type
locality of H. wallacei. (B) specific trapping locality of the holotype on Gunung Sere, Obi Island. (C) Specific trapping locality of the paratype
from Cabang Sumbali, Obi Island. (D) Live specimen of H. wallacei sp. nov. (MZB 38227) in the field at Cabang Sumbali.

within the region, new discoveries can be expected if invento- between the periotic and the squamosal; in rodents, this fora-
ries are conducted. The murine fauna of the south Moluccas is men usually transmits a substantial vein—the transverse sinus
also poorly known. Several Seramese taxa such as R. feliceus, that drains the posterior cranial dura into the internal maxil-
N. ceramicus, and R. elaphinus require molecular analysis to lary vein (Greene 1935; Wahlert 1974). The zygomatic process
confirm their taxonomic and biogeographic affinities. of the squamosal is unusually short and robust. Immediately
Halmaheramys wallacei joins 3 other terrestrial mammals so behind this process, the squamosal bears a unique dorso–lat-
far documented from the Obi island group—the cuscus P. roth- erally directed bony flange. This encloses a triangular shaped
schildi Thomas, 1898, known from Obi, Bisa, and Obilatu post-glenoid shelf that terminates at the ventral end of the
islands, the newly recorded C. nigripes known from Obi and squamoso–mastoid suture. On both sides of the braincase, the
Sulawesi, and M. obiensis (Thomas, 1911), known from Obi posterior end of the shelf is perforated by a large foramen that
and Bisa (Flannery 1994, 1995). Unlike H. wallacei, both passes into the endocranial cavity. This foramen presumably
P. rothschildi and M. obiensis are faunal elements with clear carried venous drainage from the temporal muscle to join the
Australo-Papuan, rather than ultimately Asian, origins. intracranial portion of the transverse sinus. In other murines,
Notes on the squamosal morphology of H. wallacei.—The and in the specimens from Obi Island, these homologous veins
anomalous squamosal morphology of the Bisa specimen of drain directly into the internal maxillary vein (Greene 1935),
H. wallacei (Fig. 6) has attracted passing attention (Flannery which receives the transverse sinus after its emergence through
1995); it is very striking and has not been reported for any other the postglenoid foramen; the rearrangement of these vessels
murine. Before the discovery of additional specimens from Obi, in H. wallacei of Bisa Island presumably occurred as a con-
we assumed that this morphology, as noted below, might be a sequence of the modified position of the glenoid fossa and
true anatomical characteristic of this species (Helgen and Aplin occlusion of the postglenoid foramen. On the right side of the
2005); now, we realize that it is probably an unusual individual braincase only, the postglenoid shelf is perforated by a second
feature of the Bisa animal. The glenoid fossa of the Bisa Island large foramen, located just behind the root of the zygomatic
specimen is unusually far posterior and low on the braincase for process; this foramen is also identified as a passage for veins
a murine rodent (Fig. 6); it lies immediately antero–lateral and draining the more anterior portion of the temporal muscle.
only slightly dorsal to the auditory region. The glenoid fossa The asymmetry of the vascular foramina presumably reflects
itself is of typical murine form, being an elongate and narrow their venous nature and the anomalous aspect of the anatomy
groove. The postglenoid foramen is reduced to a narrow slit of this region in H. wallacei. We are unsure of the intraspecific
204 JOURNAL OF MAMMALOGY

variability of this feature, because the sex of the Bisa specimen permit number: 4368/FRP/SM/VIII/2013) and the Ministry
is unknown; no male H. wallacei specimens were collected of Forestry, Republic of Indonesia for providing permits to
from Obi; and our sample size (n = 4) is limited. Based on our carry out fieldwork in the Moluccas. Likewise, we thank the
molecular results, which show a close relationship between the Research Center for Biology, Indonesian Institute of Sciences
Obi and Bisa populations of H. wallacei, we suspect that the (RCB-LIPI) and the Museum Zoologicum Bogoriense for pro-
Bisa specimen has a very unusual skull anomaly that is not a viding staff and support to carry out fieldwork in the Moluccas.
species-wide trait. However, we cannot exclude the possibility This publication is contribution No 2017–231 SUD of the

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that it is a surprisingly developed sexually dimorphic character Institut des Sciences de l’Evolution de Montpellier (UMR
or an unusual trait that may vary between islands. Exposition of 5554 – CNRS-IRD).
this interesting anatomical question awaits further field collect-
ing and documentation of murines from Obi, Bisa, and other Supplementary Data
islands in the North Moluccas.
Supplementary data are available at Journal of Mammalogy
online.
Acknowledgments
Supplementary Data SD1.—Newly sequenced specimens
We thank T. Flannery for helpful discussion and for the oppor- (a) and GenBank accession numbers (b) for sequences used
tunity to study the specimen from Bisa Island, and two anon- for phylogenetic reconstructions. Sequences generated in this
ymous reviewers for discussion and improvements to this study indicated in bold.
manuscript. We are grateful to the following people and insti- Supplementary Data SD2.—Supplementary methods and
tutions for granting access to specimens: S. Ingleby and A. results.
Divljan (AM, Sydney); P. Jenkins, S. Oxford, K. Dixey, and Supplementary Data SD3.—RAxML reconstructions for pro-
R. Portela Miguez (BMNH, London); D. Wilson, L. Gordon, tein-coding genes from Rbp3, Ghr, Brca1, and Cytb.
and D. Lunde (USNM, Washington, D.C.); E. Westwig, N.
Duncan, and R. S. Voss (AMNH, New York); K. C. Rowe,
K. Roberts, and K. E. Rowe (NMV, Melbourne); L. R. Literature Cited
Heaney and D. S. Balete (FMNH, Chicago); A. Achmadi, Achmadi, A. S., J. A. Esselstyn, K. C. Rowe, I. Maryanto, and M.
N. Suptriana and Maharadatun-kamsi (MZB, Cibinong); G. T. Abdullah. 2013. Phylogeny, diversity, and biogeography of
Southeast Asian spiny rats (Maxomys). Journal of Mammalogy
Véron, V. Nicolas, and C. Denys (MNHN, Paris); S. van Der
94:1412–1423.
Mije (RMNH, Leiden), H. Baagøe and M. Andersen (ZMUC,
Ali, J. R., R. Halland, and S. J. Baker. 2001. Palaeomagnetic data
Copenhagen); C. Kemper and D. Stemmer (SAM, Adelaide), from a Mesozoic Philippine Sea plate ophiolite on Obi Island, east-
and K. Travouillon (WAM, Perth). We thank V. Thomson ern Indonesia. Journal of Asian Earth Sciences 19:535–546.
(University of Adelaide) for making available in advance Cytb Aplin, K. P., and K. M. Helgen. 2010. Quaternary murid rodents of
sequence of the Bisa Halmaheramys specimen. We also thank Timor. Part I: New material of Coryphomys buehleri Schaub, 1937,
A. Frost, L. Helgen, Boeadi, E.G. Veatch, and S. Donnellan for and description of a second species of the genus. Bulletin of the
helpful discussion and assistance. We thank R. Lebrun (ISEM, American Museum of Natural History 341:1–80.
Case Postal 64, Place Eugène Bataillon, 34095 Montpellier Balete, D. S., et al. 2012. Archboldomys (Muridae: Murinae)
cedex 5, France) and Q. Martinez (ISEM) for their help in the reconsidered: a new genus and three new species of shrew mice
scanning process for the Halmaheramys wallacei holotype. from Luzon Island, Philippines. American Museum Novitates
3754:1–60.
P-HF acknowledges K. A. Jønsson, J. Kennedy, T. Haryoko,
Camacho-Sanchez, M., J. A. Leonard, Y. S. Fitriana, M.-K. Tilak,
and N. Suptriana for their help, friendship, and good com-
and P.-H. Fabre. 2017. The generic status of Rattus annandalei
pany at camp during 4 fieldtrips. P.-H. Fabre and A. H. Reeve Bonhote, 1903 (Rodentia, Murinae) and its evolutionary implica-
acknowledge the Danish National Research Foundation and a tions. Journal of Mammalogy 98:1340–1355.
National Geographic Research and Exploration Grant (8853- Carleton, M. D. 1980. Phylogenetic relationships in Neotomine–
10) for funding fieldwork in Indonesia. This research received Peromyscine rodents (Muroidea) and a reappraisal of the dichot-
support from the SYNTHESYS Project (http://www.synth- omy within New World Cricetinae. Miscellaneous Publications
esys.info/) which is financed by the European Community Museum of Zoology, University of Michigan 157:1–146.
Research Infrastructure Action under the FP7 Integrating Carleton, M. D., and G. G. Musser. 1984. Chapter 11: Muroid
Activities Program SYNTHESYS ACCESS GB-TAF-2735, rodents. Pp. 289–379 in Orders and families of recent mammals of
GB-TAF-5026, GB-TAF-5737, and GB-TAF-6945 granted the world (S. Anderson and J. K. Jones Jr., eds.). John Wiley and
Sons, New York.
to P.-H. Fabre to the NHM, London. P.-H. Fabre’s research
Claude, J. 2013. Log-shape ratios, Procrustes superimposition,
was funded by a Marie-Curie fellowship (PIOF-GA-2012- elliptic Fourier analysis: three worked examples in R. Hystrix
330582-CANARIP-RAT). Studies of Moluccan mammals by 24:94–102.
K. M. Helgen were supported by funding from the University Edwards, I. D., R. W. Payton, J. Proctor, and S. Riswan. 1990.
of Adelaide, South Australian Museum, Australian-American Altitudinal zonation of the rainforests in Manusela National Park,
Fulbright Commission, U.S. National Science Foundation, Seram, Maluku, Indonesia. Pp. 161–175 in The plant diversity of
and American Society of Mammalogists. We thank the Malesia (P. Baas, K. Kalkman, and R. Geesink, eds.). Proceedings
State Ministry of Research and Technology (RISTEK, of the Flora Malesiana Symposium commemorating Professor
 FABRE ET AL.— A NEW SPECIES OF HALMAHERAMYS 205

Dr. C. G. G. J. van Steenis. Kluwer Academic Publishers, Leiden, Eastern Indonesia. Records of the Western Australian Museum
Netherlands. 18:113–199.
Ellerman, J. R. 1941. The families and genera of living rodents, with Lanfear, R., B. Calcott, S. Y. W. Ho, and S. Guindon. 2012.
a list of named forms (1758–1936). Pp. 1–690 in Volume II. Family PartitionFinder: combined selection of partitioning schemes and
Muridae (R. W. Hayman and G. W. C. Holt, eds.). British Museum substitution models for phylogenetic analyses. Molecular Biology
(Natural History), [Mammals], London, United Kingdom. and Evolution 29:1695–1701.
Fabre, P.-H., et al. 2013. A new genus of rodent from Wallacea Lartillot, N., and H. Philippe. 2004. A Bayesian mixture model for

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/187/4767949 by Det Kongelige Bibliotek user on 24 January 2019

(Rodentia: Muridae: Murinae: Rattini) and its implication for across-site heterogeneities in the amino-acid replacement process.
biogeography and Indo–Pacific Rattini systematics. Zoological Molecular Biology and Evolution 21:1095–1109.
Journal of the Linnean Society 169:408–447. Lartillot, N., T. Lepage, and S. Blanquart. 2009. Phylobayes 3: a
Fabre, P.-H., et al. 2017a. New record of Melomys burtoni Bayesian software package for phylogenetic reconstruction and
(Mammalia, Rodentia, Murinae) from Halmahera (North molecular dating. Bioinformatics 25:2286–2288.
Moluccas, Indonesia): a review of Moluccan Melomys. Mammalia. Lecompte, E., C. Denys, K. P. Aplin, F. M. Catzeflis, M. Chades,
doi:10.1515/mammalia-2016-0137. and P. Chevret. 2008. Phylogeny and biogeography of African
Fabre, P.-H., A. Herrel, Y. S. Fitriana, L. Meslin, and L. Hautier. Murinae based on mitochondrial and nuclear gene sequences, with
2017b. Masticatory muscle architecture in a water-rat from a new tribal classification of the subfamily. BMC Evolutionary
Australasia (Murinae, Hydromys) and its implication for the evo- Biology 8:199.
lution of carnivory in rodents. Journal of Anatomy 231:380–397. Monk, K. A., Y. De Fretes, and G. Reksodiharjo-Lilley (eds.). 1997.
Flannery, T. F. 1994. Possums of the world: a monograph of the The ecology of Nusa Tenggara and Maluku. The Ecology of
Phalangeroidea. GEO Productions, Chatswood, New South Wales, Indonesia Series Volume V. Periplus Editions, Hong Kong.
Australia. Musser, G. G. 1981. Results of the Archbold Expeditions. No. 105. Notes
Flannery, T. F. 1995. Mammals of the south-west Pacific & Moluccan on systematics of Indo-Malayan murid rodents, and descriptions of
Islands. Reed Books, Chatswood, New South Wales, Australia. new genera and species from Ceylon, Sulawesi, and the Philippines.
Greene, E. C. 1935. Anatomy of the rat. Transactions of the American Bulletin of American Museum of Natural History 168:229–334.
Philosophical Society, New Series 27:1–30. Musser, G. G. 2014. A systematic review of Sulawesi Bunomys
Hall, R., G. Nichols, P. Ballantyne, T. Charlton, and J. R. Ali. (Muridae, Murinae) with the description of two new species.
1991. The character and significance of basement rocks of the Bulletin of the American Museum of Natural History 392:1–313.
southern Molucca Sea region. Journal of Southeast Asian Earth Musser, G. G., and M. D. Carleton. 2005. Superfamily Muroidea. Pp.
Sciences 6:249–258. 894–1531 in Mammal species of the world: a taxonomic and geo-
Hall, R. 2013. The palaeogeography of Sundaland and Wallacea graphic reference (D. E. Wilson and D. A. Reeder, eds.). 3rd ed. Johns
since the Late Jurassic. Journal of Limnology 72:1–17. Hopkins University Press, Baltimore, Maryland, United States.
Heaney, L. R., D. S. Balete, E. A. Rickart, M. J. Veluz, and S. Musser, G. G., and L. R. Heaney. 1992. Philippine rodents: defini-
A. Jansa. 2009. A new genus and species of small ‘tree-mouse’ tions of Tarsomys and Limnomys plus a preliminary assessment of
(Rodentia, Muridae) related to the Philippine giant cloud phylogenetic patterns among native Philippine murines (Murinae,
rats. Bulletin of the American Museum of Natural History Muridae). Bulletin of the American Museum of Natural History
331:205–229. 211:1–138.
Heaney, L. R., D. S. Balete, E. A. Rickart, M. J. Veluz, and S. Musser, G. G., K. M. Helgen, and D. P. Lunde. 2008. Systematic
A. Jansa. 2014. Three new species of Musseromys (Muridae, review of New Guinea Leptomys (Muridae, Murinae) with descrip-
Rodentia), the endemic Philippine tree mouse from Luzon Island. tions of two new species. American Museum Novitates 3624:1–60.
American Museum Novitates 3802:1–28. Musser, G. G., and M. E. Holden. 1991. Sulawesi rodents (Muridae,
Helgen, K. M. 2003. A review of the rodent fauna of Seram, Murinae) morphological and geographical boundaries of species in
Moluccas, with the description of a new subspecies of mosaic- the Rattus hoffmanni group and a new species from Pulau Peleng.
tailed rat, Melomys rufescens paveli. Journal of Zoology (London) Bulletin of the American Museum of Natural History 206:322–413.
261:165–172. Musser, G. G., and C. Newcomb. 1983. Malaysian murids and the
Helgen, K. M., and K. P. Aplin. 2005. Diversification of the Rattus giant rat of Sumatra. Bulletin of the American Museum of Natural
group in a depauperate context—the eastern Indonesian archi- History 174:327–598.
pelago. Abstract and presentation, International Mammalogical Pagès, M., et al. 2010. Revisiting the taxonomy of the Rattini tribe:
Congress, Sapporo, Japan. a phylogeny based delimitation of species boundaries. BMC
Irwin, D. M., T. D. Kocher, and A. C. Wilson. 1991. Evolution of the Evolutionary Biology 10:184.
cytochrome b gene of mammals. Journal of Molecular Evolution Pagès, M., et al. 2016. Molecular phylogeny of South-East Asian
32:128–144. arboreal murine rodents. Zoologica Scripta 45:349–364.
Jansa, S. A., F. K. Barker, and L. R. Heaney. 2006. The pattern Philippe, H. 1993. MUST: A computer package of management utili-
and timing of diversification of Philippine endemic rodents: evi- ties for sequences and trees. Nucleic Acids Research 21:5264–5272.
dence from mitochondrial and nuclear gene sequences. Systematic Poux, C., and E. J. P. Douzery. 2004. Primate phylogeny, evolution-
Biology 55:73–88. ary rate variations, and divergence times: a contribution from the
Katoh, K., K. Misawa, K. Kuma, and T. Miyata. 2002. MAFFT: a nuclear gene Rbp3. American Journal of Physical Anthropology
novel method for rapid multiple sequence alignment based on fast 124:1–16.
Fourier transform. Nucleic Acids Research 30:3059–3066. Rowe, K. C., M. L. Reno, D. M. Richmond, R. M. Adkins, and S.
Kellogg, R. 1945. Two rats from Morotai island. Proceedings of the J. Steppan. 2008. Pliocene colonization and adaptive radiations
Biological Society of Washington 58:65–68. in Australia and New Guinea (Sahul): Multilocus systemat-
Kitchener, D. J., and I. Maryanto. 1995. A new species of Melomys ics of the old endemic rodents (Muroidea: Murinae). Molecular
(Rodentia, Muridae) from Yamdena Island, Tanimbar group, Phylogenetics and Evolution 47:84–101.
206 JOURNAL OF MAMMALOGY

Rowe, K. C., P. R. Baverstock, K. P. Aplin, and C. C. Moritz. 2011. Appendix I

Recent and rapid speciation with limited morphological disparity External measurements and landmarks derived from the follow-
in the genus Rattus. Systematic Biology 60:188–203.
ing specimens of Bullimus, Bunomys, Paruromys, Sundamys,
Rowe, K. C., A. S. Achmadi, and J. A. Esselstyn. 2016. Repeated evolution
of carnivory among Indo-Australian rodents. Evolution 70:653–665.
and Taeromys were used for the skull geometric morphometric
Schenk, J. J., K. C. Rowe, and S. J. Steppan. 2013. Ecological oppor- analyses.
tunity and incumbency in the diversification of repeated con-
HALMAHERAMYS

Downloaded from https://academic.oup.com/jmammal/article-abstract/99/1/187/4767949 by Det Kongelige Bibliotek user on 24 January 2019

tinental colonizations by muroid rodents. Systematic Biology
62:837–864. Halmaheramys bokimekot
Sidiyasa, K., and I. G. M. Tantra. 1984. Analisis flora pohon hutan Halmahera Island, Boki Mekot (Latitude: 0.6118°S,
dataran rendah Wae Mual, Taman Nasional, Seram-Maluku. Longitude: 128.047°E, altitude 900 m): MZB 33261–266.
Bulletin Penlitian Hutan. Forest Research Bulletin 462:19–34.
Sikes, R. S., and The Animal Care and Use Committee of the Halmaheramys wallacei
American Society of Mammalogists. 2016. 2016 Guidelines of the Bisa Island, Air Durian (Latitude: 1.23°S, Longitude:
American Society of Mammalogists for the use of wild mammals in 127.58°E, altitude 0 m): AM M24389.
research and education. Journal of Mammalogy 97:663–688. Obi Island, Gunung Sere (Latitude: 1.624°S, Longitude:
Sody, H. J. V. 1941. On a collection of rats from the Indo–Malayan 127.709°E, altitude 870 m) and Cabang Sumbali (Latitude:
and Indo–Australian regions (with description of 43 new genera, 1.378°S, Longitude: 127.659°E, altitude 40 m): MZB and Field
species, and subspecies). Treubia 18:255–325.
Numbers: MZB 38225 (YS 341), MZB 38226 (YS 374), MZB
Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based
phylogenetic analyses with thousands of taxa and mixed models.
38227 (YS 406).
Bioinformatics 22:2688–2690.
Stamatakis, A., P. Hoover, and J. Rougemont. 2008. A rapid boot-
BUNOMYS
strap algorithm for the RAxML web servers. Systematic Biology Bunomys chrysocomus
57:758–771. Sulawesi Island, Bogani Nani Wartabone National Park:
Steppan, S. J., R. M. Adkins, P. Q. Spinks, and C. Hale. 2005. AMNH 256885–889; LAD 18; SAM 12617, 12621, 12627,
Multigene phylogeny of the Old World mice, Murinae, reveals dis- 12629. Bumbarujaba: USNM 218127, 218128, 218132–135,
tinct geographic lineages and the declining utility of mitochondrial 218140 (holotype of Rattus nigellus). Sungai Oha Kecil +
genes compared to nuclear genes. Molecular Phylogenetics and Sungai Sadaunta: AMNH 224054, 224078, 224079, 224081–
Evolution 37:370–388. 086, 224088–091, 224093, 224095, 224096, 224099–105,
Thomas, O. 1920. On mammals from Ceram. Annals and Magazine of 224109–114, 224118–126, 224128–135, 224137–140, 224143,
Natural History (Series 9) 6:422–431. 224647, 224649–660, 224662–671, 224673–688, 224692–
Thomson, V. A., et al. In press. A perspective for resolving the sys-
694, 224696–703, 224706, 224709, 224711, 224713–715,
tematics of Rattus, the vertebrates with the most influence on
human welfare. Zootaxa.
224717, 224719–725, 224728, 224729, 224731, 224733–747,
Voss, R. S. 1988. Systematics and ecology of ichthyomyine rodents 224750, 224752, 224755–758, 224762–765, 224767–769,
(Muroidea): patterns of morphological evolution in a small adapt- and 227730. Danau Lindu Valley + Gunung Kanino: AMNH
ive radiation. Bulletin of the American Museum of Natural History 223040, 223044, 223050–053, 223055, 223057, 223059,
188:1–244. 223062, 223064, 223065, 223069, 223078, 223079, 223081,
Wahlert, J. H. 1974. The cranial foramina of protrogomorphous 223082, 223292, 223297–223300, 223302, 223303, 223308,
rodents; an anatomical and phylogenetic study. Bulletin of the 223310, 223312, 223314, 223317, 223319, 223468, 223567,
Museum of Comparative Zoology 146:363–410. 223568, 224154–224156, 225148; USNM 218691, 218692,
Wallace, A. R. 1860. On the zoological geography of the Malay 218702, 218704. Gimpu: USNM 219580, 219595 (holotype of
Archipelago. Journal of the Proceedings of the Linnean Society of Rattus rallus), 219713. Bakubakulu: AMNH 229519. Gunung
London, Zoology 4:172–184.
Balease: MVZ 225697, 225714, 225810. Gunung Tambusisi:
Wallace, A. R. 1902. Island life, or, the phenomena and causes of
insular faunas and floras: including a revision and attempted solu-
AMNH 265077, 265078; MZB 12181, 12183, 12185; SAM
tion of the problem of geological climates. Macmillan and co, 15588. Pegunungan Mekongga: AMNH 101195, 101197,
London, United Kingdom. 101200, 101202, 101211, 101217, 101220, 101223, 101224,
Watkinson, I. M., R. Hall, and F. Ferdian. 2011. Tectonic re-inter- 101234, 101236 (holotype of Bunomys coelestis koka). Lalolei:
pretation of the Banggai-Sula–Molucca Sea margin, Indonesia. AMNH 101052, 101055 (holotype of Rattus lalolis), 101288.
Geological Society, London, Special Publications 355:203–224.
Watts, C. H. S., and P. R. Baverstock. 1995. Evolution in the Bunomys coelestis
Murinae (Rodentia) assessed by microcomplement fixation of Sulawesi Island, Gunung Lompobatang: AMNH 101132,
albumin. Australian Journal of Zoology 43:105–118. 101133, 101135, 101137, 101138, 101141–101144, 101149,
Whitmore, T. C. 1984. Tropical rainforests of the Far East. 2nd ed. 101150, 101152, 101153, 101155, 101157, 101158; BMNH
Oxford University Press, Oxford, United Kingdom. 97.1.3.12 (holotype of Mus coelestis).
Bunomys prolatus
Submitted 28 June 2017. Accepted 2 November 2017. Sulawesi Island, Gunung Tambusisi: AMNH 265074–076;
MZB 12187, 12188, 12190 (holotype of Bunomys prolatus),
Associate Editor was Jacob Esselstyn. 12191, 12193.
 FABRE ET AL.— A NEW SPECIES OF HALMAHERAMYS 207

Bunomys fratrorum (holotype of Rattus penitus), 218687. Mamasa area: AMNH

Sulawesi Island, Teteamoet: USNM 216836, 216837, 216839, 267790, 267793, 267794; MZB 34845, 34848−50. Pegunungan
216841, 216843, 216887–889, 216892, 216894, 216895, 216897, Latimojong: AMNH 196587, 196588, 196590. Pegunungan
216899, 216902–904, 216906, 216907, 216909–915, 216919, Mekongga: AMNH 101193, 101196, 101209, 101210, 101213,
216920, 216922–926. Kuala Prang: USNM 217587, 217589– 101216, 101222, 101227, 101231, 101235, 101237.
591, 217594, 217596–600, 217602, 217603, 217605, 217606,
217609, 217611, 217613, 217614, 217827–829, 217831, 217832, Bunomys toraja

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217834, 217835, 217837. Gunung Klabat: USNM 217581, Sulawesi Island, Mamasa region, Gunung Gandangdewata,
217585. Rurukan: BMNH 97.1.2.28 (holotype of Mus fratrorum). NMVC 37625, 37633.
Temboan: USNM 217624, 217635, 217638, 217639, 217643,
TAEROMYS
217648–651, 217653, 217655, 217656, 217659, 217661, 217662,
Taeromys celebensis
217666, 217668, 217670, 217854, 217856–858, 217866, 217868,
Sulawesi Island, Teteamoet: USNM 216795, 216801, 216806.
217869, 217876, 217880, 217881, 217887, 217896, 217898,
Mapangat: RMNH 2821. Kuala Prang: USNM 217673, 217675–
217900, 217902 Gunung Maujat + Gunung Mogogonipa: SAM
678. Amurang: RMNH 2801. Temboan: RMNH 21052, 21053;
12616, 12619, 12623, 12644.
USNM 217683, 217695, 217698. Tolitoli: USNM 200261,
Bunomys karokophilus 200264. Sungai Oha Kecil: AMNH 224539, 224640. Sungai Miu:
Sulawesi— Sungai Sadaunta, Tomado, and Sungai Tokararu AMNH 224071, 224072, 224074, 224075. Sungai Sadaunta:
AMNH 223056, 223060, 224153, 225031, 225035, 223046, AMNH 224069, 224070, 224641, 224643–645. Tomado: AMNH
223058, 223072, 223305, 223316. 223027, 223029, 223031, 223032, 223283, 223284, 223565,
224076, 224077. Sungai Tokararu: AMNH 223285, 223287.
Bunomys andrewsi Kuala Navusu: AMNH 225671–673. Sungai Tolewonu: AMNH
Sulawesi Island, Pulau Buton: AMNH 31294; USNM 175899 226411–413. Pinedapa: USNM 219562, 219565, 219706,
(holotype of Mus andrewsi). Labuan Sore: USNM 218115, 219707. Wawo: AMNH 101044, 101075, 101076.
218138. Kuala Navusu + Pinedapa: AMNH 225647–649,
225651–658, 225661–663; USNM 219581, 219587, 219589, Taeromys callitrichus
219591, 219593, 219594, 219596, 219600, 219601, 219602 Sulawesi Island, Rurukan: BMNH 97.1.2.26 (holotype of
(holotype of Rattus adspersus), 219603, 219605, 219606, Rattus maculipilis), 97.1.2.27. “Northeastern Arm”: RMNH
219619, 219620, 219622. Sungai Ranu: AMNH 249942–945; 21255. Sungai Sadaunta: AMNH 224637, 224638. Gunung
CHSW 36. Sukamaju: AMNH 229720. Gunung Balease: Kanino: AMNH 225125. Gunung Nokilalaki: AMNH 225126.
MVZ 225683, 225685, 225688, 225689, 225695, 225708, Kulawi: BMNH 40.388 (holotype of Rattus maculipilis jen-
225710, 225812. Desa Lawaki Jaya: MVZ 225691, 225698, tinki). Tamalanti: BMNH 40.389.
225699, 225702, 225719−721. Wawo + Masembo: AMNH
101059 (holotype of Rattus penitus inferior), 101061, 101069, Taeromys microbullatus
101072. Puro-Sungai Miu: AMNH 257187, 257189, 224630– Sulawesi Island, Pegunungan Mekongga: AMNH 101108
633, 224107, 224116. Tamalanti: BMNH 40.446−40.448, (holotype of Rattus microbullatus), 101109.
40.450−40.452. Tuare: USNM 219598, 219599. Mamasa area:
Taeromys arcuatus
AMNH 267796–798, 267800–804, 267806, 267807; MZB
Sulawesi Island, Pegunungan Mekongga: AMNH 101107, 101110,
34912, 34913, 34916, 34917, 34926, 34955. Lombasang:
101111 (holotype of Rattus arcuatus), 101113–115; MZB 5813.
AMNH 100996–100998, 101004, 101006 (holotype of Rattus
penitus heinrichi), 101009, 101010. Taeromys taerae
Sulawesi Island, Rurukan: AMNH 101244. Lembean: RMNH
Bunomys penitus
22569 (holotype of Rattus taerae), 22570, 22571, 36388.
Sulawesi Island, Gunung Kanino: AMNH 223805, 223806,
223809, 223811, 223814, 223815, 223819–822, 223826, Taeromys hamatus
223828, 223829, 223831–833, 223835, 223836, 223829, Sulawesi Island, Gunung Kanino: AMNH 223369, 223461,
223840, 223842, 223845–850, 223852, 223904–907, 225251, 223701, 223700. Gunung Nokilalaki: AMNH 223702, 223703,
225253, 225254, 225256, 225257, 225260, 225262, 225264, 223705, 225149, 225151, 225152. Gunung Lehio: USNM
225265, 225267, 225269, 225271–273, 225275, 225276, 218680 (holotype of Rattus hamatus), 218685.
225278–285, 225287, 225288, 225290–293, 225295–302,
225304–306, 225376. Gunung Nokilalaki: AMNH 223853, Taeromys punicans
223855, 223857, 223859, 223861–866, 223868, 223870–875, Sulawesi Island, Pinedapa: USNM 219625 (holotype of Rattus
223878–882, 223885–888, 223892, 223895–897, 223899– punicans).
902, 225307, 225308, 225310–315, 225317–325, 225328–
333, 225335, 225336, 225338, 225340–342, 225344–346, PARUROMYS
225348–354, 225359, 225361–365, 225368, 225369. Rano Paruromys dominator
Rano: USNM 219627 (holotype of Rattus sericatus), 219630, Sulawesi Island, Northern peninsula, Teteamoet: USNM
219631. Gunung Lehio: USNM 218682–684, 218686 216797, 216802−804, 216807−812, 216814, 216815,
208 JOURNAL OF MAMMALOGY

216993. Kuala Prang: USNM 217674, 217679, 217680. Sumatra Islands, Goenoeng Dempo: AMNH 106669; Mount
Rurukan: AMNH 101252. Gunung Masarang: BMNH Tanggamus Lampung: RMNH 21253–54.
97.1.2.24 (holotype of Rattus dominator). Temboan: USNM
217681, 217682, 217684−687, 217689, 217690, 217693, Sundamys maxi
217696, 217697, 217700, 217903. Ile-Ile: AMNH 101280. Java Island, Gunung Gede Pangrango: RMNH 14181, 14205–
Sungai Paleleh: USNM 200253, 200255, 200258. Tolitoli: 07, 14210–11, 13566, 21479.
USNM 200262, 200265. Sulawesi Core, Kuala Navusu:

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Sundamys muelleri
AMNH 225687−689, 225691, 225692, 225694, 225696, Sumatra Island, AMNH 102804–5, 102547, 103606; BMNH
225698−701, 225703−709, 225711−715, 225717−719, 55.939, 55.946; RMNH 18351. Rhio Archipelago, BMNH
225721−725, 225728−732, 225735, 225736, 225742−745, 9.4.1.437–38, 9.4.1.441; USNM 104838–39, 113035–6,
225747, 225749, 225751−753, 225939. Sungai Tolewonu: 113039, 115585, 115587, 113052, 114290. Thailand, BMNH
AMNH 226415−418, 226420−423, 226425−433, 226435, 55.2911, 55.2914, 55.2918, 55.2920, 55.2910, 55.2913,
226436. Pinedapa: USNM 219548, 219557, 219564, 55.2917, MNHN CG1990N573. Banka Island, RMNH
219566 (holotype of Rattus dominator camurus), 219728. 21469. Malaysia, MNHN CG1977N211, CG1981N258,
Sungai Oha Kecil: AMNH 224805. Sungai Miu; AMNH CG1981N256; RMNH21470, 23279. Banjak Island, USNM
224174, 224176−178, 224180. Sungai Sadaunta: AMNH 114286. Masalar Island, USNM114620, 114622. Palawan
224173, 224808, 224810, 224811, 224813, 224815, 224816, Island, DMNH 6196; FMNH 63154–55, 63157; USNM
224818−820, 224822, 224824, 224826−832, 224834, 478119, 478121–2, 478125, 478127–31, 478137, 478139,
224835, 224839, 224840, 224844. Sungai Tokararu + 478145–46, 478149.
Gunung Kanino: AMNH 223332, 223334, 223336, 223338,
223340, 223342, 223348, 223351, 223352, 223355, Sundamys annandalei
223573, 223575−577, 223583, 223584, 233588, 223646, Malaysia, BMNH 553152–56; MNHN CG1980N223-4,
223647, 223649, 225380−382, 225384−395, 225397−402, CG1981N233–4, CG1981N238-9, CG1980N241-2,
225404, 225453−455. Gunung Nokilalaki: AMNH 203606, CG1981N246, CG1981N248-9, CG1981N250-1,
223596, 223597, 223600, 223605, 223609, 223613, CG1981N254-5, CG1981N234–7.
223621, 223626, 223629, 223632, 223635−637, 223642, Sumatra Island, MZB 28969.
223643, 223645, 225406−416, 225418, 225422−427,
225430−432, 225434−436, 225438, 225441−446. Lambanan BULLIMUS
+ Sumarorong: AMNH 267746, 267750−754. Sulawesi Bullimus bagobus
Southeastern Peninsula, Wawo + Pegunungan Mekongga: Calicoan Island, USNM 282148. Leyte Island, DMNH 4099,
AMNH 101077, 101116−118, 101120, 101122, 101176. 4107–8, USNM 458789. Mindanao Island, DMNH 5851
Sulawesi Southwestern Peninsula, Gunung Lompobatang: Bohol Island, FMNH 87511. Dinagat Island, DMNH 4584–6.
AMNH 101123, 101160, 101162, 101164−167, 101171−174;
MZB 5593 (holotype of Taeromys dominator ursinus). Bullimus gamay
Caminguin Island, FMNH 154881, FMNH 167886, FMNH
SUNDAMYS 154823.
Sundamys infraluteus
Borneo Island, Mount Kinabalu: BMNH 71.2839-44; FMNH Bullimus luzonicus
108932–6, 108937; MCZ 36105–7, 36108; MZB 23609; Luzon Island, USNM 151505, FMNH 176577, FMNH
USNM 292759, 292763–4, 292765–8, 292770, 301075–7. 176578, FMNH 176582.