The first fossil record of endemic murid rodents from the Philippines: A Late Pleistocene cave fauna from northern Luzon

The first fossil record of endemic murid rodents from the Philippines: Alate Pleistocene cave fauna from northern Luzon

Lawrence R. Heaney,* Philip J. Piper, and Armand S. B. Mijares

(LRH) Field Museum of Natural History, 1400 S Lake Shore Drive, Chicago, Illinois 60605,

U.S.A., e-mail: [email protected];

(PJP, ASBM) Archaeological Studies Program, Palma Hall, University of the Philippines,

Diliman, Quezon City 1101, Philippines

The first fossil record of endemic murid rodents from the Philippines: Alate Pleistocene cave fauna from northern Luzon

Lawrence R. Heaney,* Philip J. Piper, and Armand S. B. Mijares

(LRH) Field Museum of Natural History, 1400 S Lake Shore Drive, Chicago, Illinois 60605,

U.S.A., e-mail: [email protected];

(PJP, ASBM) Archaeological Studies Program, Palma Hall, University of the Philippines,

Diliman, Quezon City 1101, Philippines

Abstract.—Excavations in Callao Cave, in the lowland (ca. 85 m

elevation) Cagayan River Valley of northeastern Luzon, Philippines, have

produced the first fossils of any endemic genera of Philippine murid rodents.

Three dentaries dated to the Late Pleistocene, between ca. 50,000 and 68,000

BP, are referred to the genera Batomys and Apomys; the former is a member

of the endemic ‘‘Phloeomys Division’’ of Philippine murids, and the latter of

the ‘‘Chrotomys Division,’’ also endemic to the Philippines. Batomys iscurrently known from five extant species from Luzon, Mindanao, and

Dinagat islands; the two species known from Luzon differ in size and dental

and mandibular morphology from the two fossil mandibles, and both occur

only at elevations above 1350 m. Apomys is currently known from two

subgenera on Luzon; the fossil is a member of the nominate subgenus,

which contains two species on Luzon, one of which, Apomys microdon, is

conspecific with one fossil. We hypothesize that the Batomys fossils

represent a different species from the living taxa, but we do not name itdue to the fragmentary nature of the specimens. These Apomys and Batomys

represent the first fossil small mammals from the main body of the

Philippine archipelago (east of Huxley’s Line), and the Batomys are the first

suspected extinct Pleistocene small mammal from the Philippines. The

fossils indicate greater species richness and broader distributions than at

present within this distinctive and diverse endemic radiation of mammals.

Keywords: dentary bones, endemism, fossil rodents, murid morphology

The native mammal fauna of the

Philippines is one of the most species-rich

and highly endemic in the world: approx-

imately 183 species have been recorded, of

which at least 120 (66%) are endemic to

the archipelago in a land area of

300,000 km2 (Heaney et al. 2010). Among

these, the murid rodents are perhaps the

most remarkable, with 22 genera (16

endemic; 73%) and 71 species (68 endem-

ic; 96%) recorded thus far in the archi-

pelago. These include tiny (15 g) arboreal

mice (Musseromys spp.), giant (2.6 kg)

cloud rats that are arboreal folivores

(Phloeomys spp.), and fossorial species

(Chrotomys spp.) that feed predominantly

on earthworms (Musser & Heaney 1992,

Jansa et al. 2006, Balete et al. 2008,

Heaney et al. 2009, 2010, Rickart et al.

2011b). Most of these species are mem-

bers of two diverse endemic clades,

informally known as the ‘‘Phloeomys

Division’’ and the ‘‘Chrotomys Division’’

(Musser & Carleton 2005; see also Jansa

et al. 2006, Rowe et al. 2008, Aplin &

Helgen 2010), the former with five genera* Corresponding author.

PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON124(3):234–247. 2011.

(Batomys, Carpomys, Crateromys, Mus-

seromys, and Phloeomys) and about 15

species, and the latter with four genera

(Apomys, Archboldomys, Chrotomys, and

Rhynchomys) and about 29 species (Hea-

ney et al. 2010, 2011). The extent of the

diversity and the numbers of species within

these two large endemic clades imply a

long history within the Philippines, and

molecular data attest that these two clades

have been present within the Philippines

for an estimated 10 to 20 million years

(Jansa et al. 2006, Rowe et al. 2008). Other

genera, such as Bullimus, Crunomys, Lim-

nomys, and Tarsomys, arrived more re-

cently and have undergone diversification,

though less extensively (Rickart et al.

1998, 2002; Jansa et al. 2006). All of these

genera are endemic, except Crunomys,

which includes three extant species from

the Philippines and one from Sulawesi

(Musser 1982, Rickart et al. 1998). Until

now, no fossils were known for any

endemic murid genus, and the only rodent

fossils have come from Palawan Island,

which shares most of its mammal fauna

with Borneo and may have been connected

to it during the Pleistocene (Reis &

Garong 2001, Esselstyn et al. 2004, 2010;

Bird et al. 2005, Lewis et al. 2008, Piper et

al. 2008, 2011). Indeed, most mammal

fossils from the Philippines, all of which

are Pleistocene in age, represent large

species (proboscideans, rhinoceros, pig,

deer, and water buffalo; Beyer 1957,

Bautista 1991, de Vos & Bautista 2001,

Croft et al. 2006, Piper et al. 2008, 2011),

about half of which are extinct.

Excavations in Callao Cave, in Pena-

blanca Municipality, Cagayan Province,

Luzon Island, (17u429N, 121u499E, 85 m

asl) were conducted during 2003, 2007,

and 2009 and recently produced the

oldest evidence of human presence on

Luzon, dated at 67,000 BP (Mijares et al.

2010). The human third right metatarsal

was associated with a small faunal assem-

blage that included the remains of Phi-

lippine brown deer (Cervus mariannus),

the Philippine warty pig (Sus philippensis),

an extinct bovid (possibly related to the

extant dwarf buffalo of Mindoro, Bubalus

mindorensis, and the recently discovered

fossil remains of an extinct diminutive

buffalo on Cebu, Bubalus cebuensis), and

the three murid dentaries reported here

(Piper & Mijares 2007). These faunal

remains were preserved within a thick

limestone breccia between 2.4 and 3 m

below modern ground level. The animal

bones showed a variety of modifications

caused by mechanical abrasion, transpor-

tation and re-distribution under the in-

fluence of fluvial action. Two deer molars

were initially submitted for U Series

dating and returned dates of 52 6 1.4 Ka

(Callao 1) and 54.3 6 1.9 Ka (Callao 2)

for the top and bottom of the breccias

respectively. The human metatarsal III

was submitted separately for U Series

ablation dating, and produced an age of

66.7 6 1 Ka. The disparity in the dates

supports the taphonomic study of the

bones and suggests that this assemblage is

a palimpsest of bone fragments accumu-

lated between 50 Ka and 68 Ka.

The three partial dentaries of rodents

constitute the first fossils of the Philippine

endemic murid genera to be studied,

providing an opportunity to open new

perspectives on the past diversity, distri-

bution, and ecology of this extensive

endemic radiation of mammals. The

purposes of this paper are to morpholog-

ically characterize these fossils, identify

their taxonomic affinity, and discuss their

significance to the understanding of

Philippine mammalian diversity.

Materials and Methods

With two exceptions, specimens of all

species used for comparison with the

fossils are housed at the Field Museum

of Natural History (FMNH). The fossils

are part of the collection of Callao Cave

faunal remains currently housed in the

zooarchaeology laboratory, Archaeologi-

VOLUME 124, NUMBER 3 235

cal Studies Program, University of the

Philippines. At the end of the Callao Cave

Research Project the assemblage will be

become part of the archived collections

held at the National Museum of the

Philippines. The specimen numbers cited

here are excavation numbers. Paula Jen-

kins provided molar length measurements

and photographs of the dentition of the

holotype of Crunomys fallax (housed at

the British Museum (Natural History) 5

Natural History Museum, London;

BMNH) at 103 magnification; we ex-

trapolated the width of the mandibular

molars from the length measurements and

the photographs. Michael Carleton pro-

vided dental and dentary measurements

of the holotype of Batomys dentatus

(housed at the United States National

Museum of Natural History; USNM).

We scanned and slightly modified photo-

graphs of Batomys dentatus from Musser

et al. (1998) to include in figures in this

paper. Comparison of the fossils to extant

species was conducted at FMNH. With

the exception of Batomys dentatus and

Crunomys fallax, images were obtained

with an AMRAY 1810 scanning electron

microscope using uncoated specimens.

Specimens of the fossils and the extant

taxa also were examined under a Wilde

binocular microscope at several magnifi-

cation levels, and measurements were

taken at 6X power, as follows.

M1 to M3 crown length: greatest length

taken at the occlusal surface, from the

anterior rim of the M1 anteroconid to the

rear edge of the M3 posterior loph.

M1 to M2 crown length: taken at the

occlusal surface, from the anterior rim of

the M1 anteroconid to the rear edge of the

M2 posterior cingulum.

M1 crown length: taken at the occlusal

surface along the midline, from the

anterior rim of the anteroconid to the

rear edge of the posterior cingulum.

M1 crown width: taken at the occlusal

surface, on the posterior loph (from the

hypoconid to the entoconid).



anterior rim of the first loph (protoconid

to metaconid) to the posterior rim of the

posterior cingulum.

M2 crown width: taken at the occlusal

surface, on the posterior loph (from thehypoconid to the entoconid).



anterior rim of the first loph (protoconid

to metaconid) to the posterior rim of the

posterior loph (the merged entoconid and

hypoconid).

M3 crown width: taken at the occlusalsurface, on the anterior loph (from the

protoconid to the metaconid).

Dentary depth at M1–M2: taken from

the dorsal edge of the dentary adjacent to

the point of contact between M1 and M2

to the nearest point on the ventral surface

of the dentary, usually slightly posterior

from the M1–M2 edge.The following specimens, all housed at

FMNH except as noted, were examined:

Abditomys latidens (62347); Apomys mi-

crodon (209397, 209398, 209405, 209407,

209585); Apomys musculus (147171,

190773); Archboldomys musseri (147176,

185908, 185909); Batomys dentatus

(USNM 151506); Batomys granti (62504,188321, 193689, 193691); Bullimus luzoni-

cus (180388, 180393, 180434); Carpomys

phaeurus (62291,175565); Crateromys aus-

tralis (University of Michigan Museum of

Zoology 161022); Crateromys schaden-

bergi (62294, 62295, 62296, 198870);

Crunomys fallax (BM(NH) 97.4.8.4); Cru-

nomys melanius (167391, 167888, 191499);Musseromys gulantang (178405); Rattus

everetti (180438, 180441); Tryphomys

adustus (62340–62345).

Results

Batomys sp.

Two of the three dentary fragments are

similar (II-77-J3-7554 and II-77-J3-7573;

we use the final four digits below to refer

236 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON

to these specimens). One dentary (7573)

consists of the entire anterior portion,

except for the thin layer of bone that lies

anterior to the base of the incisor

(Fig. 1A). The dentary is broken diago-

nally from the point where M2 and M3

would have made contact to a point near

the postero-ventral edge of the angular

process; no portion of the coronoid or

condylar region is present. M1 and M2 are

present and undamaged; M3 is absent, but

its alveoli are present though abraded.

The molars have high, lightly worn cusps,

indicating that it came from a young

adult at the time of its death. The second

fragment (7554; Fig. 1B) consists of the

central portion of a dentary; the incisor

and most surrounding bone, and all

portions posterior to M3, are absent.

The molars show extensive wear, indicat-

ing that the individual was an adult at the

time of its death.

Dental and dentary measurements (Ta-

ble 1) and the configuration of the molars

(Fig. 2A, B) of 7554 and 7573 are similar;

their minor differences are principally due

to age at the time of death, especially to

wear on the molars. We consider these

two specimens to represent a single

species. The robust character of the

dentary (Fig. 1A, B), with a large mental

foramen and deep masseteric fossa, ex-

cludes many of the genera of the extant

fauna of Luzon; for example, Archbold-

omys, Chrotomys, and Rhynchomys, all of

which are members of the Chrotomys

Division (Musser & Carleton 2005, Jansa

et al. 2006), have slender, delicate den-

taries, and those genera plus Apomys

have molars that are low-crowned and

much simpler in occlusal morphology

than is evident in the two fossils (see

Figs. 53 and 55 in Musser & Heaney

1992). Abditomys and Tryphomys, both

endemic to Luzon, have comparably

robust mandibles and relatively high-

crowned, complex molars. However, their

M1 molars have an anterolingual cusp

that is smaller than in the two fossils,

cusps composing the laminae are more

extensively merged and less strongly

arched, and the posterior cingulum of

M1 and M2 is moderately to much smaller

than seen in the fossils (see Fig. 70 in

Musser & Heaney 1992). We note alsothat the extant species of Tryphomys, T.

adustus, has teeth much smaller than the

fossils, and the extant Abditomys latidens

is much larger overall. The Philippine

endemic genus Bullimus, and the endemic

species Rattus everetti, also have robust

mandibles (see Figs. 74 and 77 in Musser

& Heaney 1992), but their lower molars

Fig. 1. Lateral views of dentaries of fossil

Batomys sp. from Callao Cave. A, 7573; B, 7554;

C, adult Batomys granti (FMNH 62504); D, adult

Batomys dentatus (USNM 151506; adapted from

Musser et al. 1998). Image of 7554, which is a right

dentary, is reversed to allow easy comparison

with others.


are less high-crowned than in the two

fossils, the laminae are gently arched and

are composed of cusps that are even more

extensively fused, and a well-defined

labial cusplet is present on M1 and M2.

Also, the extant species of Bullimus (B.

luzonicus) and native Rattus (R. everetti)

are substantially smaller than 7554 and

7573. We conclude that 7554 and 7573 do

not represent any of these genera.

In contrast, the molars of these two

specimens, especially the one with only

slightly worn teeth (7573), are similar to

those of a juvenile (FMNH 193699;

Fig. 2C) and old adult Batomys granti

(FMNH 62504; Fig. 2D). Batomys, and

the closely related genus Crateromys,

both of which are Philippine endemics,

are distinctive in having a large antero-

conid that forms the anterior one-third of

the M1 (Musser & Heaney 1992, Musser

et al. 1998). This anteroconid consists of

an anterocentral cusp that is fused with

anterolabial and anterolingual cusps. In

all of these morphological characters, the

two fossils are virtually identical to

Batomys granti and clearly represent a

member of the Phloeomys Division.

Table 1.—Measurements of the dentary and lower molars of fossil Batomys sp., B. dentatus, B. granti, and

Crateromys schadenbergi from northern Luzon.

Callao fossilsBatomysdentatus Batomys granti

Crateromysschadenbergi

7554 7573 151506 62504 188321 193691 193689 n 5 4adult young adult adult adult old adult adult old adult adults

M1–M3, crown 10.48 2 9.32 8.83 8.54 8.06 8.15 16.43 6 0.56

15.92–17.23

M1 crown length 4.33 4.35 3.72 3.92 3.98 3.58 3.58 6.36 6 1.20

6.15–6.61

M1 crown width 2.93 2.74 2.50 2.71 2.59 2.33 2.40 3.92 6 0.15

3.78–4.09

M2 crown length 3.12 3.14 2.76 2.65 2.61 2.46 2.52 4.82 6 0.14

4.63–4.96

M2 crown width 3.18 3.02 2.73 2.64 2.60 2.30 2.31 4.21 6 0.26

3.99–4.57

M3 crown length 2.76 2 2.74 2.46 2.21 2.04 2.27 5.15 6 0.44

4.56–5.62

M3 crown width 2.71 2 2.70 2.47 2.10 2.06 2.21 4.16 6 0.31

3.71–4.37

Dentary depth at

M1–M2

7.82 7.31 6.80 6.52 6.38 6.49 6.23 11.87 6 0.34

11.56–12.36

Fig. 2. Views of occlusal surface of lower molars

of fossil Batomys. A, 7573; B, 7554; C, juvenile

Batomys granti (FMNH 193699); D, adult Batomys

granti (FMNH 62504); E, adult Batomys dentatus

(USNM 151506; adapted from Musser et al. 1998).


The endemic genus Carpomys, a mem-

ber of the Phloeomys Division and sister-

taxon to Batomys and Crateromys (Jansa

et al. 2006), has a similar M1 anteroconid,

but its anterocentral component is com-

posed of two cusps. On a specimen of

Carpomys that shows as little wear as

7573, these two cusps should be visible (as

in the specimen shown in Fig. 35D in

Musser & Heaney 1992), but they are not.

Additionally, an anterolabial cusp on M2

is conspicuous on C. phaeurus but not

visibly present on the fossils. On M3, the

metaconid-protoconid lamina is gently

and smoothly arched in Carpomys,

whereas in the fossils the lamina is

strongly arched, with a rather deep cleft

between the metaconid and protoconid

centers, which is similar to the morphol-

ogy of Crateromys schadenbergi. We

conclude that the two fossils do not

represent Carpomys.

Based on general qualitative features,

the two fossils could represent either

Batomys or Crateromys. Crateromys scha-

denbergi, the only member of the genus

that occurs on Luzon, has molars that are

similar in most respects to the two fossils

but are somewhat higher-crowned than

those of Batomys (see Fig. 35 in Musser &

Heaney 1992), and most specimens of C.

schadenbergi have a small but distinct

posterior cingulum on M3 (on both left

and right sides in four of five specimens at

FMNH, and on one side in one specimen)

that is absent on the fossils. Crateromys

schadenbergi is much larger than the

species of Batomys (Table 1) and the

two fossils, and the dentaries are propor-

tionally much deeper than in the fossils.

We conclude that the fossils do not

represent C. schadenbergi, but the simi-

larity leads us to compare it to two

smaller species of Crateromys, each

known only from the holotype: C. aus-

tralis, from Dinagat Island, which lies at

the NE tip of Mindanao, and C. paulus,

from Ilin Island, adjacent to Mindoro.

The dentary and lower molars of both

species are generally very similar to, but

substantially larger than, the two fossils

and the dentary is much deeper (see Fig. 9

in Musser et al. 1998). On M1, the second

loph (composed of the metaconid-proto-

conid) is connected to the first loph

(anterolabial and anterolingual cusps) by

a narrow peninsula in the two fossils, and

in C. paulus (and C. schadenbergi) but not

in C. australis. The anterior edge of M2 is

slightly more slanted to the lingual side in

the fossils and C. paulus (and C. schaden-

bergi) than in C. australis, making the M2

appear less square. The internal basins

that mark the locations of the protoconid

and metaconid in M2 are proportionately

slightly larger in C. australis than in the

fossils, C. paulus, and C. schadenbergi,

and both lophs in M3 are slightly broader

in C. australis than in the fossils and C.

paulus and C. schadenbergi. As in C.

schadenbergi, the dentaries of C. australis

and C. paulus are much more robust

overall than are the fossils (compare with

Fig. 9 in Musser et al. 1985). Although

similar to Crateromys, especially C. pau-

lus, the Callao Cave fossils represent a

much smaller, less robust animal with a

thinner dentary than any extant species of

Crateromys.

A ‘‘smaller, less robust animal with a

thinner dentary’’ describes the sister-

genus to Crateromys, Batomys, quite well

(Musser & Heaney 1992, Musser et al.

1998, Jansa et al. 2006). Two species of

Batomys are currently known from Lu-

zon; both are smaller and the skull

generally less robust than the known

species of Crateromys. The dentary of

Batomys granti is smaller than that of

7554 and 7573; for example, the crown

length of M1 in the fossils is 4.33–4.35 mm,

but is 3.67–4.04 in B. granti, and the

depth of the mandible in the fossils is

7.31–7.82 mm vs. 6.38–6.55 mm in B.

granti; these differences are in the range of

10–20% (Figs. 1, 2; Table 1). A scatter-

plot of dentary depth at M1–M2 vs. crown

width of M1 for the two fossils and four


specimens of B. granti (plus one specimen

of B. dentatus; see below) clearly shows

these differences (Fig. 3). Additionally,

the laminae formed by the metaconid and

protoconid in M1, M2, and M3, and

entoconid and hypoconid in M1 and M2,

are more strongly arched than in the two

fossils, leaving a deep cleft between the

pairs of conids in each case (Fig. 2C),

except when these molars are very heavily

worn (Fig. 2D). We reject the hypothesis

that the fossils represent B. granti, but

they could represent a closely related,

larger species.

The second extant species of Batomys

on Luzon, B. dentatus, is currently known

only by the holotype (USNM 151506)

and is larger than B. granti. For example,

the crown length of the molar toothrow is

9.8 mm, vs. 7.8–8.4 mm in B. granti, but it

is smaller than the two fossils in all

measurements, except length and width

of M3 (Table 1) and the dentary of the

fossil is deeper (Fig. 3). Also, the poste-

rior cingulum on M1 and M2 is smaller

and rounder in B. dentatus (Fig. 2E),

rather than larger and cordate as in B.

granti (Fig. 2C) and the two fossils

(Fig. 2A, B). We reject the hypothesis

that the fossils represent B. dentatus but

recognize that the difference in posterior

cingulum is small, based on a sample size

of one, and we recommend that further

comparisons be made when additional

specimens of B. dentatus become avail-

able. We hypothesize that 7554 and 7573

represent a currently unknown and pos-

sibly extinct species of Batomys that is

larger than either extant species.

As discussed below, we also note that

the two species of Batomys currently

occur only above ca. 1350 m in montane

forest, not in the lowland forest habitat

that would most likely have persisted

during the late Pleistocene at the elevation

of Callao Cave (Stevenson et al. 2010),

even taking into consideration potential

lowering of the montane and submontane

vegetation zones related to depressed

global temperatures during the Pleisto-

cene (Kershaw et al. 2007). In addition,

diminution in size during the Holocene,

as observed in mammals on Borneo

(Hooijer 1962, Medway 1964, Cranbrook

1986, Harrison 2000, Cranbrook & Piper

2007, 2008) and Palawan (Piper et al.

2011), is unlikely to account for the

differences between the fossil specimens

and extant species of Batomys.

Apomys microdon

The third fossil dentary fragment, II-

77-J3-7577 (referenced below as 7577), is

that of a murid substantially smaller than

Batomys; the crown length of M1 is

2.01 mm (Table 2). The specimen is

represented by the basal portion of the

incisor (where it enters the bony sheath)

to the posterior portion of the dentary,

with the coronoid, condylar, and angular

processes missing. The dentary (Fig. 4A)

is robust, broad in lateral view and thick

beneath the molars. It has a large mental

foramen that lies below the anterior edge

of M1, slightly labial to the dorsal edge of

the mandible. The masseteric fossa is

large and deep, extending to a point

about one-third of the way anterior to

the posterior edge of M1 (Fig. 4A). The

first two molars are present in the

dentary, and what appears to be the

Fig. 3. Scatterplot (mm) of dentary depth at

M1–M2 versus crown width of M1 for Batomys

dentatus, B. granti, and two fossil Batomys (see

Table 1).


missing third molar was found in the

matrix immediately adjacent to the den-

tary. The heavily worn molars indicate

that the animal was an old adult at the

time of death (Fig. 5A). All three molars

are broad, and M1 and M2 have nearly

parallel labial and lingual margins. There

is thick enamel around the periphery of

each tooth, and each has either one (M3)

or two (M1 and M2) enamel crescents

cutting across the tooth that represents

the remains of the primary lamina. Both

M1 and M2 have a large anterior and

medial lamina and a robust posterior

cingulum of moderate size.

Species of the endemic genera Abdit-

omys, Batomys, Bullimus, Carpomys, Cra-

teromys, Chrotomys, Rhynchomys, and

Tryphomys, and the Philippine endemic

Rattus everetti are all many times larger

than this specimen, and all, except Chrot-

omys and Rhynchomys, have teeth that

are substantially more complex and high-

er-crowned. Chrotomys and Rhynchomys

have even simpler and proportionately

much less robust molar teeth (see Musser

& Heaney 1992, Heaney et al. 2009). We

reject the hypothesis that the fossil

represents any of these genera.

Genera that are currently known from

Luzon that have species similar in size to

7577 are Apomys, Archboldomys, Cru-

nomys, and Musseromys. The newly

discovered genus Musseromys is a small

(ca. 17 g) relative of Batomys, Carpomys,

and Crateromys, currently represented

only by the holotype of Musseromys

gulantang (Heaney et al., 2009). The

configuration of the dentary of 7577

is generally similar to the holotype of

M. gulantang in its robust configuration

and well-developed masseteric fossa

(Fig. 4D). The angular, coronoid, and

condyloid processes of M. gulantang are

distinctive (Fig. 5D), but these processes

are absent from 7577. However, some

differences are apparent. The base of the

incisor of 7577 is even more robust than

that of M. gulantang. The molars of 7577

are about one-third larger in width and

breadth than those of M. gulantang,

resulting in a tooth row that has roughly

twice the occusal surface area as in M.

gulantang. Most distinctively, the com-

Table 2.—Measurements (in mm) of the dentary and lower molars of fossil Crunomys sp. from Callao

Cave, Apomys microdon, the holotype of C. fallax, C. melanius, and Archboldomys musseri. Samples of 3

given as mean and range; sample of 4 as mean 6 standard deviation and range.

Callao Apomys microdon Crunomys fallax Crunomys melanius Archboldomys musseri7577 n 5 4 97.4.8.4 n 5 3 n 5 3

M1–M2, crown length 3.56 3.64 6 0.14 3.01 3.26 3.14

3.50–3.83 3.22–3.29 3.12–3.19

M1–M3, crown length 2 4.89 6 0.16 3.78 4.12 4.11

4.68–5.03 4.08–4.18 4.08–4.15

M1 crown length 2.01 2.03 6 0.13 1.73 1.92 1.77

1.89–2.18 1.90–1.93 1.74–1.80

M1 crown width 1.2 1.27 6 0.04 0.95 1.23 1.04

1.23–1.32 1.15–1.29 1.02–1.07

M2 crown length 1.57 1.68 6 0.07 1.28 1.37 1.35

1.61–1.75 1.31–1.41 1.31–1.37

M2 crown width 1.33 1.33 6 0.06 1.03 1.2 1.09

1.27–1.40 1.15–1.23 1.08–1.10

M3 crown length 1.14 1.20 6 0.03 0.79 0.86 0.99

1.18–1.25 0.82–0.92 0.98–1.01

M3 crown width 0.98 1.01 6 0.03 0.78 0.79 0.87

0.96–1.05 0.78–0.82 0.85–0.90

Dentary depth,

below M1–M2

3.7 3.61 6 0.09 2.93 3.41 2.6

3.51–3.74 3.28–3.57 2.56–2.65


plex pattern of enamel folds in the molars

of M. gulantang is similar to that in

Batomys and Carpomys. On the basis of

these differences, we reject the hypothesis

that 7577 represents Musseromys.

Archboldomys is currently known from

three morphologically similar species, all

from the mountains of Luzon. One of

these, A. musseri, occurs on Mt. Cetaceo,

which lies near Callao Cave. In compar-

ison with the Callao fossil, A. musseri has

a delicate mandible and molar teeth (see

Figs. 8, 13 in Rickart et al. 1998); in three

adult specimens, the depth of the mandi-

ble below the point of contact of M1–M2

averages 2.60 mm (vs. 3.70 mm in the

fossil), M1 averages 1.77 mm in length (vs.

2.01 mm), M2 averages 1.35 in length (vs.

1.57), and M3 averages 0.87 mm (vs.

1.14 mm). Molar configuration in the

Callao fossil and A. musseri is similar in

having simple, low-crowned molars, but

the outline of M1 and M2 in A. musseri in

occlusal view has a distinct ‘‘waist’’

between the anterior and posterior lami-

nae (see Fig. 8D in Rickart et al. 1998),

whereas the outline of M1 and M2 in the

Callao fossil is nearly straight (Fig. 5A).

Additionally, the posterior cingulum in

M1 and M2 is much more strongly

developed on the Callao fossil than in A.

musseri. On the basis of these differences,

we reject the hypothesis that 7577 repre-

sents Archboldomys musseri or any other

member of the genus.

Comparison of 7577 with the holotype

and only known specimen of Crunomys

fallax, which was taken in the foothills of

the Sierra Madre within ca. 50 km of

Callao Cave, shows a greater degree of

Fig. 4. Dentaries. A, fossil Apomys microdon

from Callao Cave (7577); B, Apomys microdon

(FMNH 209504); C, Crunomys fallax (BM(NH)

97.4.8.4); D, C. melanius (FMNH 167391).

Fig. 5. Views of occlusal surface of lower

molars. A, fossil Apomys microdon from Callao

Cave (7577); B, Apomys microdon (FMNH 209504);

C, Crunomys fallax (BM(NH) 97.4.8.4); D, C.

melanius (FMNH 167391). The M3 of 7577 is here

shown in its socket, rather than beside the dentary as

it was found in the matrix.


similarity, but differences are evident. The

dentary of C. fallax is more slender than

that of the Callao fossil and smaller

overall: the depth of the dentary below

the point of contact of M1 and M2 is

2.93 mm compared to 3.70 in the Callao

fossil, and the crown length of M1 is 1.73

in C. fallax vs. 2.01 mm in the fossil. The

masseteric fossa is equally deep in the

two, though it reaches farther anteriorly

in C. fallax than in 7577 (Fig. 4A, C). A

deep cleft between the first and second

laminae of M1 and M2 on C. fallax has no

observable counterpart on the Callao

fossil, and M3 is proportionately smaller

(Fig. 5A, C). We note that C. melanius,

known from Mindanao, Camiguin and

Leyte, is slightly larger than C. fallax, but

measurements (Table 2) and examination

of specimens show that the same differ-

ences are present. On this basis, we reject

the hypothesis that Callao fossil 7577

represents a species of Crunomys.

Most extant species of Apomys on

Luzon are much larger than the Callao

fossil and have proportionately more

gracile dentaries (Heaney et al. 2011).

However, two species are small, with one

much smaller (A. musculus) and the other

(A. microdon) very similar in size to the

fossil (Fig. 4, Table 2). Because the prin-

cipal difference between these two extant

Apomys in dentary and molar morpholo-

gy is size, we focus our comparisons on A.

microdon.

In overall configuration, the Callao

fossil dentary has no apparent differences

from A. microdon: the thickness of the

dentary, position and depth of the mas-

seteric fossa, the position and size of the

mental foramen, and the thickness of the

incisor are all nearly identical (Fig. 4A, B;

see also Musser 1982). In occlusal view,

the molars share virtually all aspects of

their configuration: the molars are robust,

with the lateral margins of M1 and M2

nearly straight and parallel (without a

‘‘waist’’ between the first and second

laminae); M2 is nearly square in outline,

although the posterior laminae on M1 and

M2 on FMNH 209405 are slightly more

bulbous laterally; the enamel posterior

edges of the first and second laminae are

similarly curved; the posterior cingula on

M1 and M2 are cordate and robust; and

M3 is in the shape of a rounded triangle,

extended somewhat posteriorly, although

that of 7577 is slightly smaller (Fig. 5A,

B). The molars of 7577 are slightly out of

alignment; we suspect that this represents

individual variation. The molars of 7577

are slightly more heavily worn than those

of the A. microdon that is figured, and we

suspect that some differences are due to

the amount of wear. Based on the

consistent similarity and absence of sub-

stantive differences, we conclude that

Callao Cave fossil 7577 represents a

specimen of Apomys microdon.

Discussion and Conclusion

Although the three fossil dentaries

reported here represent fragmentary ma-

terial that does not allow extensive

description, they can be allocated to two

extant genera, Batomys and Apomys. The

two specimens of Batomys, which we

consider to represent a single species, are

similar to extant species but cannot be

assigned to extant species due to differ-

ences in dental morphology and larger

overall size. The other specimen repre-

sents Apomys microdon, differing only

slightly from modern specimens.

Several general conclusions may be

drawn from these specimens, meager as

the material may be. First, although the

extant mammal fauna of the Philippines,

and of Luzon in particular, is one of the

globally richest in terms of numbers of

endemic species per unit area, the Late

Pleistocene fauna appears to be richer

still, by one species at least. Previously,

the past diversity of murid rodents (which

make up the great majority of Luzon

endemic mammals) could only be inferred

from phylogenies (e.g., from studies such


as Steppan et al. 2003, Jansa et al. 2006,

Heaney et al. 2011). Additional fossils

would be of great utility in determining

the full extent of the past fauna.

Second, these preliminary data imply

that one species of Philippine small

mammal may have become extinct since

the Late Pleistocene. Previously docu-

mented extinct Pleistocene mammals were

all large (proboscideans, rhinoceros, and

water buffalo; Beyer 1957, Bautista 1991,

Croft et al. 2006, Piper et al. 2008).

Information that improves our under-

standing of the timing and causes of any

extinction would add a valuable new

element to the gradually emerging history

of mammalian diversity in this complex

archipelago.

Third, the presence of Batomys sp. in

the lowlands, especially in the broad

Cagayan River Valley, is unexpected,

given that the species currently known

on Luzon occur only in the Central

Cordillera on the opposite side of the

Cagayan River, not in the Sierra Madre

immediately to the east. Further, they live

only in montane forest from ca. 1350 to

2480 m, feeding on herbaceous material

on the ground and in trees in habitat

dominated by trees such as oaks (e.g.,

Lithocarpus spp.), myrtles (e.g., Syzygium

spp.), and conifers (Podocarpus, Agathis,

and Pinus); the two species of Batomys

that occur on Mindanao have similar

ecological associations (Heaney et al.

2006, 2010; Balete et al. 2008, Rickart et

al. 2011a), although two species on the

small island of Dinagat occur at much

lower elevations (Heaney & Rabor 1982,

Musser et al. 1998). The presence of

Batomys in Callao Cave at ca. 85 m

elevation implies either that species of this

genus on Luzon had broader ecological

tolerances in the past than they do

currently, or that the climate has changed

sufficiently to alter elevational distribu-

tion of the genus. Studies have produced

evidence of elevationally lower vegetation

bands and different plant communities on

Luzon during the Late Pleistocene and

early Holocene (Stevenson et al. 2010),

but they do not indicate the presence of

the ‘‘montane’’ oak-myrtle-conifer plant

community at this low elevation. In

contrast, Apomys microdon occurs today

in the nearby foothills at elevations from

sea level to ca. 2025 m, foraging both on

the ground surface and in the trees,

probably feeding mostly on seeds and

invertebrates (Heaney et al. 2010, Balete

et al. 2011); thus, its presence at the cave

at any time in the Pleistocene or Holocene

is not surprising. However, it should be

noted that current lowland murid faunas

typically include only three or four native

species (in the genera Apomys, Bullimus,

Chrotomys, and Rattus), and the addition

of even one lowland species implies

greater species richness in the past; this

contrasts with the 8 to 12 species that

often occur at high elevation (Rickart et

al. 1991, Heaney 2001, Balete et al. 2009,

2011; Heaney 2011). Future studies may

determine whether other murid species

once present in lowlands during the

Pleistocene occur today only at much

higher elevations and on different moun-

tain ranges; such paleontological evidence

would add new and unexpected dimen-

sions to the historical biogeography and

community ecology of Philippine mam-

mals.

Fourth, at this time we have no

evidence to determine if these murids

were food for the humans living in the

cave at the time, if they were brought into

the cave by owls, or if they used the cave

as a nesting site. Given the questions

raised above about extinction, any infor-

mation on these matters would be valu-

able.

In conclusion, the discovery of these

three specimens has opened a new win-

dow onto the past history of the extraor-

dinary mammal fauna of Luzon Island.

Greater diversity existed in the Late

Pleistocene than had been known or

could be inferred from phylogenetic


studies of extant species, and greater

diversity extended into lowland areas

where current species richness of small

mammals is very low. These observations

in turn imply either significant changes in

climate or significant differences in hab-

itat use by the extinct species. Finally, the

cause(s) and extent of any extinction must

now be investigated so that its role in the

dynamics of mammalian species richness

in the archipelago can be understood.

Priorities for future research should in-

clude a search for additional fossils and

for detailed surveys of extant mammals in

the forest on nearby hills and mountains

above the cave, including the rugged areas

of karst near the cave.

Acknowledgments

Field studies at Callao Cave have been

supported and encouraged by the Na-

tional Museum of the Philippines (NMP),

the Cagayan Provincial Government, and

the Protected Areas Management Board–

Penablanca; the loan of the fossils to

FMNH was conducted under permit

from the NMP. We thank Betty Strack

for assistance in use of the scanning

electron microscope, and Andria Nied-

zielski for preparing the figures. Michael

Carleton and Paula Jenkins kindly mea-

sured the holotypes of Batomys dentatus

and Crunomys fallax, respectively, for

which we are grateful. We thank D. S.

Balete, M. D. Carleton, G. G. Musser,

and E. A. Rickart for comments that

greatly improved several earlier drafts of

this manuscript. Funding for field work

came from an Australian Research Coun-

cil Discovery Grant to Peter Bellwood

and a University of the Philippines grant

to Armand Mijares, and for carbon-

dating from the Australian Research

Council Grant DP0664144. Studies at

the Field Museum were supported by

the Barbara Brown Fund for Mammal

Research and the Negaunee Foundation.

The research of Philip Piper was funded

by a special grant from the Chancellor’s

Office and administered by the Office of

the Vice Chancellor for Research and

Development of the University of the

Philippines.

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The first fossil record of endemic murid rodents from the Philippines: A Late Pleistocene cave fauna from northern Luzon