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ORIGINAL INVESTIGATION
Diversity patterns of small mammals in the Zambales
Mts., Luzon, Philippines
Danilo S. Baletea, Lawrence R. Heaneya, Maria Josefa Veluzb, Eric A. Rickartc,�
aDepartment of Zoology, Field Museum of Natural History, 1400 S Lake Shore Drive, Chicago, IL 60605, USAbZoology Section, Philippine National Museum, P. Burgos St., Ermita 1000, Manila, PhilippinescUtah Museum of Natural History, University of Utah, 1390 E Presidents Circle, Salt Lake City, UT 84112, USA
Received 1 April 2008; accepted 15 May 2008
Abstract
In 2004 and 2005, we conducted a survey of the small mammals on Mt. Tapulao ( ¼Mt. High Peak, 2037m) in theZambales Mountains, Luzon Island, Philippines in order to obtain the first information on the mammals of this newlydiscovered center of endemism. We also tested two hypotheses regarding the relationship of species richness withelevation and the impact of alien species on native mammals. The survey covered five localities representing habitatsfrom regenerating lowland rain forest at 860m to mossy rain forest near the peak at 2024m. We recorded 11 species,including 1 native shrew, 1 alien shrew, 8 native rodents, and 1 alien rodent. Two species of Apomys and one species ofRhynchomys are endemic to Zambales; this establishes the Zambales Mountains as a significant center of mammalianendemism. Species richness of native small mammals increased with elevation, from five species in the lowlands at925m to seven species in mossy forest at 2024m; total relative abundance of native small mammals increased from 925to 1690m, then declined at 2024m. Alien small mammals were restricted to highly disturbed areas. Our results supportthe prediction that maximum species richness of small mammals would occur in lower mossy forest near the peak, notnear the center of the gradient. Our results also support the hypothesis that when a diverse community of nativePhilippine small mammals is present in either old-growth or disturbed forest habitat, ‘‘invasive’’ alien species areunable to penetrate and maintain significant populations in forest.r 2008 Deutsche Gesellschaft fur Saugetierkunde. Published by Elsevier GmbH. All rights reserved.
Keywords: Endemism; Elevational gradients; Species richness; Invasive species; Philippines
Introduction
The mammalian fauna of the Philippines is remark-able for its high level of overall species richness andendemism (over 70% of the ca. 125 species of non-volant mammals; Heaney et al. 1998; Balete et al. 2007).Much of the diversity is associated with the geological
history of the archipelago. Most of the islands areoceanic in origin, and have had no dry land connectionsto the Asian continent. Each modern island (or set ofadjacent islands that were connected to each otherduring Pleistocene periods of low sea level) is a uniquecenter of mammalian biodiversity, with levels ofendemism ranging from 40% to nearly 90% (Heaney1986, 2004; Heaney et al. 1998; Heaney and Regalado1998). On Luzon, the largest island in the country at108,000 km2, three sub-centers of mammalian endemismhave been recognized: the Central Cordillera of northern
ARTICLE IN PRESS
www.elsevier.de/mambio
1616-5047/$ - see front matter r 2008 Deutsche Gesellschaft fur Saugetierkunde. Published by Elsevier GmbH. All rights reserved.
doi:10.1016/j.mambio.2008.05.006 Mamm. biol. 74 (2009) 456–466
�Corresponding author. Tel.: +1 801 585 7759;
fax: +1 801 585 3684.
E-mail address: [email protected] (E.A. Rickart).
Author's personal copy
Luzon, Mt. Isarog in southern Luzon, and the northernSierra Madre of NE Luzon (Heaney et al. 2005; Onget al. 2002; Rickart et al. 1991, 1998; Rickart andHeaney 1991). This paper provides the first documenta-tion of the ecology and diversity patterns of speciesfound in the fourth sub-center of Luzon mammaldiversity, the Zambales Mountains of west-centralLuzon, including the newly described Rhynchomys
tapulao (Balete et al. 2007), and two species of Apomys
that were discovered during this survey (Heaney et al. inpreparation).
In conducting our survey of Mt. Tapulao, the highestpeak in the Zambales Mountains at 2037m, we alsogathered data relevant to two general issues. Regardingthe first of these, recent studies of the pattern of speciesrichness of small mammals along elevational gradientshave demonstrated that maximum species richnessusually does not occur in the lowlands, but rather atsome higher elevation. This pattern has been documen-ted among small mammals in places as diverseas Central America (McCain 2004), Madagascar(Adrianjakarivelo et al. 2005), Taiwan (Yu 1994),Tanzania (Stanley and Hutterer 2007), Malaysia(Md. Nor 2001), Mexico (Sanchez-Cordero 2001), andthe Rocky Mountains of Utah, USA (Rickart 2001),among other regions (McCain 2005). Our previousstudies of small mammals along elevational gradients inthe Philippines have documented a consistent pattern ofincreasing species richness and relative abundance withincreasing elevation up to about 2000m; when themountain reaches only this elevation, species richnessalso reaches its maximum near this elevation (Heaney2001; Heaney et al. 1989, 1999; Rickart et al. 1991,1993). On higher mountains, such as Mt. Kitanglad,Mindanao Island, species richness peaks at about2000–2200m and then declines steadily above this level,producing a curvilinear pattern along the elevationalgradient (Heaney 2001; Heaney et al. 2006).
While the existence of a curvilinear pattern along suchgradients is becoming widely accepted, the causesremain in debate (e.g., Colwell et al. 2005; Dunn et al.2007), and further studies are needed to document theextent of variation and its causes. We note two primaryhypotheses with differing predictions. The mid-domaineffect predicts maximum species richness at roughly themid-point of an elevational transect (e.g., Colwell et al.2004; McCain 2005, 2007), whereas our ecologicallybased empirical studies on Mt. Isarog and Mt. Bali-it(Heaney et al. 1999, 2005; Rickart et al. 1991) havefound that species richness of Philippine small mammalspeaks at the level at which clouds form, causing atransition from montane to mossy forest, typically1800–2200m, regardless of the height of the mountain.
We also use the Tapulao survey data to test thefollowing hypothesis: when a diverse communityof native Philippine small mammals is present in either
old-growth or disturbed forest habitat, alien species areunable to invade and maintain significant populations(Heaney et al. 1999). This hypothesis, which is based ona pattern documented in three areas of the Philippines(Heaney et al. 1989, 1999, 2005, 2006; Rickart et al.1991, 1993), stands in sharp contrasts with the commonassumption that non-native species from continentalareas are competitively superior to endemic islandspecies (e.g., Whittaker and Fernandez-Palacios 2007,p. 295–300).
Methods
Study area
At 2037m, Mt. Tapulao (also called High Peak) is the
highest point in the Zambales Mountain Range, on the
west-central flank of Luzon (Fig. 1). The Zambales Range is
bounded by the South China Sea on the west and north,
the Central Plains on the east, and Subic Bay and the
Mt. Natib/Mariveles complex on the southeast. The Zambales
Mountains are known, along with Mindoro, for the occurrence
of the Sumatran pine, Pinus merkusii, known to local people as
‘‘tapulao’’.
The Zambales Mountain Range constitutes a geologically
distinct block of Luzon, the Zambales Ophiolite Complex,
known for both its active volcanoes in the southeastern
portion of the range (including Mt. Pinatubo), and for its
mantle-derived ultramafic and ultrabasic sequences emplaced
during island arc formation (Bachman et al. 1983; Hashimoto
1981). It is known for its chromite and nickel deposits and was
one of the world’s top sources of metallurgical chromite from
the mid-1930s to early 1990s. The area is now being explored
for platinum.
In contrast to the geological resources, the Zambales biota
is poorly known. Based mainly on its floristic endemism and
rich bird fauna, the mountain range has been recognized as a
high priority conservation area in the Philippines (Mallari
et al. 2001; Ong et al. 2002), but it currently lacks protected
areas. In a 1992 survey, 50 species of amphibians and reptiles
were recorded, of which 45 were first records for the mountains
(Brown et al. 1996). Among mammals, Heaney et al.
(1998, 2002) reported only 9 confirmed species from Zambales
Province, and considered it to be poorly known. Ong et al.
(1999) tentatively reported Apomys spp., Bullimus luzonicus,
Chrotomys mindorensis, and Rattus everetti from low eleva-
tions near Subic Bay. Mildenstein et al. (2005), Ruedas et al.
(1994), and Stier and Mildenstein (2005) reported on bats from
Zambales Province. Using specimens included in this study,
Balete et al. (2007) described Rhynchomys tapulao, the first
high-elevation endemic mammal from Zambales, and current
studies indicate that two species of large mice, referred to here
as Apomys sp. 1 and A. sp. 2, are endemic to Zambales
(Heaney et al. in preparation).
The vegetation of Mt. Tapulao consists of several types:
‘parang’ grassland, logged-over and regenerating lowland
dipterocarp forest, montane forest, mossy forest, and pine
forest. Parang grassland comprised much of the lowland areas
on the west side of Mt. Tapulao up to ca. 500m. It occupies
ARTICLE IN PRESSD.S. Balete et al. / Mamm. biol. 74 (2009) 456–466 457
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the gently sloping foothills, dominated by cogon
(Imperata cylindrica) and erect bamboo locally called ‘‘buho’’
(Schizostachyum lumampao). Trees and shrubs, including
banaba (Lagerstroema speciosa; Lythraceae) were low and
scattered. Highly disturbed lowland forest below 900m existed
in fragments restricted to gullies and steep riverbanks. Slash-
and-burn farming (kaingin) and logging for the few remaining
tall dipterocarps in the area were extensive. Between 900 and
1200m, regenerating lowland forest was more extensive but
signs of both present and past logging were common. Between
approximately 1200 and 1700m, montane forest occurred on
the sides of undisturbed steep ridges. Cogon and pine trees
dominated extensive sections of the ridge-tops and eroded
slopes. Some eroded slopes up to ca. 1800m appeared to have
been caused mainly by mining, especially the east section
facing Sawtooth Mountain. Primary mossy forest occurred
from 1800m to the peak at 2037m, but certain sections
(marked by forest clearing, discarded garbage, and presence of
cogon and pine) showed distinct signs of past disturbance
related to mining. Volcanic ash from the 1991 eruption of
Mt. Pinatubo was visible at all of our sites. Other relevant
habitat data on the High Peak and the Zambales Range can be
found in Brown et al. (1996), Mallari et al. (2001), and Ruedas
et al. (1994).
Our survey was conducted at five sampling localities
(Fig. 1), enumerated and described below, from March 2004
to January 2005. Represented habitats included disturbed,
regenerating lowland dipterocarp forest (Sites 1 and 2, at 860
and 925m), lightly disturbed lower montane forest (Site 3, at
1200m), lightly disturbed old-growth montane forest (Site 4, at
1690m), and old-growth lower mossy forest (Site 5, at 2024m).
Localized heavy disturbance at Sites 2–5 was associated with a
mining road.
� Site 1. Upper Salaza River, 4.25 km W, 2.25 km S Tapulao
peak, 860m elev., 15127056.800N, 120104054.300E (05–08
April 2004). This site was located on a steep slope above
the bank of a nearly dry tributary of Salaza River, well
away from a mining road. The vegetation was lowland
dipterocarp forest that had been partially logged, but had
regenerated well by the time of our survey; the canopy
reached ca. 20m, consisting mainly of species of Dipter-
ocarpaceae, Fagaceae, Lauraceae, and Myrtaceae. DBH of
canopy trees did not exceed 50 cm. Emergents were
uncommon, consisting mainly of almaciga (Agathis sp.)
that reach up to ca. 25m high and ca. 50–90 cm DBH.
Canopy vines were particularly common, including jade
vine (Strongylodon cf. macrobotrys) and climbing bamboos
(Dinochloa spp.) that covered the crowns of many trees.
Climbing pandans (Freycinetia spp.) were uncommon.
Epiphytic ferns and orchids were present on tree trunks
and large branches. Forest floor vegetation consisted of tree
saplings, rattans (Calamus spp.), and herbaceous plants
such as gingers (Zingiber spp.) and ferns, including tree
ferns (Cyathea spp.). Wild banana (Musa spp.) and figs
(Ficus spp.) were uncommon. In open and recently eroded
sections of the river banks, erect pandans (Pandanus spp.),
cogon (Imperata cylindrica) and saw grass (Saccharum
spontaneum), were abundant. Leaf litter on the forest floor
was light, with accumulations of 2–3 cm around tree trunks,
and scattered patches of humus did not exceed 2 cm.
Because 2 of the 4 days of our trapping here coincided with
heavy rain, we do not believe our sampling at this site was
sufficient, and so the data from this site were excluded from
detailed analysis.
� Site 2. Lower Ugbog, 6 km W, 2 km S Tapulao peak, 925m
elev., 15127045.700N, 120103058.800E (14–19 January 2005).
This locality was situated along an old mining road that led
directly to an abandoned bunkhouse at ca. 1750m on Mt.
Tapulao. Vegetation was secondary lowland dipterocap
forest but showed more disturbance and signs of recent
timber poaching than Site 1. The canopy reached ca. 20m,
with composition and structure of forest tree and forest
floor vegetation similar to Site 1, but large, emergent
Agathis were rare. Climbing bamboo was similarly abun-
dant, but jade vines were less common. Pandanus was
ARTICLE IN PRESS
Fig. 1. Map of Mount Tapulao, showing the location of study areas in 2004 and 2005, indicated by encircled numbers. Locality
numbers as in text. Inset map of Luzon Island shows location of Mt. Tapulao.
D.S. Balete et al. / Mamm. biol. 74 (2009) 456–466458
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thicker here than at Site 1 and figs were more common.
Ferns and cogon were abundant along the sides of the road.
Amounts of leaf litter and humus were similar to Site 1.
� Site 3. Upper Ugbog, 4 km W, 2.5 km S Tapulao peak,
1200m elev., 15127042.200N, 120105002.300E (23–27 March
2004). This site lay along an old mining road; near the road
were small clearings dominated by grasses or planted with
sweet potato, taro and a few bananas, including an area
where a demolished building of a mining company once
stood. The rest of the site was lightly disturbed lower
montane forest with a canopy of ca. 15–17m. Several old
tree stumps suggested this area was logged in the past.
Common trees included species of Myrtaceae, Fagaceae,
and Lauraceae. Fewer emergents, mainly Agathis, were
present. Rattans and pandans were abundant in the
understory. As at Sites 1 and 2, climbing bamboos and
jade vines were the most abundant canopy vines, sometimes
covering entire crowns of trees. Leaf litter was more
abundant than at lower sites, and humus was a bit thicker
and covered wider but scattered spots. Ferns and herbac-
eous plants such as gingers were common on the forest
floor. Cogon, fruiting figs, ground ferns and tree ferns were
also common along the mining road.
� Site 4. Pulta Mayor, 1.5 km W, 1.6 km S Tapulao peak,
1680m elev., 15128003.000N, 120106025.200E (30 March–02
April 2004). This locality was situated on a ridge-top along
the old mining road, marked by abandoned stockpiles of
chromite ore. The forest away from the road was mature
upper montane forest, consisting mainly of Myrtaceae and
Fagaceae, with a canopy of ca. 10–12m, and emergents of
up to 15m (Fig. 3). Climbing bamboos were abundant and
covered much of the canopy, especially near the mining
road. Climbing pandans were present but uncommon. In
the understory, rattans, erect palms (Pinanga sp.) and tree
ferns were moderately common. Large rocks were scattered
on the forest floor. On both sides of the mining road, the
forest was highly disturbed and some areas showed signs of
recent burning. In disturbed areas adjacent to the forest,
erect bamboos (Bambusa sp.) were abundant while pine
trees as well as cogon were common closer to the road.
Amounts of leaf litter and humus were similar to Site 3.
This site was close to an abandoned bunkhouse situated at
the side of a very steep slope, surrounded entirely by pine
trees up to 20m tall and with DBH of up to 50 cm. A small
spring below the bunkhouse was the only source of water.
� Site 5. 0.15 km W, 0.02 km N Tapulao peak, 2024m elev.,
15128054.800N, 120107010.400E (05–13 January 2005). This
site lies along the trail that branches northwest of the old
mining road and ends at the peak of Mt. Tapulao, ca.
2037m. Our campsite was situated on a flat, grassy area
below the peak, covered with a mix of grasses (Imperata
cylindrica and Saccharum spontaneum), shrubs (Rubus spp.)
and stunted trees no taller than 2m, such as Syzygium spp.
(Myrtaceae), Vaccinium spp. (Vacciniaceae), and Ficus spp.
(Moraceae), as well as species of Theaceae and at least two
flowering members of Compositae (Fig. 4). A few pine
saplings also were present. The condition of the area
indicated that it had been cleared in the past. The forest
surrounding the campsite was old-growth mossy forest. The
trees were small and stunted, with a canopy of ca. 5–7m,
and a few emergents reaching ca. 10m. Canopy trees
consisted mainly of Syzygium spp. and Leptospermum spp.
(Myrtaceae), Lithocarpus spp. (Fagaceae), and Podocarpus
spp. (Podocarpaceae) along with members of Lauraceae
and Elaeocarpaceae. Many trees had gnarled trunks thickly
covered with mosses and liverworts. Epiphytic orchids and
ferns were common on tree trunks and branches. Climbing
pandans were abundant and the most common vine on tree
trunks, even extending above the crowns of emergents.
Understory vegetation included species of Ericaceae (Rho-
dodenron spp.), Melastomataceae (Medinilla spp.), Thea-
ceae (Camelia spp., Eurya spp., etc.), Vacciniaceae
(Vaccinium spp.) and Winteraceae (Drymis sp.). Stunted
Terminalia sp. (Combretaceae) was also observed. The
ground was relatively dry and only moderately covered
with mosses; leaf litter was 3–5 cm thick and fairly
continuous, and the humus layer was 2–3 cm thick, above
a layer of volcanic ash (from the Mt. Pinatubo eruption of
1991) of about equal thickness.
Trapping procedures
This study followed field methods employed in our previous
surveys of small mammals in the Philippines (Heaney et al.
1989, 1999, 2006; Rickart et al. 1991, 1993). Victor rat traps,
Museum Special snap traps, and National live traps were used
to capture rodents and shrews. For trapping on the ground
surface, traps were placed under root tangles, in front of
burrow entrances, along runways, and beside or on top of
fallen logs. Traps were baited with either live earthworms or
with fried coconut coated with peanut butter. For above-
ground trapping, Museum Specials were set on horizontal
branches of trees, crisscrossing vines of climbing pandans
(Freycinetia) and climbing bamboos (Dinochloa), or over-
hanging lianas; all arboreal traps were baited with fried
coconut coated with peanut butter. All traplines were
maintained for 3 days and serviced regularly twice each day,
early in the morning (after sunrise, ca. 700 h) and in the late
afternoon (before sundown, ca. 1700 h) to retrieve captures
and to replace bait. Within each locality, we sampled several
sites to include ridge-tops, upper and lower ridge sides, and
any other evident variation in habitat.
The adequacy of sampling of the non-flying small mammals
was gauged by calculating species accumulation rates for each
sampling locality and for the transect as a whole. This is the
best indicator of the completeness of sampling for species
richness of small mammals in any place where pre-existing
information is limited or absent, as in much of the Philippines
(Heaney 2001, Heaney et al. 1999, 2006; Rickart et al. 1991).
When possible, trapped animals were released at the site of
capture; only those animals with certain identifications were
released. Voucher specimens were measured, examined for
reproductive condition, and either preserved as complete
bodies in formalin (transferred to ethanol) or prepared as
complete skeletons. Vouchers have been deposited at the Field
Museum of Natural History, Chicago (FMNH); a portion will
be transferred to the National Museum of the Philippines,
Manila (NMP). The capture and handling of animals in the
field was conducted in accordance with guidelines for animal
care and use established by the American Society of
Mammalogists (Gannon et al. 2007).
ARTICLE IN PRESSD.S. Balete et al. / Mamm. biol. 74 (2009) 456–466 459
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Data analysis
Results of the survey are presented in Table 1, including
those individuals that were released. In three cases, we infer the
presence of a particular species at a given elevation because of
its documented presence at trapping sites above and below
along the transect (Rickart et al. 1991). We report the total
number of trap-nights (defined as one trap set for 24 h), the
number of traps placed on the ground with earthworm or
coconut bait, and the number of traps with coconut bait placed
arboreally (Table 2). Trap success (Table 2) was derived for
each species at each study site by bait type, as the number of
individuals of each species captured with the relevant bait
divided by the corresponding number of trap-nights that the
bait used� 100 (i.e., the number of captures per 100 trap-
nights). Bait preference of each species was derived in similar
fashion, expressed as the value of their total captures per bait
type divided by the relevant total of trap-nights for the bait
used� 100, and presented under the total column in Table 2.
Weighted relative abundance of each species at each site
(Table 3) was calculated as the number of individuals captured
divided by the total number of traps set (either on the ground
or in the trees, depending on whether the species is terrestrial
or arboreal)� 100. Thus, for Apomys sp. 1, which lives only on
the ground, we did not include arboreal traps in this
calculation. The unweighted value of the same parameter
was expressed as the average of each species’ trap success for
the two bait types used, as presented in Table 2. Similarly, for
chi-square tests of diel activity, bait preference, and arbore-
ality, we used only the number of trap-nights that was relevant
to that species. Linear regressions were calculated with an HP
15C hand-held calculator; chi-square tests were run using
Excel.
Results
Our survey documented 11 species of non-flying smallmammals on Mt. Tapulao, consisting of 2 shrews and 9murid rodents (excluding the giant cloud rat Phloeomys
pallidus, which we treat as a large mammal; Table 1).A species accumulation curve for the nine nativespecies documented during the entire survey (Fig. 2A)shows a gradual rise in the number of species as weadded localities along the transect, and as we ap-proached a total of 2000 trap-nights. The long plateauafter 2000 trap-nights, the fact that we obtained three ormore individuals of each species, and our success insampling in all major habitats, indicates that weprobably obtained all of the species of native non-volant small mammals on Mt. Tapulao at 925melevation and above. Species accumulation curves forindividual sites (Fig. 2B) also showed some evidence ofreaching plateaus, except at Site 1 (860m), which weexclude from analyses because heavy rain prevented acomplete site survey. Although some species may havebeen missed at individual sites, these curves suggest thatour data represent reasonable estimates of overallspecies richness.
ARTICLE IN PRESS
Table 1. Mammals documented on Mt. Tapulao, Zambales Province, Luzon Island in 2004 and 2005 surveys
Scientific name English name Site and elevation (m) Total
1 2 3 4 5
860 925 1200 1690 2024
Crocidura grayi Luzon shrew 0 2 P P 18 20
Suncus murinus Asian house shrew 3 P 2 1 0 5
Apomys sp. 1 Large forest mouse 6 21 37 50 0 114
Apomys sp. 2 Large forest mouse 0 0 0 0 35 35
Apomys microdon Small Luzon forest mouse 0 0 0 0 9 9
Apomys musculus Least Philippine forest mouse 0 0 0 0 6 6
Bullimus luzonicus Large forest rat 0 3 2 4 0 9
Chrotomys mindorensis Striped shrew-rat 0 2 P 2 2 6
Rattus everetti Common Philippine forest rat 4 10 6 4 2 26
Rattus exulans Spiny ricefield rat 0 2 1 1 0 4
Rhynchomys tapulao Zambales shrew-rat 0 0 0 0 3 3
Total captures 13 40 48 62 75 238
No. of trap-nights (ground traps, coconut bait) 240 369 344 329 413 1695
No. of trap-nights (ground traps, earthworm bait) 200 280 312 162 483 1437
No. of trap-nights (arboreal traps, coconut bait) 0 257 46 0 284 587
Overall trap success (weighted by bait type) – 10.4 10.7 11.3 10.7 –
Overall trap success (unweighted by bait type) – 6.4 6.7 13.7 8.1 –
Total No. of native small mammals 2 5 3+2 4+1 7 9
0 ¼ absent, P ¼ presumed present, based on occurrence below and above a study site. The total number of species is the number documented plus
those presumed present.
D.S. Balete et al. / Mamm. biol. 74 (2009) 456–466460
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Studies of the shrew rat, Rhynchomys, show that thespecimens from Tapulao are most similar to northernLuzon shrew-rats, R. soricoides, from the CentralCordillera, but are sufficiently different to warrantrecognition as a distinct species, R. tapulao (Balete etal. 2007). Genetic and morphological studies of the largeApomys from Tapulao have revealed two distinct formsthat we believe represent undescribed species, hereinreferred to as Apomys sp. 1 and 2 (Heaney et al. inpreparation). We note that two of these endemic species(R. tapulao and Apomys sp. 2) were found only at ourhighest site (2024m), near the peak, in mossy forest; theother Zambales endemic species (Apomys sp. 1) wastaken from 860 to 1690m, in both lowland and montanerain forest.
Species richness for Site 1 is excluded from ouranalyses because heavy rains prevented complete sam-pling at this site. Nonetheless, we know that at least twonative (Apomys sp. 1 and Rattus everetti) and one non-native species (S. murinus) were present. At Sites 2–4,five native species were documented or inferred ateach site; and at Site 5, seven species were documented(Table 1). This increase in species richness withincreasing elevation, though not statistically significant,follows a general pattern seen on Mt. Isarog insoutheastern Luzon, the Balbalasang area in the CentralCordilleras, and Mt. Kitanglad on Mindanao (Heaney2001; Heaney et al. 1999, 2003, 2005, 2006; Rickart et al.1991).
Total relative abundance (unweighted, measuredas the number of small mammals captured per 100trap-nights, standardized to equal numbers ofearthworm and coconut baits; Table 3) showed asubstantial increase from 6.43 in the lowlandforest (Site 2) and 6.70 in the lower montane forest(Site 3) up to 13.66 in the upper montane forest(Site 4, Fig. 3). In mossy forest (Site 5, Fig. 4), relativeabundance dropped to 8.08. The correlation betweenelevation and abundance is not statistically significant,but this probably reflects the small number of sitesand the fact that the underlying pattern appears to becurvilinear.
Most individual species were captured in numbers toolow to allow reliable estimates of their relative abun-dances along the elevational gradient. However, for thetwo most abundant species, we see strong but opposingeffects of elevation (Table 3). For one of the largeApomys (sp. 1), there was a significant increase in trapsuccess with elevation, with relative densities of 3.45(925m, Site 2), 5.51 (1200m, Site 3), and 11.83 (1680m,Site 4) individuals per 100 trap-nights (r ¼ 0.999,Po0.05). In contrast, R. everetti showed a significantdecline in trap success with elevation, with relativedensities of 1.67 (925m, Site 2), 1.13 (1200m, Site 3),0.62 (1680m, Site 4), and 0.24 (2024m, Site 5)individuals per 100 trap-nights (r ¼ �0.934,
ARTICLE IN PRESSTable
2.
Capture
bybaittypefornativenon-volantsm
allmammalsalongtheelevationaltransect
onMt.Tapulao
Species
Elevation(m
)Total
925
1200
1690
2024
Coco
Worm
Coco
Worm
Coco
Worm
Coco
Worm
Coco
Worm
Co
cidu
rag
ray
i0[358]0
2[227](0.88)
00
00
1[359](0.28)
17[479](3.55)
1[717](0.14)
19��
[706](2.69)
Ap
om
ys
mic
rod
on
00
00
00
9[643](1.40)
0[479]0
9[643](1.40)
0[479]0
Ap
om
ys
mu
scu
lus
00
00
00
4[359](1.11)
2[479](0.42)
4[359](1.11)
2[479](0.42)
Ap
om
yssp.1
7[369](1.90)
14[280](5.00)
28[344](8.14)
9[312](2.88)
23[329](6.99)
27[162](16.67)
00
58[1042](5.57)
50[754](6.63)
Ap
om
yssp.2
00
00
00
17[413](4.11)
18[483](3.73)
17[413](4.11)
18[483](3.73)
Bull
imus
luzo
nic
us
1[369](0.27)
2[240](0.83)
2[344](0.58)
0[312]0
4[329](1.22)
0[162]0
00
7[1042](0.67)
2[714](0.28)
Ch
roto
my
sm
indo
rensi
s1[369](0.27)
1[240](0.42)
00
0[329]0
2[162](1.23)
0[377]0
2[483](0.41)
1[1075](0.09)
5[885](0.56)
Ratt
us
ever
etti
6[369](1.63)
4[240](1.67)
4[344](1.62)
2[312](0.64)
4[329](1.22)
0[162]0
1[377](0.26)
1[483](0.21)
15[1419](1.05)
7[1197](0.58)
Rh
yn
cho
my
sta
pu
lao
00
00
00
1[377](0.26)
2[483](0.41)
1[377](0.26)
2[483](0.41)
Trap-nights
are
shownin
brackets,standardized
capturesper
100trap-nights
inparentheses.See
Methodssectionfordetailsoncalculatingthesevalues.Probabilitiesare
forw2
tests.
��Po0.01.
D.S. Balete et al. / Mamm. biol. 74 (2009) 456–466 461
Author's personal copy
0.05oPo0.10). Thus, the overall trend in relativeabundance is composed of several different individualtrends.
Native species of small mammals differed in theirelevational distributions (Table 1). Rattus everetti wasthe only species recorded across the entire samplinggradient, but several others were also broadly distrib-uted. Crocidura grayi and Chrotomys mindorensis were
captured or inferred to be present at all but the lowestelevation site, but absence there may simply reflectincomplete sampling. Apomys sp. 1 was recorded at allsites except the highest elevation site in mossy forest,whereas Bullimus luzonicus was absent at both highestand lowest elevations. Four native species appear to berestricted to the highest elevation (Site 5, Fig. 4),including Apomys sp. 2, A. microdon, A. musculus, and
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Table 3. Relative abundance (individuals/100 trap-nights) and diel activity patterns of native, non-volant small mammals along the
elevational transect on Mt. Tapulao
Species Elevation (m) Diel period
925 1200 1690 2024 Nocturnal/crepuscular Diurnal
Cocidura grayi 0.44 (0.34) 0 0 1.92 (2.15) 14 6
Apomys microdon 0 0 0 0.70 (0.80) 9�� 0
Apomys musculus 0 0 0 0.76 (0.72) 6� 0
Apomys sp. 1 3.45 (3.24) 5.51 (5.64) 11.83 10.18) 0 106��� 2
Apomys sp. 2 0 0 0 3.92 (3.91) 34��� 1
Bullimus luzonicus 0.55 (0.49) 0.29 (0.30) 0.62 (0.81) 0 9�� 0
Chrotomys mindorensis 0.33 (0.34) 0 0.61 (0.41) 0.20 (0.23) 1 4�
Rattus everetti 1.67 (1.65) 1.13 (0.91) 0.62 (0.81) 0.24 (0.23) 22��� 0
Rhynchomys tapulao 0 0 0 0.34 (0.35) 0 3��
All species 6.43 (6.04) 6.70 (6.86) 13.66 (12.22) 8.08 (8.39) 197 18
In each block under elevation the upper value is the unweighted capture rate, and the lower value (in parentheses) is the weighted capture rate (see
Methods section). Captures and trapping effort per species as in Table 2. Probabilities are for w2 tests.�Po0.05.��Po0.01.���Po0.001.
Fig. 2. Species accumulation curves for (A) all field survey locations on Mt. Tapulao and (B) individual field location on Mt.
Tapulao. Each symbol represents 1 day of trapping (see Methods section).
D.S. Balete et al. / Mamm. biol. 74 (2009) 456–466462
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Rhynchomys tapulao. This is consistent with previousstudies that have found distinctive communities of smallmammals in mossy forest (Heaney 2001; Heaney et al.1999, 2005, 2006; Rickart et al. 1991). The two non-native species, Suncus murinus and Rattus exulans, bothhad relatively broad elevational distributions but werenot found in mossy forest at Site 5.
We captured Crocidura grayi, all four species ofApomys, Bullimus luzonicus, Chrotomys mindorensis, andRattus everetti in disturbed areas near the mining roadwhere natural vegetation was regenerating, indicatingthat most of the native small mammal species on thisgradient exhibit some tolerance for habitat disturbance.Eight of nine specimens of Apomys microdon werecaptured in traps set above ground, on climbing
pandans and bamboo (Freycinetia and Dinochloa)tangles on trees, demonstrating significant arborealtendencies (w2 ¼ 14.37; Po0.001). All other specieswere captured exclusively on the ground; chi-squaretests were significant for all species with samples of nineor more.
Significant bait preference was observed only inCrocidura grayi, which were caught in higher numberswith earthworm bait than with coconut (w2 ¼ 8.18,P ¼ 0.004). For members of other genera that oftenshow strong bait preference (e.g., Chrotomys for earth-worms and Bullimus for coconut) our sample sizes weretoo small to show statistical significance.
Capture data revealed clear differences in diel activitypatterns of species (Table 3). The two vermivorous
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Fig. 3. Upper montane forest at 1680m, showing Syzygium (Myrtaceae) and Lithocarpus (Fagaceae) (tall trees at the background)
and grassy edge of sawgrass (Saccharum spontaneum) and cogon (Imperata cylindrica) at the foreground. Note at the background the
presence of Pinus merkusii (left), as well as tree fern, Cyathea (center), and climbing bamboos, Dinochloa, on top of vegetation
(right).
Fig. 4. Mossy forest at 2024m (background), showing emergents over canopy (left), consisting of Syzygium (Myrtaceae) and
Lithocarpus (Fagaceae). Note the climbing pandans (Freycinetia) towering over the canopy at the center to far right at the
background. Foreground shows grassy patch (Saccharum spontaneum) at the edge of the forest together with Pinus merkusii,
Leptospermum sp., and Rubus spp.
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shrew-rats, Chrotomys mindorensis and Rhynchomys
tapulao, had significantly more diurnal than nocturnalcaptures (w2 ¼ 4.23, P ¼ 0.038 and w2 ¼ 4.2, P ¼ 0.040,respectively). Crocidura grayi showed no significant dielpattern (w2 ¼ 1.12, P ¼ 0.290), but from the relativelylarge sample, this clearly indicates activity duringboth day and night. All other species showed signi-ficant nocturnal activity (Apomys sp. 1, w2 ¼ 70.4,Po0.0001; Apomys sp. 2, w2 ¼ 21.69, Po0.001; A.
microdon, w2 ¼ 6.43, P ¼ 0.011; A. musculus, w2 ¼ 4.28,P ¼ 0.0384; B. luzonicus, w2 ¼ 6.43, Po0.011; R. ever-
etti, w2 ¼ 15.71, Po0.001). Of these species, Apomys sp.1 and Apomys sp. 2 had daytime captures of two andone individuals, respectively; all others were exclusivelynocturnal. These diel patterns are similar to thosereported for related species elsewhere (e.g., Heaney etal. 1989, 1999, 2006; Rickart et al. 1991).
We captured two invasive, alien species: the Asianhouse shrew (Suncus murinus), a widespread commensalspecies, and the spiny ricefield rat (Rattus exulans), acommon agricultural pest (Table 1). At Sites 2–4, wecaptured small numbers of both species in heavilydisturbed habitat along the old mining road dominatedby grasses and ferns. One specimen of S. murinus wascaptured in disturbed forest at Site 1. Near Site 4, weobserved several rodents inside and underneath anabandoned bunkhouse. Although we did not captureany, we visually identified them as either Rattus exulans
or R. tanezumi, the Asian house rat. Alien species werenot recorded in mature or high-quality regeneratingforest habitat along the study transect. The remainingnine species of small mammals that we recorded(Table 1) are Philippine natives that are associated withforest habitats.
Discussion and conclusions
Our survey of Mt. Tapulao provides the first extensivedata on the non-volant mammals of the ZambalesMountains. Of the nine species of native smallmammals documented, Rhynchomys tapulao isendemic, and our taxonomic studies indicate that twospecies of Apomys also are new to science and arelikewise endemic to the region. It is clear that theZambales Mountains represent a distinctive and pre-viously unrecognized center of mammalian diversity,comparable to Mt. Isarog, also a small mountainthat has three endemic species (Heaney et al. 1999;Rickart et al. 1991).
On Mt. Tapulao we documented an increase in speciesrichness from five, at the three lower sites, to seven at thesite nearest the top of the mountain (Table 1). While thistrend does not show a statistically significant correlationwith elevation, it is clearly not consistent with theprediction of a mid-domain effect, which requires a peak
in species richness near the center of the elevationalgradient (Colwell et al. 2004, 2005; McCain 2004, 2005,2007). In contrast, the documented pattern is consistentwith the prediction of maximum species richnessin the lowest portions of mossy forest, which onMt. Tapulao begins at about 1800m, near the peak.Because of the limitations of this study (particularly,little forest to sample below 800m, and an inadequatesample at 860m because of heavy rains), we do notconsider our data to constitute a strong test of themid-domain effect hypothesis. However, our results areclearly not consistent with that hypothesis, but aresupportive of the alternative ecologically based hypoth-esis. These results are very similar to those fromMt. Isarog and Mt. Bali-it (Heaney et al. 1999, 2005;Rickart et al. 1991) and add to the accumulatingevidence that will, in due course, provide a strong testof both hypotheses.
We further note that relative abundance onMt. Tapulao (Table 3) increased steadily from thelowest reliable site, in lowland forest at 925m, tomontane forest at 1690m, and then declined at 2024m.This is generally consistent with our earlier observationsof a correlation between species richness and total smallmammal abundance (Heaney 2001; Heaney et al. 1989,1999, 2006; Rickart et al. 1991). Overall, our data(Tables 1–3) suggest a shift with increasing elevationfrom granivore/omnivores to an increasing percentageof vermivores, and from nocturnal to diurnalspecies (i.e., a shift from abundant Apomys sp. 1 andRattus everetti at the lower elevations, to more abun-dant Crocidura grayi, Chrotomys mindorensis, andRhynchomys tapulao at higher elevations). These dataare also consistent with the hypothesis that the increasein species richness is associated with a shift from awarmer, drier climate at lower elevations to a cooler,wetter climate in the lower mossy forest (Heaney 2001;Rickart et al. 1991).
While the Zambales shrew rat (Rhynchomys tapulao)was not recorded outside of undisturbed mossy forest,all other native species, including the endemic species ofApomys, were caught in both undisturbed and indisturbed forest, and some also were taken in grassysecond growth at forest edges. This demonstrates thatmost of these native small mammals can tolerate at leastsome habitat disturbance. The presence of two alieninvasive species, Suncus murinus and Rattus exulans, isan indicator of habitat disturbance along the studygradient. Indeed, our study sites followed the miningroad that led up to ca. 1800m on Mt. Tapulao. Acrossthe entire transect, we noted both mining-relateddisturbance and the attendant habitat disturbance andforest clearing associated with an influx of people usingthe access road, including hunting and timber poaching.The same alien species have been recorded in similarhabitat conditions on other mountains in Luzon,
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including Mt. Isarog in Camarines Sur province and Mt.Bali-it in Kalinga province (Heaney et al. 1999, 2005).However, on Mt. Tapulao, these alien species werenot recorded in the forest interior, despite the factthat forests there had been disturbed. Thus, the nativespecies have maintained their presence in the faceof past habitat disturbance and do not show anysigns of being displaced by the alien species. Theinability of alien species to penetrate either primary ordisturbed but regenerating forest habitats has beenobserved elsewhere in the Philippines, on Mt. Isarog inBicol, Mt. Pangasugan on Leyte, and the Mt. Bali-itarea of Kalinga Province (Heaney et al. 1989, 1999,2005, 2006; Rickart et al. 1991, 1993). We believethat resistance to invasion is, in part, a function ofnative diversity. Heaney et al. (1999) hypothesizedthat on oceanic islands, the success of invasion bynon-native small mammals is determined by the numberof species in the native community of small mammals.Results of the Tapulao survey clearly support thishypothesis.
Our data show that the disturbed lowland forestsupports more than half of the native non-flyingsmall mammals of Mt. Tapulao. While many speciesshow a high level of tolerance to habitat disturbance,we believe that the large mammals are the mostseriously threatened species due to the combination ofhabitat loss and hunting pressure. Lowland forest isthe most heavily exploited and severely reduced vegeta-tion type in the Philippines due to the presence ofcommercially important tree species, especially thedipterocarps, and their proximity to human settlements.On Mt. Tapulao, extensive logging during the last fewdecades has substantially reduced lowland forest.Although regeneration is occurring in some areas,on-going timber poaching, clearing for gardens, andmining activities continue to threaten the remaininglowland forest.
Based on the data presented here, we stronglyrecommend the protection of the remaining forest ofMt. Tapulao and the sustainable management ofresources to protect its many unique and highly diversemammals, among other wildlife (e.g., Brown et al.1996; Mallari et al. 2001; Ruedas et al. 1994). Our datafurther suggest that in order for this biodiversityto be protected in perpetuity, all habitat types, fromdisturbed and regenerating lowland forest to primarymossy forest, must be included in any protectionprogram. Prompt protection of the remaining forest,including the disturbed and regenerating lowlandforest, will ensure the conservation of this uniqueassemblage of mammals in the Philippines, as well asprotecting the headwaters of many of the mostimportant rivers that provide water to the cities of bothZambales Province and the Central Plains of Pampanga,Pangasinan, and Tarlac.
Acknowledgements
Our initial efforts to conduct this survey were stronglyencouraged and supported by Philip Camara and BlasTabaranza; we offer thanks to both for their supportand hospitality. We thank Joel Sarmiento, RolandoCereno and sons, Rodolfo Florentino, Romulo Tamayoand sons, Jimmy Tawataw, and the people of BarangayDampay-Salaza who provided assistance with fieldwork. The Department of Environment and NaturalResources provided encouragement and permits for allof our activities; we especially thank Director MunditaLim, Carlo Custodio, and Antonio Manila of theProtected Areas and Wildlife Bureau, and CENRO L.Ignacio of Masinloc, for their efforts to make thisresearch possible. The figures were prepared byL. Kanellos. We thank J. Phelps, M. Schulenberg, andW. Stanley for assistance with curation of the specimens,and P. Sierwald for providing the German summary.N. R. Ingle, J. Sedlock, and an anonymous reviewerprovided comments that improved earlier drafts of themanuscript. Funding was provided by the BarbaraBrown, Ellen Thorne Smith, and Marshall Field Fundsof the Field Museum, and a grant from the GraingerFoundation.
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