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Habitat Disturbance and the Ecology of Small Mammals in the Philippines

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 Diversity and Distributions, (Diversity Distrib.) (2011) 17, 530–541
A Journal of Conservation Biogeography
BIODIVERSITY Mammals of the northern Philippines:
RESEARCH
tolerance for habitat disturbance and
resistance to invasive species in an
endemic insular fauna
Eric A. Rickart1*, Danilo S. Balete2, Rebecca J. Rowe1 and Lawrence
R. Heaney2

1
Utah Museum of Natural History, University ABSTRACT
of Utah, Salt Lake City, UT 84112, USA,
2 Aim Island faunas, particularly those with high levels of endemism, usually are
Division of Mammals, Field Museum of
Natural History, 1400 S Lake Shore Drive,
considered especially susceptible to disruption from habitat disturbance and
Chicago, IL 60605, USA invasive alien species. We tested this general hypothesis by examining the
distribution of small mammals along gradients of anthropogenic habitat
disturbance in northern Luzon Island, an area with a very high level of
mammalian endemism.
Location Central Cordillera, northern Luzon Island, Philippines.

Methods Using standard trapping techniques, we documented the occurrence

and abundance of 16 endemic and two non-native species along four disturbance
gradients where habitat ranged from mature forest to deforested cropland. Using
regression analysis and AICc for model selection, we assessed the influence of four
predictor variables (geographic range, elevational range, body size and diet
breadth) on the disturbance tolerance of species.
Results Non-native species dominated areas with the most severe disturbance
and were rare or absent in mature forest. Native species richness declined with
Diversity and Distributions

increasing disturbance level, but responses of individual species varied.

*Correspondence: Dr Eric A. Rickart, Utah
Museum of Natural History, University of
Utah, Salt Lake City, UT 84112, USA.
E-mail: rickart@umnh.utah.edu
Elevational range (a measure of habitat breadth) was the best predictor of
response of native species to habitat disturbance. Geographic range, body size and
diet breadth were weakly correlated.
Main conclusions The endemic small mammal fauna of northern Luzon includes
species adapted to varying levels of natural disturbance and appears to be resistant
to disruption by resident alien species. In these respects, it resembles a diverse
continental fauna rather than a depauperate insular fauna. We conclude that the
long and complex history of Luzon as an ancient member of the Philippine island
arc system has involved highly dynamic ecological conditions resulting in a biota
adapted to changing conditions. We predict that similar responses will be seen in
other taxonomic groups and in other ancient island arc systems.
Keywords
Biogeography, disturbance tolerance, endemic species, habitat disturbance
gradients, invasive species, island faunas.

especially sensitive to anthropogenic habitat changes (Fordham

INTRODUCTION
Oceanic islands exhibit high levels of endemism across a wide
range of taxa (Whittaker & Fernández-Palacios, 2007; Kier
et al., 2009), and island endemics typically are considered
& Brook, 2010). Accordingly, concern for insular faunas is
especially great (Ceballos & Brown, 1995; Ricketts et al., 2005;
Amori et al., 2007). Deforestation is the primary threat to
biodiversity on tropical islands (Brooks et al., 1999; Sodhi

DOI:10.1111/j.1472-4642.2011.00758.x
530 http://wileyonlinelibrary.com/journal/ddi ª 2011 Blackwell Publishing Ltd
 Habitat disturbance & Philippine mammals

et al., 2004; Butchart et al., 2010). However, invasive species

pose an additional threat to native faunas that may be
exacerbated by habitat disturbance (Sax et al., 2005; Corlett,
2010). Island faunas are often especially vulnerable to non-
indigenous invasive species (Berglund et al., 2009) and insular
small mammals, in particular, to non-native rodents (Harris,
2009).
The mammalian fauna of the Philippines constitutes one of
the foremost examples of mammalian diversification within an
ancient oceanic archipelago (Heaney & Rickart, 1990; Steppan
et al., 2003; Jansa et al., 2006). For an area of its size, the
Philippines also has one of the highest levels of mammalian
endemism in the world. The most recent published faunal
synopsis (Heaney et al., 1998) lists 99 native non-volant
species, of which 85 (86%) are endemic. Subsequent discov-
eries and taxonomic revisions by the authors and colleagues
have increased these numbers to 103 and 93 (90%), and c. 25
additional species await description.
Habitat loss poses the greatest threat to biodiversity in the
Philippines, where primary forest cover has declined from
c. 70% of the total land area to c. 7% during the 20th century
(Heaney & Regalado, 1998), and both human population
density and growth rate are very high (Cincotta et al., 2000).
Invasive species are also a major problem and include several
species of non-native mammals, some of which may invade
Figure 1 Map of Luzon Island, Philippines, showing location of
forests (Heaney et al., 1998). The combination of exceptional
four disturbance gradients in the Central Cordillera region.
endemism and severe environmental degradation makes the
Philippines a high priority for global conservation (Heaney
et al., 1999; Myers et al., 2000). 12103¢ E, 925–2150 m), Mt. Data National Park, Mountain
We have surveyed mammals throughout the Philippines to Province (1622¢ N, 12052¢ E, 2228–2310 m) and Mt. Pulag
assess patterns of species richness and relative abundance National Park, Benguet Province (1634¢ N, 12052¢ E, 2285–
across local elevational gradients (Heaney et al., 1989, 2006a; 2850 m). In each area, we surveyed mammal communities at
Rickart et al., 1991, 2011; Balete et al., 2009). Most areas where multiple localities where habitat ranged from mature forest to
we have worked have had varying levels of past or ongoing deforested cropland, providing four replicate gradients of
anthropogenic habitat disturbance from logging or agriculture, habitat disturbance.
allowing us to make qualitative observations on the responses Our study involves small (< 500 g) rodents (family Muri-
of both native and non-native species to disturbance (Rickart, dae) and shrews (Soricidae), including 16 native and two non-
1993; Ong & Rickart, 2008). Here, we present quantitative native species (Table 1). The native non-volant mammals of
analyses of the occurrence and abundance of native and non- Luzon are all endemic to the Philippines, but the extent of their
native small mammals across four gradients of habitat geographic distributions vary. Several species are restricted to
disturbance in northern Luzon. Using multimodel analysis, the Central Cordillera region, some occur beyond the Cordil-
we assess the relative importance of four ecological and lera but are restricted to the Luzon faunal region, and others
distributional traits (geographic range, elevational range, body occur more broadly among islands that are within the oceanic
size and diet breadth) as potential drivers of disturbance portion of the Philippines (Heaney et al.,1998). Most of the
tolerance of native and non-native species. We also discuss the native rodents belong to two indigenous clades (Jansa et al.,
capacity of native species to occupy regenerating habitat and 2006; Heaney et al., 2009). One clade is represented by four
the conditions under which non-native species become estab- arboreal or scansorial species belonging to the genera Batomys,
lished. Carpomys and Musseromys. The second, which includes
members of the vermivorous ‘shrew-rat’ genera (Archboldomys,
Chrotomys and Rhynchomys) together with native mice (Apo-
METHODS
mys), is represented by nine species. Both clades are very
Between 2000 and 2008, we conducted trapping surveys of ancient, with molecular clock estimates of 15–20 Mya for their
small mammals in four study areas in the Central Cordillera of arrival in the Philippines (Jansa et al., 2006). Bullimus
northern Luzon Island (Fig. 1): Mt. Amuyao, Mountain luzonicus and Rattus everetti are native rodents belonging to
Province (1701¢ N, 12107¢ E, 1520–2690 m elevation), Bal- much younger clades of c. 3–5 Mya (Jansa et al., 2006). The
balasang-Balbalan National Park, Kalinga Province (1727¢ N, one native shrew, Crocidura grayi, belongs to an endemic clade

Diversity and Distributions, 17, 530–541, ª 2011 Blackwell Publishing Ltd 531
E. A. Rickart et al.

Table 1 Species attributes, occurrence patterns and habitat disturbance scores for small mammals on four gradients in northern Luzon,
Philippines.

Total number of individuals– (n) and disturbance scores (S)

All
Mt. Amuyao Balbalasang Mt. Pulag Mt. Data gradients
Geographic Elevation Body Diet
range km2 * range (m)  sizeà breadth§ n S n S n S n S n S

Native species
Apomys abrae 8768 1400 62 4 26 2.42 105 2.35 8 3 139 2.59
Apomys datae 6372 1200 82 4 211 1.21 380 1 226 2.18 86 2 903 1.6
Apomys microdon 106533 700 25 3 3 1.51 3 1.51
Apomys musculus 114917 740 22 3 9 1.14 6 1 7 2.29 7 2 29 1.61
Archboldomys kalinga 4215 1090 25 2 9 1.26 21 1 1 2 9 2 40 1.56
Archboldomys sp. 83 805 45 2 13 1.13 13 1.13
Batomys granti 3773 880 178 3 10 1 6 1 3 2 19 1.33
Bullimus luzonicus 105065 1690 475 4 10 1.81 5 1.27 7 2.26 27 2.36 49 1.92
Carpomys Insufficient Insufficient 165 3 1 2 1 2
melanurus data data
Carpomys Insufficient Insufficient 123 3 1 1 1 1
phaeurus data data
Chrotomys silaceus 4215 1000 122 1 44 1.11 9 1 33 2.03 86 1.38
Chrotomys whiteheadi 4215 1840 125 1 22 2.99 33 2.26 27 2 82 2.42
Crocidura grayi 116385 1250 10 2 52 1.35 27 1 15 2.45 5 2.59 99 1.85
Musseromys sp. 951 745 19 3 4 1 3 1 7 1
Rattus everetti 241326 1605 315 4 16 2.12 26 2.37 1 2 24 2.35 67 2.21
Rhynchomys soricoides 4215 1095 185 1 11 1.19 17 1 14 1.72 42 1.3
Non-native species
Rattus exulans 1017910 1925 70 4 51 3.33 23 3.92 20 3.3 43 3.38 137 3.48
Rattus tanezumi 1008455 1495 180 4 21 3.89 16 4 2 2 14 2.82 53 3.18

*Measured from IUCN maps, modified based on current distributional data.

 As documented across all gradients, plus additional records from Cordillera region (Heaney et al., 1998).
àMean adult body weight (g).
§ Diet groups ranked from highly specialized to generalist: 1, vermivore; 2, insectivore; 3, granivore/frugivore; 4, omnivore.
–For analyses, the total number of individuals was standardized using per site catch totals rarefied by sampling effort.

that entered the Philippines c. 1–6 Mya (Esselstyn & Brown,
2009). Rattus exulans and R. tanezumi, the two non-native
rodents on our gradients, are both widespread in Southeast
Asia and occur throughout the Philippines (Heaney et al.,
1998). They were introduced from the Asian mainland, most
likely in association with prehistoric human colonization or
trade (Musser & Carleton, 2005). Our understanding of
mammalian diversity in the Philippines remains incomplete.
Although the species definitions used herein are supported by
recent morphological and genetic studies (Steppan et al., 2003;
Rickart et al., 2005; Jansa et al., 2006; Balete et al., 2007;
Heaney et al., 2009, 2011), future work may result in some
taxonomic changes, including splitting some of the native taxa
that are widespread in the Philippines. However, such taxo-
nomic splits would not affect the uniformity of the Cordilleran
fauna as we now understand it and would not appreciably
impact the results of our study.
We used standard field methods proven effective for small
mammal surveys in the Philippines (Rickart et al., 1991, 2011;
Heaney et al., 2006a; Balete et al., 2009) that involved trapping
across microhabitats at multiple localities to obtain a com-
prehensive assessment of local assemblages. At each of the four
study areas, trapping was conducted during the dry season
(between January and May). Individual localities along each
transect were surveyed over 5- to 18-day periods with effort
ranging between 200 and 1500 trap nights (mean 609; n = 38
localities). At most localities, sampling was sufficient to
document the presence and relative abundance of most species
(as assessed through species accumulation rates and reflected
in the relatively complete occupancy of species at localities
within their elevational ranges; see Tables S1–S4 in Supporting
Information). At each locality, we used a combination of snap
traps and live traps to capture small mammals. Most traps were
set on the ground surface, along runways, near holes or in
subsurface openings. Other traps (c. 10–40% at most localities)
were placed 1–5 m above ground, on horizontal branches,
within tree cavities or on intersecting vines. Traps were baited
with either fried coconut coated with peanut butter (50–90%
of total trap effort) or live earthworms (10–50%). For most
traps, baits were alternated on consecutive days. Voucher
specimens of all species were deposited at the Field Museum
and the Philippine National Museum.

532 Diversity and Distributions, 17, 530–541, ª 2011 Blackwell Publishing Ltd

At each locality, we recorded information on general habitat
characteristics, amount of natural and anthropogenic distur-
bance, disturbance history and successional stage. Criteria for
assessing habitat disturbance and regeneration were based on
patterns of forest disturbance and plant community succession
associated with traditional agriculture in the Central Cordillera
(Kowal, 1966). We assigned each locality to one of four ranked
categories of habitat disturbance (from least to most distur-
bance): (1) intact or nearly intact mature forest, (2) mature
forest or forest fragments with moderate disturbance because
of selective logging, (3) heavily disturbed mixed pine (Pinus
kesiya) and broadleaf forest, heavily disturbed margins of
mature forest or regenerating secondary forest and (4)
deforested areas including crop margins, fallow cropland,
areas of early secondary growth dominated by brushy vegeta-
tion and periodically burned grassland or open pine woodland.
Among the four study areas, the elevational range of
localities varied (< 100–1225 m) as did the severity and spatial
distribution of habitat disturbance (see Tables S1–S4 in
Supporting Information). Disturbance was negatively corre-
lated with elevation at Balbalasang, but there was no significant
or consistent relationship between disturbance and elevation
on the other gradients. Disturbance was most extensive at Mt.
Data where surveys were confined to a narrow (< 100 m)
elevational zone in a mosaic of remnant mossy forest,
secondary growth and cropland, and no localities could be
categorized as intact mature forest (rank 1). The other three
gradients included the full range of habitat disturbance
categories. At Balbalasang and Mt. Amuyao, disturbance was
most severe at lower elevations where there was extensive
agriculture. Disturbance also was significant at some high
elevation localities, particularly near the summit of Mt. Pulog
where periodic fire created a mosaic of grassland and forest.
To summarize association with habitat disturbance, we
calculated a disturbance score (S) of a species (i) as
Pk
j¼1  nj ðRj Þ
Si ¼
Ni
where nj is the number of captures of the species at jth locality,
Rj is the disturbance rank at that locality and Ni is the total
number of captures across all survey localities (k). Thus, S
potentially ranged from 1 (restricted to least-disturbed habi-
tats) to 4 (restricted to greatest disturbance). Because trapping
effort was not uniform across localities, for each gradient, we
standardized the abundance of each species at each locality
using total captures rarefied by sampling effort. Values for S
were calculated separately for each local gradient and were
averaged to represent a composite regional gradient. We
acknowledge that our disturbance metric does not account for
imperfect detection.
We used an information-theoretic approach (Burnham &
Anderson, 2002) to assess the influence of species character-
istics on habitat disturbance scores. On the basis of our field
studies conducted over the past two decades (Rickart et al.,
1991, 2011; Balete et al., 2009) and review of traits often
associated with response to habitat loss (e.g. Laurance, 1991;
Diversity and Distributions, 17, 530–541, ª 2011 Blackwell Publishing Ltd
Habitat disturbance & Philippine mammals
Newmark, 1994; Swihart et al., 2003; Lee et al., 2005; Boyles &
Storm, 2007; Feeley et al., 2007), we selected four variables
that summarize key distributional and ecological traits
of species: (1) geographic range size (log-transformed km2)
based on species distribution maps from the IUCN Red List
(http://www.iucnredlist.org/technical-documents/spatial-data#
mammals) modified to include recent distribution records
(http://www.fieldmuseum.org/philippine_mammals/introduction.
asp), using an Albers equal area conic projection for south
Asia in ArcGIS v 9.3.1 (ESRI, Redlands, CA, USA), (2) extent
of elevational range (in metres, divided by 100) within the
Cordillera region as documented from available historical and
recent records, (3) body size (log-transformed mean adult
weight, in grams) and (4) degree of trophic specialization, as
reflected in the variety of food items found in stomachs and
categorized by ranks from most to least specialized (vermi-
vore, insectivore, granivore/frugivore, omnivore). Variables
showed low levels of collinearity (rs < 0.60). We did not
include the two Carpomys species in these analyses because
each was represented by a single specimen and are otherwise
so poorly known that data are insufficient to estimate these
variables.
Each predictor variable was considered individually and in
combination, resulting in 15 possible a priori explanatory
models. For each of the four local gradients and for the
regional (composite) gradient, we assessed full model sets for
two species groups, one including all species and a second for
native species only. We used linear regression and Akaike’s
information criterion corrected for small sample size (AICc) to
assess model performance, ranking models within each set
using DAICc. We interpret the strongest model as that having
the greatest AICc weight (a measure of model likelihood),
recognizing that unnested models with DAICc < 2 are often
considered equivalent (Burnham & Anderson, 2002). Because
determining a ‘best’ model can be problematic, we model
averaged the results for each regional gradient to provide a
basis for interpreting the significance and stability of each
predictor after accounting for model-selection uncertainty.
The composite model also illustrates the direction of the
relationship between each parameter and disturbance toler-
ance. We limited model averaging to a confidence set of
candidate models defined as those with AICc weights within
10% of the greatest weight. Because of small sample sizes, we
present 95% confidence intervals on the model-averaged
coefficients. Parameters are interpreted as uninformative
(P > 0.05) if the confidence intervals include zero.
Correlation was assessed using Spearman’s coefficient (rs).
Regression analyses were conducted using spss (v.17; SPSS,
Chicago, IL, USA). Capture data were effort-standardized
using the R statistical framework version 2.9.2 (R Core
Development Team 2009, http://www.r-project.org).
RESULTS
Across all four local gradients, 22 928 trap nights yielded 1769
captures of small mammals representing 16 native and two
533
E. A. Rickart et al.

non-native species (Table 1). The number of species per (a)

gradient ranged from 11 (Mt. Data) to 15 (both Balbalasang
and Mt. Amuyao). Nine species occurred on all gradients, and
four occurred on single gradients. The number of gradients
occupied and regional habitat disturbance score of species
were significantly correlated (rs = 0.54, n = 18, P < 0.02). On
three of the four gradients, species showed consistent
responses to habitat disturbance as reflected by significant
correlation of disturbance scores between gradients (Mt.
Amuyao vs. Balbalasang, rs = 0.90, n = 13, P < 0.005; Mt.
Amuyao vs. Mt. Data, rs = 0.70, n = 11, P < 0.05; Balbalasang
vs. Mt. Data, rs = 0.70, n = 11, P < 0.05). On the Mt. Pulag (b)
gradient, disturbance scores for most native species were
consistently higher and were not correlated with those of the
other gradients (Mt. Amuyao, rs = 0.32, n = 11, P = 0.30; Mt.
Data, rs = 0.38, n = 8, P = 0.28; Balbalasang, rs = 0.03,
n = 10, P = 0.65).
Species richness declined with increasing levels of habitat
disturbance (Fig. 2a). Native species richness was greatest in
least-disturbed (three gradients) or moderately disturbed
habitat (one gradient) and declined with increasing distur-
bance. Non-native rodents were abundant only in deforested
(c)
areas or severely degraded forest (ranks 3 & 4), and they were
not recorded in least-disturbed mature forest (Fig. 2b). Across
all four gradients, overall abundance of native mammals was
greatest in moderately disturbed habitat (rank 2), lower in
(d)
least-disturbed habitat (rank 1) and declined in more heavily
disturbed areas (Fig. 2c).
Of the 16 native species (Table 1), all but two had
disturbance scores > 1, indicating some association with (e)
habitat disturbance. Six native species occurred in previously
deforested areas that supported either secondary forest (rank
3) or early secondary growth (rank 4). However, none of the
native species had overall disturbance scores approaching those
of the two non-natives (S > 3.0). Apomys datae, the most Figure 3 Relative abundance (percent trap success) of selected
abundant species on all four gradients, generally had low native species of small mammals across gradients of increasing
disturbance scores (Table 1 & Fig. 3a). It was most common in habitat disturbance: (a) Apomys datae, (b) Apomys abrae, (c)
least-disturbed or moderately disturbed habitats and occurred Rattus everetti, (d) Chrotomys whiteheadi and (e) Crocidura grayi.
in more heavily disturbed habitat on only one gradient. In
contrast, Apomys abrae, the second most abundant species, was
strongly associated with intermediate disturbance levels (ranks disturbed habitats. Other native species were much less
2 & 3) and only rarely encountered in intact forest (Fig. 3b). abundant overall, and many were restricted to a subset of
Neither of these species was recorded in the most severely gradients (Table 1), but most occurred over a range of

(a) (b) (c)

Figure 2 (a) Total species richness of

small mammals across four gradients of
increasing habitat disturbance. White bars
separate native (lower) and non-native
(upper) species. (b) Relative abundance
(percent trap success) of non-native spe-
cies across the four disturbance gradients.
(c) Relative abundance (percent trap suc-
cess) of all native species.

534 Diversity and Distributions, 17, 530–541, ª 2011 Blackwell Publishing Ltd
 Habitat disturbance & Philippine mammals

disturbance conditions. Rattus everetti and Chrotomys white-
headi (Fig. 3c,d) had very similar patterns of occurrence and
were less common in mature forest (rank 1) than they were in
moderately or severely disturbed habitat. While less abundant,
Crocidura grayi (Fig. 3e) also had broad occurrence across
three of the four gradients.
Model performance varied between gradients and species
groups (Table 2; for complete results, see Table S5 in Sup-
porting Information). Overall model support was low. In only
three cases did a given model receive strong support (AICc
weight > 0.60). Additionally, three of the eight data sets
contained multiple unnested models with DAICc < 2, render-
range consistently appeared in the highest-ranking model or
set of models (DAICc < 2). For native species only, results were
more variable across gradients with each predictor identified at
least once. For two of the four gradients, the same model
received the highest weight (DAICc = 0) for both species
groups.
For the regional gradient, single models also were not
overwhelmingly supported for either the entire group of
species or natives alone. Of the four predictor variables,
elevational range and geographic range appeared in the
highest-ranked models for both species groups. The model-
averaged result for each species group was

DT ðall speciesÞ ¼ 0:404 þ 0:246ðlogGRÞ þ 0:118ðER=100Þ  0:236ðlogBSÞ þ 0:115ðDBÞ

DT ðnative speciesÞ ¼ 0:446 þ 0:120ðlogGRÞ þ 0:106ðER=100Þ  0:272ðlogBSÞ þ 0:080ðDBÞ

ing it difficult to choose a ‘best’ model (Table 2). For data sets where DT is disturbance tolerance, GR is geographic range, ER
that included all species, elevational range and geographic is elevational range, BS is body size and DB is diet breadth.

Table 2 Summary statistics for linear regressions and results of model selection for disturbance tolerance of small mammals. Within
groups, models are ranked based on Akaike’s information criterion corrected for small sample size (AICc). All models with AICc weights
>0.10 are included, which encompasses all models where DAICc < 2. For the complete model set, see Table S5 in Supporting Information.

Gradient and Species group Model* R2 RSS K AICc DAICc AICc weight

Mt. Amuyao
All species (n = 15) ER 0.644 4.434 3 )10.099 0.000 0.5723
GR, ER 0.672 4.084 4 )7.515 2.585 0.1571
ER, DB 0.660 4.238 4 )6.959 3.140 0.1191
Native species (n = 13) ER 0.750 1.180 3 )22.526 0.000 0.6377
GR, ER 0.772 1.079 4 )19.356 3.170 0.1307
ER, BS 0.769 1.090 4 )19.224 3.302 0.1223
Balbalasang
All species (n = 14) GR, ER 0.645 5.328 4 )1.081 0.000 0.4743
ER 0.446 8.314 3 1.104 2.185 0.1591
GR 0.418 8.727 3 1.783 2.864 0.1133
Native species (n = 12) ER 0.392 2.269 3 )10.987 0.000 0.6177
Mt. Data
All species (n = 11) GR 0.400 1.401 3 )13.239 0.000 0.3780
ER 0.297 1.643 3 )11.487 1.753 0.1574
Native species (n = 9) DB 0.124 0.887 3 )10.054 0.000 0.2898
ER 0.092 0.919 3 )9.735 0.319 0.2471
GR 0.084 0.927 3 )9.657 0.397 0.2376
BS 0.005 1.007 3 )8.912 1.142 0.1637
Mt. Pulog
All species (n = 11) GR 0.482 1.563 3 )12.036 0.000 0.4519
ER 0.422 1.743 3 )10.837 1.199 0.2481
Native species (n = 9) GR 0.510 0.718 3 )11.957 0.000 0.7713
Combined gradients
All species (n = 16) GR, ER 0.785 1.671 4 )24.510 0.000 0.5322
GR, ER, BS 0.803 1.532 5 )21.536 2.974 0.1203
Native species (n = 14) ER 0.656 1.003 3 )28.505 0.000 0.3909
GR, ER 0.715 0.832 4 )27.077 1.428 0.1915
ER, BS 0.713 0.836 4 )27.010 1.495 0.1852
ER, DB 0.691 0.902 4 )25.946 2.559 0.1088

*Predictor variables: ER (elevational range), GR (geographic range), BS (body size), & DB (diet breadth).

Diversity and Distributions, 17, 530–541, ª 2011 Blackwell Publishing Ltd 535
E. A. Rickart et al.
Table 3 Regional gradient model averaging results. Composite model slope and intercept parameter estimates and associated standard
errors and 95% confidence intervals.
Species group Parameter Estimate
All species Intercept )0.404
GR* 0.247
ER* 0.118
BS )0.236
DB 0.115
Native species Intercept 0.446
GR 0.120
ER* 0.106
BS )0.272
DB 0.080
*Significant predictor at P < 0.05.
Composite models for the two groups show similar direction-
ality for predictors (positive for geographic range, elevational
range and diet breadth, and negative for body size). When all
species were considered, disturbance tolerance was significantly
(P < 0.05) positively related to geographic range size and
elevational range size. In contrast, elevational range size is the
only significant (P < 0.05) predictor of disturbance tolerance
for native species (Table 3).
DISCUSSION
Biotic surveys across gradients of habitat disturbance provide
direct information on the relative tolerance of native species to
disturbance and the conditions promoting invasion by non-
native species. Where they include regenerating secondary
habitats, they also are informative regarding the reestablish-
ment of native assemblages. A number of studies have used this
approach to assess effects of habitat disturbance on small
mammal communities in tropical regions (Dwyer, 1984;
Lehtonen et al., 2001; Wijesinghe & Brooke, 2005; Umetsu &
Pardini, 2007; Suntsov et al., 2009).
These and other studies have also documented distinct
differences between continental and island systems. Studies in
continental tropical forests have noted increased small mam-
mal abundance and/or diversity associated with moderate
forest disturbance or fragmentation (Isabirye-Basuta & Kasen-
ene, 1987; Wu et al., 1996; Malcolm, 1997; Pardini, 2004;
Lambert et al. 2006; Suntsov et al., 2009). Such phenomena
generally are attributed to increased habitat heterogeneity or
resource availability, and edge effects that allow coexistence of
forest-restricted and disturbance-adapted species (Malcolm,
1997; Harrington et al., 2001; Pardini, 2004). They also are
consistent with the intermediate disturbance hypothesis (Con-
nell, 1978), which attributes increased diversity to a disruption
of competitive equilibrium with intermediate levels of distur-
bance. In contrast, studies conducted on disturbance responses
of small mammals on tropical islands have documented
decreased diversity and abundance with moderate disturbance,
536
95% CI
SE Upper Lower
0.443 0.541 )1.348
0.097 0.453 0.041
0.029 0.180 0.055
0.226 0.246 )0.718
0.104 0.338 )0.107
0.357 1.216 )0.325
0.082 0.297 )0.056
0.025 0.160 0.052
0.183 0.123 )0.666
0.068 0.227 )0.066
which may reflect the predominance of sensitive forest-
dependent species (Andrianjakarivelo et al., 2005; Wijesinghe
& Brooke, 2005; Wells et al., 2007). Effects of more severe
forest disturbance on tropical small mammal faunas involve
major reduction in native species richness and abundance, with
the loss of forest-dependent species, increase in species
associated with early seral stages and presence of non-native
species (Dwyer, 1984; Lynam, 1997; Wijesinghe & Brooke,
2005; Scott et al., 2006; Umetsu & Pardini, 2007; Suntsov et al.,
2009).
Based on these prior studies, it is apparent that the
distribution patterns of native species along the four distur-
bance gradients on Luzon Island are similar to those typically
seen for small mammals in the continental tropics. This reflects
the fact that the native small mammal fauna is ecologically
diverse and includes species that react differently to distur-
bance. A few species appeared to have very limited tolerance as
reflected in consistently low disturbance scores. At Mt. Data,
our most disturbed site, two such species (Chrotomys silaceus
and Rhynchomys soricoides) were documented historically
(Thomas, 1898; Sanborn, 1952) but were not detected in our
survey and presumably are no longer present. However, most
native species exhibited moderate tolerance for habitat distur-
bance, and some were actually more abundant in light to
moderately disturbed areas than they were in more pristine
habitat. Additionally, more than one-third of the native species
occurred in previously deforested areas where forest was
regenerating. This demonstrates a substantial level of resilience
in response to recovery from severe disturbance.
The impact of non-native rodents on island faunas has
received considerable attention (e.g. Drake & Hunt, 2009).
However, few studies have examined the role of habitat
disturbance in their establishment and spread. On Madagascar,
the invasive Rattus rattus is considered a possible threat to
endemic small mammals (Goodman, 1995). Although studies
there have demonstrated the widespread occurrence of R. rat-
tus in forested habitats as well as its positive association with
disturbance (Lehtonen et al., 2001; Ganzhorn, 2003), there is
Diversity and Distributions, 17, 530–541, ª 2011 Blackwell Publishing Ltd

no direct evidence that it has displaced native species.
Although non-native rodents have been implicated in the
extinction of several insular mammals on isolated islands with
highly depauperate faunas (Harris, 2009), in most cases, the
specific mechanisms involved are poorly known.
On the Luzon disturbance gradients, non-native rodents
were abundant where habitat was most severely disturbed,
much less common at intermediate levels of disturbance
(including secondary forest) and were not encountered in
intact forest. These results suggest that non-native species
require substantial disturbance to become firmly established,
and their persistence requires sustained disturbance that
disrupts forest regeneration. Furthermore, the inverse patterns
of occurrence and abundance of native and non-native species
across the disturbance gradients (Fig. 1) demonstrate that the
community dynamics associated with habitat disturbance and
regeneration result from the differential responses of these
groups and indicate the role of direct competition. Specifically,
they suggest that: (1) non-native species cannot effectively
invade mature forest where natives have competitive superi-
ority, (2) successful establishment of non-natives requires
disturbance severe enough to eliminate most of the native
species and (3) native species reoccupy regenerating habitat
where they ultimately displace non-native species. These
suppositions can and should be tested with additional field
studies in the Cordillera region. Surveys conducted along
‘regeneration’ transects consisting of areas in different stages of
succession following disturbance (e.g. Dwyer, 1984), or long-
term monitoring in regenerating habitat would provide
information on the dynamics of native and non-native species
during secondary succession, rates of faunal recovery and other
details on the reestablishment of natural communities in
secondary forest.
The diversity of the native small mammal fauna appears to
be a key factor in limiting the spread of non-native species in
the Cordillera region. This is illustrated by counterexamples
from elsewhere in the Philippines; non-native species are
common in mature forest only on geologically young or very
small islands where native communities are naturally depau-
perate (e.g. Biliran, Camiguin and Negros islands; Heaney
et al., 1989, 2006b; Rickart et al., 1993). In these instances,
non-native species appear to be ‘naturalized’ as additional
community members, and although they probably compete
with native species, the result is coexistence rather than
wholesale displacement. Although our study suggests that non-
native rodents do not severely threaten native mammal
communities in northern Luzon, their presence is nonetheless
disruptive. Indiscriminant rodent control measures target
beneficial native species as well as non-native pests (Ong &
Rickart, 2008). Furthermore, non-natives may transmit exotic
parasites or diseases to less resistant native hosts (Dowler et al.,
2000; Duplantier & Duchemin, 2003; Wyatt et al., 2008).
Although model selection did not reveal a single factor or set
of factors having overwhelming or consistent influence on
disturbance tolerances of species, this is not surprising given
the ecological diversity of the Luzon fauna. Different results for
Diversity and Distributions, 17, 530–541, ª 2011 Blackwell Publishing Ltd
Habitat disturbance & Philippine mammals
the separate gradients may reflect variation in local ecological
processes and disturbance history. However, because species
disturbance scores across the gradients were generally consis-
tent, we believe model selection and model averaging for the
composite regional gradient provides a general assessment of
the important determinants of disturbance relationships. For
the full species group, geographic range emerged as a strong
determining factor at this regional scale. To a large extent, the
importance of this variable was because of the two non-native
species that have both the broadest geographic distributions
and the highest disturbance scores. With their removal,
geographic range was not a strong predictor for native species
alone.
Endemic or range-restricted species typically are viewed as
less tolerant to disturbance than are widespread species,
presumably because of greater ecological specialization
(Brown, 1995). Several studies have emphasized the vulner-
ability of tropical island endemics in particular (Wijesinghe &
Brooke, 2005; Meijaard et al., 2008; Berglund et al., 2009;
Kier et al., 2009). The non-volant small mammals that are
native to northern Luzon are all endemic to the Philippines,
but their geographic ranges vary substantially. Lack of
support for geographic range as an explanatory variable in
our study demonstrates that range restriction per se has little
influence on disturbance tolerance of native species in
northern Luzon.
Niche breadth is often cited as a major factor influencing
response of species to habitat perturbations (e.g. Terborgh &
Winter, 1980; Vázquez & Simberloff, 2002). We examined two
species attributes that represent different components of
ecological specialization. Diet breadth has been associated
with sensitivity to disturbance (Laurance, 1991; Boyles &
Storm, 2007). However, this factor received very little support
among models despite the fact that several members of the
Luzon fauna have highly specialized diets. As a case in point,
Chrotomys whiteheadi, a vermivore, had one of the highest
disturbance scores among native species. This species occurs
across the entire disturbance spectrum, including agricultural
sites where it feeds on non-native earthworms and snails
(Rickart et al., 2005; Stuart et al., 2008). For this species,
trophic specialization has facilitated exploitation of novel
resources that are abundant in highly disturbed habitats.
In our study, elevational range was clearly the most
important predictor variable for disturbance response of native
species. This variable was also found to be an important
indicator of disturbance sensitivity in Southeast Asian birds
(Lee et al., 2005). Because forest type in the Philippines is
primarily a function of elevation (Whitmore, 1984; Heaney &
Regalado, 1998), elevational range serves as a proxy measure
for the range of natural habitats occupied by native species. Its
emergence as an important factor indicates that the natural
ecological amplitude of a species is an important determinant
of disturbance tolerance.
Luzon is an ancient oceanic island with a highly endemic
fauna. It also has suffered severe habitat degradation during
the past century. Given prevailing ideas about the susceptibil-
537
E. A. Rickart et al.

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SUPPORTING INFORMATION
Additional supporting information may be found in the online
version of this article:
Table S1 Capture data for small mammals at localities on Mt.
Amuyao.
Table S2 Capture data for small mammals at localities in
Balbalasang-Balbalan National Park.
Table S3 Capture data for small mammals at localities in Mt.
Data National Park.
Table S4 Capture data for small mammals at localities in Mt.
Pulag National Park.
Table S5 Summary statistics for linear regressions and results
of model selection.
As a service to our authors and readers, this journal provides
supporting information supplied by the authors. Such mate-
Diversity and Distributions, 17, 530–541, ª 2011 Blackwell Publishing Ltd
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Habitat disturbance & Philippine mammals
rials are peer-reviewed and may be re-organized for online
delivery, but are not copy-edited or typeset. Technical support
issues arising from supporting information (other than missing
files) should be addressed to the authors.
BIOSKETCH
Research activities of the authors deal with the processes that
shape spatial and temporal patterns of mammalian diversity.
All are interested in how human activities affect biodiversity.
Author contributions: L.R.H., D.S.B. and E.A.R. conceived the
project and collected the data, R.J.R. and E.A.R. performed
data analyses, and E.A.R. led the writing which involved all the
authors.
Editor: Bruce Patterson
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