Journal of Tropical Ecology (1993)

9:409-433.

With

2 figures

A ciimparison
of amphibian
communities
through time and from place to place in Bornean
forests
ROBERT

F. INGER

Field Museum of Natural

and HAROLD
History,

K. VORIS

Chicago, Illinois,

USA

ABSTRACT.
We sampled riparian
frogs along 18 streams at eight localities in Borneo. At four of
these sites we sampled during more than one year. Altogether
49 species were included
in our
study and total sample size was 13,249. We measured
overlap in species occurrences
and arrays
of abundances
within and among localities. Variation
over the time span of our study was minor
within communities.
Overlaps
between streams at a locality were generally
higher than overlaps
of pairs of streams from different localities. Environmental
variation,
particularly
in stream width
and gradient,
had a clear effect on both intra-and
inter-locality
overlaps. Although
rainfall varied
between localities and within localities over time, that variation
did not seem to affect overlaps
among or within communities.
Environmental
factors did not account for all differences in overlaps
between communities.
Instead,
regional processes, perhaps the timing of barriers
or speciation
events, appear to have been responsible
for geographic
restrictions
of several species, leading to
variation
in overlap values.
KEY WORDS:
forests.

anurans,

Borneo,

community

structure,

community

variation,

Malaysia,

rain

INTRODUCTION

When one looks at community

structure within a relatively small area, the
significance ecologists attach to local phenomena,
such as biotic interactions
and species-specific responses to environmental
features, is understandable.
These are the most apparent phenomena,
even if they are not always easy to
tease apart and evaluate. However, as Ricklefs (1987) observed, features of local
community
structure may be strongly affected by regional processes, such as
barriers to dispersal, the history of speciation, and other phylogenetic
events.
For certain aspects of community
structure viewed at a regional scale, Hanski
( 1982) proposed a model relating distribution
of species across sites to their
abundances. This model assumes that species populations fluctuate in stochastic
fashion over time in response to biotic interactions
and environmental
fluctuations. In effect, local processes lead to regional patterns. A study by Gascon
( 1991) on larvae of Amazonian
frogs shows the inter-play of local and regional
processes. These tadpoles had species-specific responses to abiotic habitat characteristics and Gascons data give hints of biotic interactions,
e.g. scarcity of
409

410

ROBERT

F.

INGER

AND

HAROLD

K.

VORIS

co-occurrence
of larval species, a typical local process. Yet the restriction
of
two larval forms to stream microhabitats
is clearly a product of phylogenetic
history. These two, Atelopus p&her and Centrolenella oyampiensis, belong to genera
all of whose larvae develop in streams (Duellman
& Lynch 1969, McDiarmid,
1978) regardless of the distributions
of other sympatric
tadpoles of other genera.
Most studies of community
structure
in tropical amphibians
have concentrated on a single, relatively
restricted
area (e.g. Crump
1971, Gascon 1991,
Heyer 1973, Inger 1969, Inger & Colwell
1977, Toft & Duellman
1979). That
concentration
perhaps explains the primary
focus on local processes.
In this
paper we examine variation among Bornean amphibian
communities
across an
area approximately
700 km wide, which obliges us to consider regional processes
as well as local ones.
Our analysis is restricted
to that segment of the Bornean amphibian community occurring
along rain forest streams, species that spend their entire life cycles
in this riparian habitat or that utilize streams for breeding and larval development. We begin with examination
of variation over a 22-year period at one site,
Nanga Tekalit,
Sarawak
(Figure
1, site 1 ), which provides
a standard
with
which to evaluate variation
over space. We then consider
factors associated
with variation
from place to place.

1100
I

114O
I

I
1

1180
I

Figure 1. Map showing the eight localities in the Malaysian

states of Sarawak
(numbers
l-4) and Sabah
(numbers
5-8) on the island of Borneo. The localities are (1) Nanga Tekalit,
(2) Segaham,
(3) Pesu, (4)
Labang,
(5) Mendolong,
(6) Purulon,
(7) Marak
Parak, and (8) Danum.

Variatibn among frog communities

SAMPLING

411

SITES

Our sampling of stream frogs was conducted

at eight localities in rain forests
below 800 m in Borneo in the Malaysian
states of Sabah and Sarawak
(Figure
1, Table 1). Distances
between localities range from 35 to 640 km (Table 2).
Full details of these sites are given in Appendix
A.
Sites differed in several ways:
(i) Topography.
The only flat area was Labang (site 4, Figure 1). The rest
were hilly (e.g. Danum, site 8) to steep (Purulon and Segaham, sites 2 and
(ii)

(iii)

(iv)

(v)

6).
Elevation.
All except Purulon and Mendolong
(site 5) were below 300 m
asl. The streams at Purulon are at 320-370 m and the one at Mendolong
at 750 m.
Vegetation.
The entire area of Mendolong
included in this study had been
selectively
logged. The forest at Marak-Parak
(site 7) was old (45-50 y)
secondary growth that now has a high closed canopy. Labang was covered
with flat, alluvial forest. Most of the area at Pesu and all the area at the
remaining sites was well-drained,
hilly, and covered with primary dipterocarp forest. There was a small area of swamp forest at Pesu (site 3), and
both Danum and Nanga Tekalit (site 1) had a few flat areas.
Rainfall. Amount
of rainfall during sampling periods varied greatly from
site to site. The four in Sarawak
had the most precipitation,
with few
months having <300 mm. In contrast,
the sites in Sabah rarely had >300
mm.
Streams. Regardless
of amount of rainfall, all streams in this study were
perennial.
All became turbid after heavy rain, but only Sungai Seran at
Labang was continually
turbid. Sungai Seran was also the only low gradient stream and the only one with a silt bottom. Stream widths vary from
3 to 25 m. Streams less than 8 m wide were under canopy, those 8-10 m
partially under canopy. Banks of even the largest streams were under trees.

MATERIALS

AND

METHODS

Field procedures
At each site work was divided between effort along streams and in the forest
proper. Data from the non-riparian
work, which consisted of forest floor plots,
search of buttress-enclosed
areas, and night transects
through the forest, are
not used in this paper, but contribute
to an understanding
of the total fauna at
each site. The riparian work included collecting and observing
tadpoles by day
and collecting and observing
frogs during night transects.
The data from the
night transects
along fixed segments (250600
m) of streams form the basis of
this paper. On streams at four of the localities, we marked stations at 15-30 m
intervals with plastic flagging and recorded the position of each frog observed

Table

1.

The number

of night

stream

transects

and the number

First sample

Year

Labang

Seran

1963

29

477

Ensurai
Sekentut
Selubok
Set-bong
Lawan
Wong
Pesu

1962
1962
1962
1962
1962
1962
1964

36
36
15
36
17
12
78

747
772
640
1038
469
319
1775

Segaham

Segaham
Marok

1984
1984

13
10

612
331

Danum

Cabin
P. Tambun
S.Kalison
W6S5
Surinsin

1989
1986
1989
1986
1988

4
5
7

PeSU

Marak

Parak

each year on each stream.

Second

Stream

Tekalit

observed

period

Locality

Nanga

Transects

of anurans

Anurans

Year

sample

period

Transects

Third

sample

Transects

period

Anurans

Year

Anurans

1984
1984

5
5

241
247

1984

252

1970
1970
1970
1970

5
5
5
5

295
206
232
377

1984

51

97
476
194

1990
1989
1990

7
4
9

179
88
267

1990

306

4
4

213
206

1989

71

1990

122

fz

Mendolong

1987

234

1989

327

Mendolong

Kilampon

1989

322

1990

284

Purulon

Purulon

1989

257

1990

234

E;
F
c

1990

291

;
;:

413

Variation among frog communities

Table

2.

Distances

(km)

between

Nanga
Tekalit

Labang
Nanga Tekalit
Pew
Segaham
Danum
Marak
Parak
Mendolong

180

localities

Pesu

in Sarawak

Segaham

35
166

77
125
56

and Sabah.

Danum

Marak
Parak

565
640
540
555

.
Mendolong

485
615
475
500
210

295
425
285
305
275
185

Purulon
340
475
330
350
250
145
45

relative to the stations. We recorded or captured every frog seen as we waded

upstream (see Appendix B). The Sungai Seran at Labang (see Appendix A)
was too silty for wading and was searched from boats.
At Nanga Tekalit in 1962/63 we marked, released, and recaptured frogs on
three streams - Ensurai, Sekentut, and Serbong. To avoid the bias of counting
the same frog many times, we used the number of individuals
seen (either in a
quarter or during the entire year) rather than number of observations of those
species marked and released.
Table 1 gives the number of transects and number of individuals
per stream
per year. Intervals between transects for Nanga Tekalit in 1962/63 are given
elsewhere (Inger & Greenberg
1966). Intervals
in other years and at other
places varied according to the lengths of the sampling periods (see Appendix
A).
Statistical analysis

We relied on two measures of overlap to assess the similarity

between
samples. The first of these, overlap of abundance arrays, uses Morisitas
index
as modified by Horn (1966)
C = 2CnunJ(h,

where nji = number

of individuals

+ h,)N,Nz

of species i in sample j and

,
hj = cnj,/Nj2
Wolda (1981) f ound this index to be relatively independent
of sample
diversity.
The second measure of overlap, of species present in two samples,
Czekanowski coefficient (Wolda 198 1) :
overlap

(or similarity)

= 2c/(S + L)

size and
uses the

414

ROBERT

where c = number
S = number
L = number

F.

INGER

AND

HAROLD

K.

VORIS

of species common to the two samples

of species in smaller sample
of species in larger sample

As Wolda pointed out, most of the binary similarity

coefficients have some
weaknesses, but the Czekanowski
increases linearly
from zero to 1.0 as c
increases, and is simple to calculate.
We have the impression
that our estimate of the abundance array of the
community
on a stream approaches the true value after about five transects.
We have tested this assumption in the following way. We calculated the overlap
between two of the most heavily sampled streams at Nanga Tekalit
(site 1,
Figure I), Serbong, and Ensurai, using one transect drawn at random from the
36 on each stream in 1962/63. We then recalculated the overlap after adding a
second transect drawn at random, repeating the process until we had overlaps
based on five randomly
drawn transects. We followed this procedure twice.
Overlaps based on a single transect from each stream were 0.555 and 0.549 in
the two sets, increasing to 0.774 and 0.842, respectively, when two transects
were drawn from each stream, and reaching 0.812 and 0.839 after five transects.
As the last values are 95-98% of the value (0.85) obtained from the full data
set from each stream, we believe that our samples from every stream (see Table
1) in the study were adequate for our purposes.
For inter-locality
measures of overlap, we summed data for a stream across all
years of sampling before calculating overlaps of abundance arrays with another
stream. We assessed the effect of this procedure on the overlaps between the
Palum Tambun
at Danum, Sabah (site 8, Figure l), and each of the three
streams at Nanga Tekalit, Sarawak, sampled during three years. Consequently,
for the overlap of Palum Tambun
(sampled 1986, 1989, 1990) with Sekentut
(sampled 1962, 1970, 1984) we had nine new overlap values, and nine between
Palum Tambun
and Ensurai and between Palum Tambun
and Serbong. For
the Palum Tambun/Sekentut
pair, the mean of the nine overlaps was 0.61
(SD = 0.11) compared with 0.65 when all years for a stream were combined.
For Palum Tambun/Serbong
the mean of nine was 0.5 1 (SD = 0.14) compared
to 0.51 for years combined. The mean of nine for Palum Tambun/Ensurai,
0.44
(SD = 0.1 l), diverged further from the value for years combined, 0.54, but still
close enough to justify combining
years.
RESULTS

AND

DISCUSSION

Over short (within locality) or long distances (between localities),

variation
among these riparian frog communities
might appear because of differences in
general topography or vegetation, rainfall regimes (between localities), or physical characteristics
of streams (gradient, width, bottom characteristics,
etc.).
However, before accepting any observed differences between a pair of communities as reflecting inter-community
variation, it is necessary to consider that a

415

Variation among frog communities

single community
might vary over time. If the variation between two communities is no greater than the variation
over time within one of them, then the
observed difference between the two communities
may have only transient biological significance. We therefore begin our analysis with an examination
of
variation within communities.
Our analysis has the following organization:
(i) Variation
over time within
a stream, thus holding stream characteristics
(width, gradient, etc.) and general
environment
constant, but allowing for the effects of temporal variation in rainfall and species behaviour over shorter (<year) or longer (>year) periods.
(ii) Variation
between streams at a locality, thus holding general environment
(topography and vegetation) relatively constant but allowing for effects of differences in stream characteristics.
(iii) Comparison
of the effects of time and distance within a locality. This comparison is restricted to four streams at Nanga
Tekalit that are similar in gradient, width, and bottom types, thus minimizing
the effects of stream characteristics.
(iv) Variation
between communities
over
greater distances (i.e. at different localities),
thus allowing for effects of differences in general environment
(topography
and vegetation,
rainfall)
and in
stream characteristics
(width, gradient, etc.).

Variation within localities

Nanga Tekalit (site 1, Figure

1). This is our largest data set in terms of numbers

of individuals,
numbers of streams, numbers of transects, and length of observation time (Table 1). We use variation in it, among other things, as a standard
against which to evaluate variation
at other localities and overlaps between
localities.
(i) Variation
over time. If the assemblage of species and individuals
on a
stream varies over time, there should be gradual, if not continuous, divergence
from an initial observed state. Under this hypothesis, within-stream
overlaps
of abundance arrays and species occurrences between adjacent quarters of a
year should be larger than overlaps between non-adjacent
quarters. We test
this prediction with the data from 1962/63 on the four larger streams at Nanga
Tekalit (Table 3), the streams for which we have most data during that year.
.
Table 3. Overlap
Tekalit, Sarawak,

of abundance
arrays
in 1962 and 1963.

Overlap
Quarters
1x2
2X3
3x4
1X3
2X4
1x4

and of species occurrences

of Abundance

between

Arrays

Overlap

Ensurai

Sekentut

Serbong

Selubok

0.92
0.98
0.96
0.91
0.94
0.90

0.93
0.93
0.96
0.94
0.91
0.89

0.98
0.82
0.91
0.86
0.81
0.86

0.84
0.84
0.90

Ensurai
0.81
0.80
0.93
0.73
0.73
0.73

quarters

within

of Species
Sekentut
0.73
0.86
0.87
0.74
0.79
0.80

streams

at Nanga

Occurrences
Serbong

Selubok

0.83
0.92
0.96
0.81
0.88
0.79

0.76
0.84
0.85

416

ROBERT

F.

INGER

AND

HAROLD

K.

VORIS

These are also the streams most similar in width, bottom types, and gradient.
Overlaps of abundance arrays between adjacent quarters were slightly greater
but the difference is not significant
than between non-adjacent
quarters,
(Mann-Whitney
test, single-tailed,
P = 0.09). However, overlaps of species
occurrences between adjacent quarters are significantly
larger than those
between non-adjacent
quarters (Mann-Whitney
test, single-tailed,
P = 0.025).
Of the 16 species absent from these streams in one or several quarters (i.e.
those that depressed between-quarter
overlaps of species occurrences),
nine
were represented by <5 individuals
during the entire year on one or more
streams, and eight were found in only one or two quarters. Given these small
numbers, even random distribution
into quarters would drive down overlap in
species occurrences. Consequently,
neither measure of overlap provides convincing support for the hypothesis at this time scale.
Divergence from an initial state might accumulate over longer time intervals.
We test this hypothesis by comparing
overlaps between quarters of one year
(Table 3) with overlaps between years (intervals of 8, 14, 22 years) on the same
four streams (Table 4). Overlaps of abundance arrays between quarters of one
year were significantly
greater than overlaps between years (Mann-Whitney
test, single-tailed,
P = 0.001). However, overlaps of species occurrences showed
to bear in
no such difference (Mann-Whitney
test, P = 0.18). It is important
mind that a species need have been observed just once to be counted as present
in a given year and increase overlap of species occurrences with another year,
while the same species would have depressed between-quarter
overlap.
Although
overlaps of abundance arrays seem to support the hypothesis of
divergence over time, Table 4 shows no relation between the length of the
interval in years and overlap values.
(ii) Variation
over distance. Distances between streams at Nanga Tekalit
varied from 0.5 km to 13 km. At this point in the analysis, we use two additional,
smaller streams. Between-stream
overlaps of abundance arrays within years
(Table 5) and summed across years (Table 6) generally had a much broader
range than overlaps of species occurrences (Tables 5 and 6). Distance was not
a predictor of overlap. Overlaps between Wong and both Selubok and Sekentut
were smaller than the overlaps between the last two and both Ensurai and

Table 4. Overlap
Tekalit,
Sarawak.

of abundance

Overlap

arrays

and of species occurrences

of Abundance

between

Arrays

Overlap

Years

Ensurai

Sekentut

Serbong

Selubok

1962x 1970
1962x1984
1970x 1984

0.81
0.86
0.84

0.84
0.81
0.85

0.88
0.87
0.72

0.73

Ensurai
0.73
0.77
0.82

years

within

of Species
Sekentut
0.74
0.82
0.90

streams

at Nanga

Occurrences
Serbong

Selubok

0.74
0.78
0.79

0.82

Variation among frog communities

Table 5. Overlap
of abundance
arrays
wak. The rows for Selubok and Lawan
Overlap
1962
Ensurai
Sekentut
Serbong
Selubok
Lawan

Ensurai
Sekentut
Serbong

Ensurai
Sekentut
Serbong

Ensurai
Sekentut
Serbong
Selubok
Lawan

Overlap

of Species

Sara-

Occurrences

Selubok

Lawan

Wong

Sekentut

Serbong

Selubok

Lawan

Wong

0.96

0.85
0.87

0.92
0.88
0.85

0.52
0.53
0.69
0.45

0.38
0.29
0.29
0.28
0.42

0.76

0.78
0.78

0.76
0.80
0.80

0.74
0.64
0.62
0.71

0.89
0.70
0.73
0.76
0.82

of Abundance

Sekentut

Serbong

Selubok

0.71

0.71
0.68

0.77
0.84
0.77

of Abundance

Sekentut

Serbong

0.82

0.79
0.95

Table 6. Overlap
wak. Observations

Arrays

Tekalit,

Serbong

Overlap
1984

between streams at Nanga

cells in 1970 and 1984.

Sekentut

Overlap
1970

of Abundance

and of species occurrences

are omitted due to empty

417

Selubok

Arrays
Lawan

Overlap
Wong

Serbong

Selubok

0.73

0.89
0.80

0.67
0.79
0.79

Overlap
Sekentut

Serbong

0.55
0.41
0.42

0.81

0.87
0.76

between

Overlap

Overlap

Sekentut

Serbong

Selubok

0.92

0.83
0.88

0.95
0.90
0.87

of Species

Wong

of abundance
arrays and of species occurrences
for each stream are summed over all years.
of Abundance

Occurrences

Sekentut

Arrays
Lawan

of Species

Arrays

streams

Lawan

Wong

Occurrences

Selubok

Lawan

Wong
0.59
0.69
0.58

at Nanga

Tekalit,

Sara-

of Species Occurrences

Lawan

Wong

Sekentut

Serbong

Selubok

Lawan

Wong

0.43
0.42
0.38
0.45

0.44
0.35
0.33
0.37
0.45

0.83

0.88
0.91

0.79
0.86
0.86

0.85
0.73
0.84
0.73

0.94
0.85
0.90
0.81
0.83

.
Serbong (Tables 5 and 6), despite the fact that Selubok and Sekentut
were
much closer to Wong (see Appendix
A).
Wong and Lawan were only half the widths
of the other four streams and
had much lower overlaps of abundance
arrays with the four larger ones than
the last had with each other (Table 6). Except for width,
Lawan was very
similar to Selubok and Sekentut, having a bottom mainly of sand and gravel,

418

ROBERT

F.

INGER

AND

HAROLD

K.

VORIS

with open pools, rifIles, and side pools. In terms of microhabitats

known to be
used by five dominant species (Inger 1969), Rana blythi, R. ibanorum, R. chalconota,
R. signata, and Pedostibes hosei, for larval development
(Inger et al. 1986) and for
adult perch sites (Inger 1969), Lawan should have had very high overlap of
abundance arrays with Sekentut and Selubok. Its low overlap of abundance
arrays with those streams suggests that it provided a significantly
different
environment,
particularly
for the larger species, such as R. b&hi and R. ibanorum.
These two species constituted 6% and 5%, respectively, of the Lawan sample
but 23-25% and 12-22% of the samples from Sekentut and Selubok (see
Appendix B; authorization
for species names is also given here). These large
species also had low abundances (3% and 7%) respectively) on Wong.
However, more than stream size was involved, for the two small streams,
approximately
the same size, had a low overlap of abundance arrays with each
other. Wong had the steepest gradient of all the streams at Nanga Tekalit,
which may explain why Lefitobrachella mjobergi, a riflle breeding species (Inger
1985), was one of the more abundant species on Wong but was seen only once
on three of the larger streams and not on the others. Staurois natator, a frog that
in our experience perches on rocks or leaves overhanging
streams, constituted
25% of the sample from Wong, but less than 1% of the other five samples.
Overlaps of species occurrences did not show a dichotomy between the small
and large streams. Although
there was not complete correspondence
between
the species seen on the small streams with those on the large ones, the streams
were close enough for any species in the area to reach them. Species that did
not or could not maintain
sizeable populations
on the small streams, i.e. those
that depressed overlap of abundance arrays, none the less contributed to overlap
of species occurrences.
(iii) Comparison
of the effects of time and the unique qualities of each stream.
The Nanga Tekalit data set allows comparison of small-scale time and distance
(as represented by the distinct assemblage on each stream) effects. For this
purpose we use data only from the four larger streams to increase the time
range (Table 1) and to avoid the complicating
effects of differences in stream
size. Overlaps of abundance arrays between streams within quarters (range
0.69-0.91, median = 0.84) were smaller than overlaps between quarters within
streams (median = 0.91, Table 3) (Mann-Whitney
test, two-tailed, P C 0.01).
At these scales, between-stream
effects contributed
more to variation than time.
Expanding
the time scale changed the results. The overlaps between years
within streams (Table 4) did not differ from overlaps between streams within
years (Table 5) (M ann-Whitney
test, two-tailed, P > 0.10). Overlaps of species
occurrences between streams within time intervals (quarters or years) did not
differ from overlaps between time intervals within streams (Mann-Whitney
tests, P > 0.10).
Other multi-year and multi-stream

at l-4 y at Danum

Within-stream
overlaps of abundances
7), Purulon (site 6; 0.87, 0.93), and Men-

samples.

(site 8) (Table

Variation among frog communities

Table 7. Overlap
streams at Danum,

of abundance
Sarah.

Overlap

Years
1986x
1986x
1969x

of Abundance

Cabin

Palum
Tambun

0.90

0.85
0.96
0.80

1989
1990
1990

arrays

419

and of species occurrences

Arrays

Overlap

Sapat
Kalison

W6S5

0.74

0.68
0.72
0.64

between

of Species

Cabin

Palum
Tambun

0.83

0.77
0.83
0.76

years

within

Occurrences

Sapat
Kalison

W6S5

0.86

0.72
0.76
0.83

dolong (site 5; 0.84, 0.93, 0.94) ranged from 0.64 to 0.96 (median = 0.85). As
a set, they are smaller than the overlaps between quarters at Nanga Tekalit
(Mann-Whitney
test, single-tailed,
P = 0.03), but did not differ from those
between longer intervals at Nanga Tekalit
(Mann-Whitney
test, P > 0.20).
Within-stream
overlaps of species occurrences between years at Danum, Purulon (0.74, 0.84), and Mendolong
(0.65-0.86) did not differ significantly
from
those at Nanga Tekalit (Mann-Whitney
tests, P > 0.10).
Between-stream
overlaps of abundances and of species occurrences at Purulon (0.97 and 0.89, respectively)
were much higher than between streams at
Danum (Table 8). The two streams at Purulon joined near the origins of the
surveyed sections and were very smiliar in size, gradient, bottom substrate, and
frequency of microhabitat
types.
At Danum between-stream
overlaps of both abundance arrays and species
occurrences (Table 8) fell within the range of those among streams at Nanga
Tekalit.
As at Nanga Tekalit,
distance between streams at Danum, varying
between 1 and 12 km, did not account for differences in overlaps of abundances
between streams. The Palum Tambun was much farther from the Cabin stream
and Sepat Kalisan than from the stream at W6S5, yet had higher overlaps with
the first two. Physical differences between these streams are not clearly related
to their overlaps. All streams had mixtures of pools, riffles, and torrents, though
W6S5 had a steeper gradient. Danum was the only site besides Nanga Tekalit
where the data permitted
a comparison of time and distance effects. Between-

Table 8. Overlap
Danum,
Sabah.

of abundance

Overlap

Cabin
Palum Tambur
Sapat Kalison

arrays

of Abundance

Palum
Tambum

Sapat
Kalison

0.73

0.65
0.83

and of species occurrences

Arrays

W6S5
0.84
0.65
0.57

Overlap

between

of Species

Palum
Tambun

Sapat
Kalison

0.76

0.83
0.83

streams

Occurrences

W6S5
0.74
0.90
0.82

at

420

ROBERT

F.

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AND

HAROLD

K.

VORIS

year, within-stream
overlaps both of abundance arrays and species occurrences
(Table 7) were significantly
higher than between-stream,
within-year overlaps
(Mann-Whitney
tests, two-tailed, P < 0.05).
Summa? of in&a-locality

variation

(1) Within-stream
overlaps
(abundance
arrays and species occurrences)
between short intervals (3 months) were very high (tested at Nanga Tekalit
only).
(2) Within-stream
overlaps between years were also high (four localities), but
at Nanga Tekalit were not as high as overlaps between 3-month intervals.
(3) Between-stream
overlaps (abundance arrays and species occurrences) were
strongly affected by stream width and gradient.
(4) If stream characteristics
did not vary, overlaps (abundance
arrays and
species occurrences) between streams within years did not differ from overlaps between years within streams. This comparison
was possible only at
Nanga Tekalit.
Variation between localities

Values of inter-locality,
between-stream
overlaps of abundance arrays had a
very broad range, 0.01-0.83 (Tables 9, 10, ll), and represent a significant
shift downward from intra-locality
overlaps. Inter-locality
overlaps of species
occurrences followed the same pattern; the range was broad and 81% of the
values fell below the range of intra-locality
overlaps.
Effects of stream character.
Between-stream
overlaps of abundance
arrays at
Nanga Tekalit were affected by stream width. Stream width appears to have
been an important
factor in inter-locality
overlaps as well. We have grouped
streams (Table 1) into four size categories (map numbers in parentheses): width
3-6 m: Marok (2), Wong (l), Lawan (1); width 7-9 m: Purulon (6), Kilampon
Table 9. Overlap
of abundance
arrays and of species
Sarawak.
Stream data were summed over all years.
Overlap

of Abundance

Segaham
Locality

Stream

Nanga
Tekalit

Ensurai
Sekentut
Selubok
Serbong
Lawan
Wong
Segaham
Marok
Pesu

Segaham
Pesu

Segaham
0.37
0.29
0.29
0.24
0.45
0.22

Marok
0.10
0.12
0.12
0.09
0.22
0.27

occurrences

Arrays

between

Overlap

Pesu

Labang

Pesu

Seran

Segaham

0.54
0.70
0.44
0.59
0.25
0.22
0.26
0.07

0.28
0.36
0.30
0.26
0.26
0.16
0.12
0.04
0.67

0.72
0.78
0.68
0.70
0.60
0.71

streams

between

of Species

Segaham

localities

Occurrences

in

Pesu

Labang

Marok

Pesu

Seran

0.60
0.64
0.59
0.57
0.42
0.66

0.60
0.63
0.59
0.60
0.55
0.62
0.60
0.56

0.47
0.49
0.43
0.46
0.39
0.38
0.44
0.41
0.61

Table

10.

Overlap

of abundance

arrays

and of species occurrences

OVERLAP

Locality

Stream

Danum

Cabin
P. Tambun
S. Ka.lison
w6S5

Marak
Parak
Mendolong

OF

Mmak

Mendolong

Surinsin

Mendolong

0.21
0.19
0.09
0.18

0.65
0.39
0.37
0.49
0.15

between

ABUNDANCE

streams

between

localities

in Sabah.

ARRAYS

OVERLAP

Purulon
Purulon
0.83
0.57
0.56
0.80
0.29
0.68

Stream

Kilampon
0.83
0.55
0.54
0.78
0.24
0.63

data were summed

OF

SPECIES

Ma&&

Mendolong

surinsin

Mendolong

0.45
0.54
0.40
0.48

0.67
0.63
0.65
0.72
0.67

over all years.

OCCURRENCES
Purulon
Pundon
0.59
0.67
0.58
0.65
0.71
0.84

Kilampon
0.61
0.63
0.60
0.67
0.60
0.80

s
2.
z?.
s
s
s
T
2
6
g
sN.
-g.

Table
years.

11.

Overlap

of abundance

arrays

and of species

occurrences

between

streams

between

OVERLAP

OF
SABAH

localities

ABUNDANCE

Labang
Nanga
Tekalit

Pesu
Segaham

Stream

Cabin

Seran
Ensurai
Sekentut
Selubok
Serbong
Lawan
Wong
Pesu
Segaham
Marok

0.19
0.30
0.34
0.30
0.30
0.38
0.27
0.24
0.16
0.20

P. Tambun
0.21
0.54
0.65
0.54
0.51
0.29
0.27
0.42
0.14
0.27

Mamk

Mendolong
Mendolong

W6S5

Surinson

0.20
0.48
0.63
0.45
0.57
0.30
0.52
0.54
0.17
0.16

0.08
0.15
0.18
0.16
0.16
0.33
0.30
0.14
0.11
0.44

0.01
0.02
0.03
0.02
0.02
0.02
0.04
0.03
0.09
0.03

OF

SPECIES

SABAH
Danum

Stream

data were

summed

over all

ARRAYS

S. Kaiison

OVERLAP

and Sarawak.

LOCALITIES

Danum
Sarawak
Localities

in Sabah

0.07
0.09
0.09
0.09
0.09
0.15
0.28
0.06
0.07
0.09

Purulon
Purulon

Kilampon

0.02
0.03
0.04
0.03
0.04
0.10
0.25
0.04
0.10
0.17

0.01
0.02
0.04
0.02
0.04
0.07
0.18
0.06
0.08
0.14

OCCURRENCES

LOCALITIES
Mart&

Mendolong
Mendolong

Purulon

Sarawak
Localities

Stream

Cabin

P. Tambun

S. Kalison

W6S5

Surinson

Labang
Nanga
Tekalit

Seran
Ensurai
Sekentut
Selubok
Serbong
Lawan
Wong
Pesu
Segaham
Marok

0.38
0.65
0.65
0.49
0.62
0.61
0.68
0.56
0.61
0.41

0.43
0.67
0.67
0.62
0.59
0.59
0.65
0.49
0.59
0.50

0.44
0.68
0.63
0.59
0.65
0.65
0.71
0.60
0.55
0.51

0.40
0.70
0.60
0.55
0.57
0.56
0.64
0.51
0.51
0.52

0.15
0.43
0.52
0.39
0.42
0.40
0.46
0.33
0.40
0.36

Pew
Segaham

0.28
0.60
0.54
0.49
0.56
0.50
0.62
0.45
0.50
0.51

Purulon

Kilampon

0.24
0.53
0.56
0.46
0.49
0.42
0.60
0.42
0.53
0.54

0.28
0.60
0.54
0.49
0.51
0.50
0.66
0.40
0.45
0.47
rlrt

~.

Variation among frog communities

423

(6), Cabin (8), W6S5 (8), Sepat Kalisan (8); width 10-14 m: Pesu (3), Seran
(8), and the four larger streams at Nanga
(4), Mendolong
(5)) P a 1urn Tambun
Tekalit (1); width 25 m: Segaham (2). If stream width accounts for a significant
part of the inter-locality
variation, overlaps between streams within size categories should be greater than overlaps between streams across size categories.
Overlaps
(grouped into four classes: cO.21, 0.21-0.40,
0.41-0.60,
BO.60)
within-stie
categories were significantly
greater than those across size categories
(chi-square = 19.4, df = 3, P < 0.01); 57% of the within-size category overlaps
(n = 30) exceeded 0.40 compared to 17% of the between-size overlaps (n =
82).
Between-stream
overlaps at Nanga Tekalit showed some effect of differences
in stream gradients. If differences in gradients affect inter-locality
overlaps,
overlaps between streams of similar gradients should exceed those between
streams of differing gradients. We grouped streams into the following gradient
classes from steepest (A) to flat (E); A: M arok, Purulon, Kilampon,
Mendolong;
B: Surinsin, Segaham; C: W6S5, Wong; D: Pesu, Lawan, Ensurai, Sekentut,
Selubok, Serbong, Cabin, Palum Tambun,
Sepat Kalisan; E: Seran. Overlaps
were grouped as in the preceding paragraph. Overlaps within gradient classes
were significantly
larger than those across classes (chi-square = 26.31, P <
0.01); 53% of the within-class overlaps (n = 30) exceeded 0.40, in contrast to
14% (n = 99) of the between-class overlaps.
Inter-locality
overlaps of species occurrences gave slightly different results.
Overlaps within-and
between-width
classes did not differ (chi-square = 4.94,
P = 0.30). However, overlaps within gradient classes were significantly
greater
than overlaps between those classes (chi-square = 12.44, P < 0.02). We interpret these results as indicating
that stream gradient had a greater effect than
stream width on the occurrences of species.
The effect of stream gradient is best seen on the Seran, the only stream
flowing through flat forest and the only one with turbid water and a silt bottom.
These circumstances
almost certainly account for the absence of any of the 15
species (27% of 55) in our data set that breed at riffles and torrents and have
larvae that either attach to rocks or wriggle into interstices between rocks and
gravel on stream bottoms. These 15 include all five species of Amolops (Inger
1966), three species of Ansonia (Inger 1992) four species of Leptobrachella, and
three species scattered through other genera (Inger 1985, and unpublished
data). An additional
five species absent along the Seran have been observed
elsewhere only at turbulent,
rocky areas of other streams: Micrixalus baluensis,
Philautus hosei, Rana hosei, Staurois latopalmatus, S. tuberilinguis (unpublished
data).
The two streams at Segaham (Figure 1, locality 2) show interaction
of stream
width and gradient on overlap. Although
the two streams, Marok (3 m) and
Segaham (25 m), joined where they were sampled, their overlap of abundance
arrays was only 0.07 and, though their overlap of species occurrences was higher
(0.65) it was still lower than the overlaps at Nanga Tekalit.
The five largest
species at that locality were much more abundant on the Segaham (41% of the

424

ROBERT

F.

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AND

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K.

VORIS

sample) than on the Marok (8%). Both are high gradient streams. However,
the Marok consists of a series of small waterfalls separated by short pools over
gravel and rock, whereas the Segaham has long stretches of foaming rapids over
large boulders, the kind of habitat that supports populations
of adult Rana hosei
and Amolops cavitym~anum and is used by tadpoles of A. cavi~mpanum and Bufo
juxtasper. The last two species were five times more abundant and Rana hosei 20
times more abundant on the Segaham than on the Marok (Appendix B).
Effects of rainfall patterns. Another environmental
factor that may have played
a role is the pattern of local rainfall. Variation
in rainfall locally may have
affected overlaps over time within streams, and systematic differences between
localities in amount and seasonal distribution
of rainfall may have affected
inter-locality
overlaps. Several features of the climate of Borneo are important
here: (1) At any given site, in the great majority of years there are no months
totally lacking rain. For example, over a 30-year period at Melalap Estate, a
recording station 10 km from Purulon (site 6), no month lacked rain and only
two had <20 mm; this is the site with the lowest annual rainfall in our set of
eight. (2) Locally, the amount of rainfall within months varies greatly from year
to year. To illustrate,
during a 20-year period, the within-month
variation in
rainfall ranged from 235 to more than 550 mm at both Sandakan and Sibu,
cities more than 700 km apart on opposite coasts of Borneo. At Melalap Estate
the coefficients of variation for rainfall during the 30-year interval ranged from
42% to 61% per month. Similar yearly variation, though not as extreme, was
evident at Danum (site 8) and Mendolong
(site 5) during a 3-year interval
(Figure 2). (3) There is great variation
among areas in total precipitation.
Annual rainfall at the sites for which we have at least one full year of observations were 1355 mm at Melalap
( 10 km from Purulon, 10 y mean), 2688 mm
at Danum (4 y), 2947 mm at Mendolong
(5 y), and 5669 mm at Nanga Tekalit.
During the actual months of sampling, rainfall at Purulon (169 and 45 mm)
was much less than at Danum (190-3 17 mm per month) or Mendolong
(180284 mm per month). (4) Heavy rain storms may be very local. Rains heavy
enough to cause short-term flooding are often restricted to a single, small catchment area or two. If heavy rainfall affects activity of frogs, its effects are not
necessarily coincident on all the streams at a locality.
Despite the great variation
in monthly
precipitation
at Nanga Tekalit
in
1962/63 (Figure 2), within-stream
overlaps between quarters were uniformly
high (Table 3). In that year, days with rainfall >25 mm, which was enough
to cause spates on the observation streams, were distributed
at random through
the year (Lloyd et al. 1968). Rainfall was moderately
heavy during the other
sampling periods at Nanga Tekalit and overlaps of abundance arrays between
years remained high (Table 4). The fact that sampling periods at Nanga Tekalit
over the years did not occur during the same calendar intervals appears to have
had little effect. Within-stream,
between-year overlaps using data from the
entire year 1962/63 did not differ from overlaps using data only from those

Variation among frog communities

RAIN

500

mm (1887)

IN

w MELALAP

425

u MENDOLONG

w DANUM

MAMJJASOND
MONTH

RAIN IN mm
1000

(1908)

+ Nanga

Tekallt

1963

MELALAP

JFMAMJJASOND

MONTH
RAIN

700

IN m m

(WSO)

td MELALAP

i-i MENDOLONG

DANUM

JASOND

MONTH
Figure 2. Monthly
rainfall
data for three years at three localities in Sabah. Melalap
is 8 km from
sampled locality
Purulon.
The middle graph gives the monthly
rainfall for Nanga Tekalit
(Sarawak)
1962163.

our
in

426

ROBERT

F.

INGER

AND

HAROLD

K.

VORIS

parts of 1962/63 matching

the periods of work in 1970 and 1984 (Wilcoxon
matched-pairs
signed-ranks test, P > 0.05).
Although rainfall varied appreciably from year to year at Danum (Figure 2)
and during sampling periods, there was no association between rainfall and
amount of overlap within streams (Table 7). At Purulon rainfall during the
second sampling period was less than 30% that in the first period (see above),
yet overlaps between years were very high (0.87, 0.92). Similarly,
at Mendolong
between-year overlaps were high (0.84-0.94) despite variation in rainfall.
If differing amounts of rainfall (either at the time of sampling or annually)
affect inter-locality
overlaps significantly,
overlaps between localities having
similar
rainfall should be larger than those between localities
differing in
amounts of rain. To test this hypothesis, holding stream gradient and width
constant, we compare overlaps of abundance arrays between the four larger
streams at Nanga Tekalit and Pesu (site 3), both areas with high rainfall, with
overlaps between those streams and Palum Tambun
at Danum (about half as
much rain). Differences between the two sets of overlaps (see Tables 9 and 11)
do not differ significantly
(Mann-Whitney
test, P > 0.20). All other interlocality tests of rainfall effects are confounded by differences in gradient or
stream width. However, overlaps of abundance arrays between Purulon and
Mendolong
(twice as much rain) were high (BO.60) despite differences in
stream width. Also overlaps between Purulon streams and those at Danum
(twice as much rain) were also high (0.54-0.83, Table 10) despite differences
in gradient.
Restricted geographic distributions.

In all the preceding analyses, a tacit assumption is that all species are available at all localities. There is evidence, on the
contrary,
that some species have limited
geographic
distributions
within
Borneo. For this part of the analysis, we use all frogs observed at a locality,
whether on a surveyed stream or not, to establish presence in an area. General
distribution
is based on Inger ( 1966), Inger & Dring ( 1988), Inger & Stuebing
(1992) and Matsui (1986). Ab un d antes and distributions
of species mentioned
below are given in Appendix B.
One of the dominant
species along streams in hilly areas of Sarawak, Rana
ibanorum, is currently known only from Sarawak. Intensive,
repeated search at
Danum (site 8) in streams that provide appropriate
habitats (clear streams
having beds of sand, gravel, and rock) and at other similar streams 100 km
south and 175 km west of Danum (field work by Inger) have failed to uncover
this species in eastern Sabah. Bufo asper, abundant on streams at all four localities in Sarawak, was also absent at Danum and the eastern Sabah localities
referred to above, again, despite the presence of appropriate
habitats. Other
abundant stream-side species that appear to have geographically
restricted distributions,
despite wider availability
of suitable habitat, include Amolops phaeomeluS (found in central Sarawak) and A. whiteheadi (western Sabah). Altogether,
overlaps because of
11 species (20%) in our data set depress inter-locality
geographically,
as distinguished
from ecologically,
restricted distributions.

Variation among frog communities

427

Do these restricted ranges reflect historical processes or competitive

interactions with ecologically
similar species? We look for evidence of biotic interactions within groups of closely related species, which, as they are usually ecologically homogeneous,
are most likely to show competition.
There were eight
such groups in our sample, four of which were present in sufficient numbers
for statistical analysis.
1. Rana ibanorum co-occurred with two related large species along streams at
Nanga Tekalit (site 1) (Inger & Greenberg 1966). All three were absent from
four streams in western Sabah that lacked suitable microhabitat.
Correlations
of relative abundances of these species in the 14 streams where at least one
was present were positive. This suggests that the absence of R. ibanorum from
appropriate
habitat in eastern Sabah is independent
of the distribution
of the
other two species.
2. The two large species of Bufo, usper and juxtasper, which form a distinct
species group (Inger 1972), co-occurred on seven streams. As their abundances
were negatively correlated (Spearman r, = -0.57, P < O.Ol), the absence of B.
asper from its usual habitat in eastern Sabah could be the result of competition.
3.. The two species of Amolops having geographically
restricted distributions
(see above),.each co-occurred with an abundant congener, poecilus in the case of
phaeomeru&nd
orphnocnemis in the case of whiteheadi. Larvae of phaeomerus and
poecilus have been collected together in tadpole stations (Inger 1985) as have
tadpoles of the other two (unpublished
data). Relative abundances of whiteheadi
and orphnocnemis were positively correlated, whereas abundances of phaeomerus
and poecilus were negatively correlated though not at a significant level (P >
0.05). The distributions
of whiteheadi and phaeomerus were not completely complementary as neither occurred in eastern Sabah.
4. The three species of Staurois (Appendix B) co-occurred in four streams and
in pairs or singly in the remaining
14 streams. Their relative abundances were
positively correlated, which makes competition
an unlikely explanation
of the
absence of S. tuberilinguis from streams at Danum and other streams in eastern
Sabah that lie outside our study area.
The other groups having one or more species with geographically
restricted
ranges had small sample sizes (Appendix
B). They include: three species of
slender toads, Ansonia, one widely distributed
and two absent from eastern
Sabah though sympatric at two localities in Sarawak; two species of horned
frogs, Megophy,
one apparently
restricted to central Sarawak and sympatric
with the second which was observed across the study area; and three species
of small pelobatid toads, Leptobrachella, with one restricted to Sabah and two
to Sarawak. As a genus, Leptobrachella exhibits strong altitudinal
stratification
(Inger & Stuebing 1992), suggesting that in this group competition
may be
important,
if not universal. The other two groups show no evidence that biotic
interactions
play a role in their geographic restrictions.
According to Hanski (1982)) for many organisms there is a positive correlation between local abundance and regional distribution;
i.e. species tend to be
either locally abundant
and widespread (core species) or locally rare and

428

ROBERT

F.

INGER

AND

HAROLD

K.

VORIS

regionally scarce (satellite species). An earlier paper (Inger 1969) on the frogs
of the streams at Nanga Tekalit noted that nine species accounted for >85%
of observations
and each contributed
>3.5% of the sample. Hanskis model
predicts that these nine species should have been equally abundant at Danum,
where streams were very similar to those at Nanga Tekalit in width, gradient,
and array of microhabitats.
Yet at Danum these nine species constituted <40%
of the total and four were completely absent: Amolops phaeomerus, Rana ibanorum,
R. hosei, and Bufo asper. Hanskis model also predicts that locally rare species
should not be ubiquitous;
yet of the ten species that occurred at seven or all
eight of our localities, six were rare (< 1% of sample) at Nanga Tekalit and
five were rare at Danum. The Bornean frogs do not fit Hanskis model.
Summary of between locality variation
(1) Inter-locality
overlaps of species abundances
were strongly affected by
stream width and gradient.
(2) Inter-locality
overlaps of species occurrences were affected by stream gradient but not by stream width.
(3) The magnitude
of inter-locality
overlaps (abundance
arrays and species
occurrences) were not related to distance between localities.
(4) Variation
between localities
in rainfall
had little
effect on overlap
(abundances and species occurrences).
(5) Inter-locality
overlaps were affected by species that have geographically
restricted ranges that cannot be related to distribution
of suitable microhabitats or ecological competitors.
CONCLUSION

Variation
over the time span of our study was relatively minor within communities. In contrast, variation
between communities
was appreciable,
but not
strongly related to distance. Overlaps between pairs of streams at a locality,
involving
distances < 13 km, were generally higher than overlaps of pairs of
streams from different localities. Yet distances between localities, 45-640 km,
were not correlated with overlap values. In part, the lack of correlation may be
traced to ten species that occurred at seven or eight of the localities. The ubiquity of these species reflects the similarity
of some microhabitats
across most
or all of the territory studied.
Nonetheless, environmental
variables had a clear effect on variation between
communities.
The principal
factors were stream width and gradient, which
affected both intra-and
inter-locality
overlaps. Perhaps the most striking
example of the effect of differences in stream width was the overlap of abundance
arrays (0.07) between the Segaham (25 m) and its tributary the Marok (2 m).
The extreme example of effect of stream gradient was the Sungai Seran, the
only stream flowing through flat terrain and the only one having a silt bottom
and completely
lacking riffles and torrents; it lacked all the species known to

Variation among frog communities

429

breed in clear, turbulent

water, i.e. roughly a quarter of the species in our
study.
There were significant differences within and between localities in rainfall,
both on an annual basis and at the times of sampling. Yet this variation did
not account for differences in overlaps among communities.
Although environmental
factors had strong effects on inter-locality
overlaps,
they do not account for all of the variation. At least 11 species have geographically restricted ranges that cannot be explained on the basis of distribution
of
suitable microhabitats.
Nine of these co-occur with at least one similar congener
at one or more localities. Regional processes (sensu Ricklefs 1987), perhaps the
existence or timing of barriers to dispersal or the timing of speciation events,
appear to be responsible for their geographic restrictions
rather than biotic
interactions.
ACKNOWLEDGEMENTS

We wish to express our thanks to men of the Iban longhouse, Rumah Jimbong.
Without
their able assistance, none of the work at Nanga Tekalit would have
taken place. We also wish to acknowledge Lucas Chin, Director, and Charles
Leh, Zoologist, both of the Sarawak Museum,
who arranged for government
permits and eased many logistical problems. We are grateful to the authorities
of Sabah Parks, Sabah Forest Industries, and Yayasan Sabah for permission to
work in areas under their respective jurisdictions
and for living accommodations. We are also grateful to Sabah Parks and Universiti
Kebangsaan Malaysia
(Kampus
Sabah) for provision of camping equipment,
transportation,
and
logistical assistance. We thank R. B. Stuebing, F. L. Tan, and P. Yambun for
assistance in the field and for many kindnesses. Professional colleagues, J. P.
Bacon, S. Emerson, K. J. Frogner, W. Hosmer, D. Karns, F. W. King, J. C.
Murphy, and P. Walker, helped us collect at various times. We are grateful to
M. Lloyd and B. Zimmerman
for helpful comments on the manuscript.
We
received valued technical assistance from A. Resetar. Field and laboratory work
were partially supported by grants from the National Science Foundation,
the
Allen-Heath
Memorial
Foundation,
and the National Geographic
Society.

LITERATURE

CITED

CRUMP,
M. L. 1971. Quantitative
analysis of the ecological distribution
of a tropical herpetofauna.
Occasional
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DUELLMAN,
W. E. & LYNCH,
J. D. 1969. Descriptions
ofhlopus
tadpoles and their relevance to atelopodid classification.
Herpetologica 25~231-240.
GASCON,
C. 1991. Populations
and community-level
analyses of species occurrences
of Central Amazonian
rainforest
tadpoles. Ecology 72: 1731-l 746.
HANSKI,
I. 1982. Dynamics
of regional distribution:
the core and satellite species hypothesis.
Oikos 38:210221.
HEYER,
W. R. 1973. Ecological interactions
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of HerpGtologr 7~337-361.

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INGER

AND

HAROLD

K.

VORIS

HORN,
H. 1966. The measurement
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INGER,
R. F. 1966. The systematics
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INGER,
R. F. 1969. Organization
of communities
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of Animal Ecology 38123-148.
INGER,
R. F. 1972. Bufo of Eurasia. Pp. 108-l 18, 357-360 in Blair, F. W. (ed.). Evolution in the genus Bufo.
University
of Texas Press, Austin.
INGER,
R. F. 1985. Tadpoles of the forested regions of Borneo. Fieldiana: Zoology (n.s.) 26:1-89.
INGER,
R. F. 1992. Variation
of apomorphic
characters
in stream-dwelling
tadpoles of the bufonid genus
Ansonia (Amphibia:
Anura).
Zoological Journal of the Linncan Society 105:225-237.
INGER,
R. F. & COLWELL,
R. K. 1977. Organization
of contiguous
communities
of amphibians
and
reptiles in Thailand.
Ecological Morwgraphr
47~229-253.
INGER,
R. F. & DRING,
J. 1988. Taxonomic
and ecological
relations of Bornean
stream toads allied to
Ansonia leptopus (Guenther)
(Anura:
Bufonidae).
Malayan Nature Journal 419:461-471.
INGER,
R. F. & GREENBERG,
B. 1966. Ecological
and competitive
relations among three species of frog
(genus Rana). Ecology 47~746-759.
INGER,
R. F. & STUEBING,
R. B. 1991. Frogs of Sabah. Sabah Parks Publication, no. 10.
INGER,
R. F. & STUEBING,
R. B. 1992. The montane amphibian
fauna of northwestern
Borneo. Muluyun
Nature Journal 46:41-5 1.
INGER,
R. F., VORIS,
H. K. & FROGNER,
K. J, 1986. Organization
of a community
of tadpoles in rain
forest streams in Borneo. Journal of Tropical Ecology 2: 193-205.
LLOYD,
M., INGER,
R. F. & KING,
F. W. 1968. On the diversity
of reptile and amphibian
species in a
Bornean rain forest. American Naturalist 102:497-515.
MATSUI,
M. 1986. Three new species of Amolops from Borneo. Copeis 1986:623-630.
McDIARMID,
R. W. 1978. Evolution
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G. M. & Bekoff,
M. (eds). The development of behavior: comparative and evolutionary aspects. STPM Press, New York.
RICKLEFS,
R. E. 1987. Community
diversity:
relative roles of local and regional processes. Science 235:167171.
TOFT,
C. A. & DUELLMAN,
W. E. 1979. Anurans
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H. 1981. Similarity
indices, sample size and diversity.
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Accepted

27 April

s.

1993

Variation among frog communities

APPENDIX

A.

Site

Site characteristics.

Upper

four in Sarawak,

Segaham

1 37N/113
35E
loo-230
hilly
primary
forest

3 7/113 48E
<200
hilly
primary
forest

2 44N/113
135-610
steep

6
3-14
moderate
clear
sand to bedrock

1
12
moderate
clear
sand to rock

2
2-25
steep
clear
Ige rock to bedrock

Mar/Aug

Apr/Jun

Sep 62lSept 63 365 d

Apr/Jul
70 94 d
Mar/Apr
84 28 d
1

Site

Danum

Marak-Parak

Mendolong

Purulon

Coordinates
Elevation
(m)
Topography
Vegetation

5 12N/117
50E
170-200
hilly
primary
forest

6 18N/116
42E
200
hilly
old 2nd forest

4 54N/115
42E
600-1350
hilly
logged forest

5 13N/115
57E
300-430
steep
primary
forest

Streams:
number
widths (m)
gradient
clarity
bottom

4
8-14
moderate
clear
sand to Ige rock

1
12
moderate
clear
Ige rock

1
12
steep
clear
Ige rock to bedrock

2
8-9
steep
clear
Ige rock to bedrock

Oct/Dec
Oct/Dec
Oct/Dec
8

OctlNov

NovlDec
87 25 d
Jul/Aug
89 29 d
Aug 90 22 d
5

Jun/Jul89
28 d
Sep 90 23 d

(m)

Streams:
number
widths (m)
gradient
clarity
bottom
Dates:
first
second
third
Locality
(Figure

first
second
third
Locality
(Figure

Nanga

3 21N/113
27E
Cl00
flat
primary
forest

1
10
low
turbid
mud

Ott

63/Feb

64 128 d

Tekalit

four in Sabah.
Pesu

Coordinates
Elevation
Topography
Vegetation

Labang

lower

431

64 155 d

55E

84 61 d

1)

1)

86 53 d
89 45 d
90 55 d

88 23 d

432

ROBERT

F.

INGER

B. List of species and specimens.

& Stuebing (1991).

SPECIES
cavitympanum
orphnocnemis
phaeomerus
poecilus
whiteheadi
albomaculata
leptopus
longidigita
spinulafer .

0
0
90
13
0
0
32
0
0

0
0

0
0

83
4
0
0
12
0
0

107
52
2
0
0
0
0
0
0
8
0

121
0
2
0
0
1
0
0
0
20
0

Bufo asper
Bufo divergens
Bufo juxtasper
Chaperina furca
Leptobrachella
Leptobrachella
Leptobrachella
Leptobrachella
Leptobrachium
Leptobrachium
Leptobrachium

baluensis
mjobergi
parva
serasanae
hendricksoni
montanum
nigrops

Leptolalax

gracillis

Megophrys
Megophrys

edwardinae
nasuta

Micrixalus
Microphyia

baluensis
petrigena

Occidoqga

baluensis

3
0
0

VORIS

Sex-bong

Selubok

given

in Inger

Wong

Lawan

0
0

0
0

330
28
0
0
21
0
0

107
13
0
0
20
0
0

2
12
0
0
5
0
0

0
0
0

71
11
0
0
0
1
0
0
0
9
0
5

45
0
0
0
0
1
0
0
0
5
0
3

15
48
1
0
0
17
0
0
0
3
0
7

14
1
0
0
0
0
0
0
0
0
0
1

0
0

0
4

2
3

(1966,

1985) and

Segaham
Segaham

Marok
3
0
1
3
0

28
0
1
76
0
137
1
0
0

2
0
0
3

13
0
83
0
0
0
0
0
0
0
0

1
0
8
0
0
96
4
0
0
20
0

1
2

3
0
0

2
0

143
0
0
2
0
0

1
14

0
2

0
1

0
0

1
1

0
2

1
0

12
0

10

0
48
0

5
106
0

50
0

29
0

1
1
0

4
0
0

0
6
2

0
1
0

disgregus
hosei
tectus

0
6
0

0
0
0

0
4
0

0
5
1

0
27
0

0
8
0

0
0
0

0
0
5

baramica
bbthi
chalconota
glandulosa
hosei
ibanorum
ingeri
kuhli
laticeps
malesiana
paramacrodon
sign&a

0
257
171
0
100
247
12
12
0
0
0
69

0
307
156
0
56
141
82
14
0
0
0
150

0
292
200
0
36
199
43
9
0
0
0
272

0
200
125
0
20
191
44
17
0
0
0
23

0
10
45
0
4
25
1
16
0
0
0
10

0
30
135
0
0
22
18
55
0
0
0
11

0
18
70
0
117
26
3
0
0
0
0
2

0
14
5
0
2
0
0
78
2
0
0
1

1
3
18

0
7
2

0
1
11

0
10
4

0
1
0

0
1
1

0
0
11

0
0
1

1
2
0
1281

7
3
0
1221

6
3
0
1664

3
0
0
870

4
80
7
349

2
15
0
468

5
2
0
605

0
7
21

Pedostibes hosei
Pedostibes rugosus
Philautus
Philautus
Philautus
Rana
Rana
Rana
Rana
Rana
Rana
Rana
Rana
Rana
Rana
Rana
Rana

Sekentut

K.

for species names

Nanga
Tekalit
Ensurai

ANURAN
Amolops
Amolops
Amolops
Amolops
Amolops
Ansonia
Anronia
Ansonia
Ansonia

HAROLD

Authorities

APPENDIX

Inger

AND

Rhacophorus bimaculatus
Rhacophorus gauni
Rhacophorus pardalis
Staurois latopalmatus
Staurois natator
Staurois tuberlinguis
TOTALS

292

&

Variation among frog communities

Labang
Seran

Marak
Parak
Surinsin

Purulon
Purulon

Kilampon

Danum
Cabin

P.Tambun

SKalison

W6S5

Mendolong
Mendolong

0
0
0
0
0

0
0
0
0
0

2
31
0
0
0

2
218
0
0
29

25:
0
0
5

0
96
0
0
0

0
161
0
0
0

0
66
0
0
0

0
108
0
0
0

3
216
0
0
161

0
1
0
0

0
0
0
0

0
0
0
0

0
0
0
0

0
0
0
0

0
20

0
5
0
2

0
0
0
3

0
0
124
0

217
2
6

27
0
0

1
0
53

2
0
60

0
1
22

0
2
18

0
2
1

0
0
13
0

0
0
0
0
1
0
0
0

0
00
0
0
0
2
2
0

0
0
0
0
0
0
0
3

3
0
0
0
0
0
6
0
18

0
1
0
0
0
1
3
0

0
0
12
0
0
5
0
34

0
0
4
0
0
0
0
14

0
0
0
0
0
0
3
0

0
0
0
60
0
0
2
0

16

0
0
0
3
0
0
1
0
18

32

0
0

0
0

0
0

0
0

0
5

0
0

0
6

0
0

0
4

0
0

0
0
0

0
0
0

0
0
0

2
0
0

5
0
2

2
0
0

3
0
0

3
0
0

8
0
0

2
0
0

60
0

18
0

0
0

0
0

1
241
118
315
187
5
181
10
0
0
0
379

0
0
0
14
38
57
155
0
0
61
0
0
1
9
7

0
0
0
0
0
1
0
14
0
0
5
0
0
0
0

0
0
0
0
0
9
0
4
0
0
50
0
0
0
10

15
0
0
0
0
0
20
50
0
0
0
6
30
0
0
0
14

42
0

0
0
1

0
0
0
0
0
0
0
1
0
1
0
0
48
0
0
0
24

1
0
0
0
235
48
0
0
0
1
91
0
0
0
56

12
0
0
5
0
0
83
37
0
0
0
1
17
0
0
0
82

1
0
4
0
0
0
10
33
0
0
0
0
113
0
0
0
21

0
0
0
1
0
0
0
73
0

5
0
19

11
0
7

0
1
0

0
1
0

0
3
0

0
9
0

0
42
2

0
19
1

0
20

0
11
1
1761

0
2
0
411

136
1
1
207

20
73
15
514

6
63
11
549

5
6
0
276

32
39
0
851

0
73
0
451

0
7
3
4
26
0

Pew
Pesu

2:
0
2:
6
0
0
0
0
0
4
0

400

11
22
177
844