142
BIOTROPICA 33(1): 142?152 2001
Herpetofaunal Diversity and Abundance in Tropical Upland
Forests of Cameroon and Panama1
Ulrich Hofer2
Department of Vertebrates, Natural History Museum, Bernastrasse 15, 3005 Berne, Switzerland
and
Louis-Fe?lix Bersier
Zoological Institute, University of Neucha?tel, rue Emile-Argand 11, 2007 Neucha?tel, Switzerland
ABSTRACT
Two tropical upland forests, Mount Kupe in Cameroon and Bosque Protector Palo Seco in Panama, were compared
in terms of herpetofaunal species richness and density of individuals. Based on rarefaction, whereby samples are
standardized for abundance, Palo Seco had signi?cantly more species of frogs and lizards. Extrapolations to total local
species richness, by ?tting the Michaelis?Menten equation to the species accumulation curves and by using Chao's
estimator, yielded divergent results: more lizard species on Mount Kupe, and an equal number of frogs at both sites.
These disparities can be accounted for by differences in evenness, which was higher in Palo Seco. Frog density was
signi?cantly higher on Mount Kupe, snake density signi?cantly higher in Palo Seco, and lizards exhibited no density
difference. Overall, the results revealed a less consistent pattern and more moderate differences than what is known
from southeast Asian?Central American comparisons. This outcome is discussed in the light of available knowledge,
but quantitative data from African forests are too sparse to allow general conclusions.
RESUMEN
Se comparo? la herpetofauna de dos bosques tropicales hu?medos ubicados en las montan?as, Mount Kupe en Cameru?n
y Bosque Protector Palo Seco en Panama?, en relacio?n a la riqueza espec???ca y la densidad de individuos. Con base
en el me?todo de rarefaccio?n,en el cual los muestreos se estandarizan en base a su abudancia, Palo Seco presenta
signi?cativamente ma?s especies de anuros y lagartos. Extrapolaciones con respecto a la riqueza espec???ca total de los
sitios, mediante un ajuste de la ecuacio?n de Michaelis?Menten a las curvas de acumulacio?n de especies, y utilizando
el ??ndice de Chao, produjeron resultados divergentes: ma?s especies de lagartos en Mount Kupe, y el mismo nu?mero
de especies de anuros en ambos sitios. Dichas diferencias pueden resultar de una equitatividad ma?s alta en Palo Seco.
La densidad de anuros resulto? signi?cativamente ma?s alta en Mount Kupe, mientras que la densidad de serpientes fue
signi?cativamente ma?s alta en Palo Seco, y no se encontro? una diferencia entre la densidad de lagartos en ambos
sitios. En general los resultados muestran patrones menos consistentes y diferencias ma?s moderadas de las que se
conocen entre el Sureste de Asia y Centroamerica. Se discuten los resultados con base en la informacio?n disponible,
sin embargo, la existencia de datos cuantitativos para bosques africanos es demasiado escaza como para permitir
conclusiones generales.
Key words: Amphibia; Cameroon; density; evenness; Panama; Reptilia; species richness; tropical wet forest.
COMPARING SAMPLES OF AMPHIBIANS AND REPTILES
from Neotropical and southeast Asian lowland rain
forests revealed that both diversity and density are
higher in the Neotropics. Samples usually encom-
passed the leaf litter zone or a single type of mi-
crohabitat. Heyer and Berven (1973) and Voris
(1977) analyzed the tree buttress microhabitat and
based their comparisons on average species diversity
per individual, thus incorporating both species
richness and evenness. Diversity of amphibians and
1 Received 19 February 1999; revision accepted 9 No-
vember 1999.
2 Corresponding author: E-mail: Ueli.Hofer@cscf.unine.ch
reptiles found on tree buttresses was higher in the
Neotropical collection and the authors concluded
that overall herpetofaunal diversity in a given rain
forest largely determines the diversity associated
with a particular microhabitat. Scott (1976) and
Inger (1980a) compared the densities of non-ri-
parian leaf litter herpetofaunas. Standardized to the
number of individuals per 100 m2, Central Amer-
ican lowland forest densities were about an order
of magnitude higher than in Indo-Malayan ones, a
result supported by further data from Central
American sites (Toft 1980, Lieberman 1986, Fauth
et al. 1989). Scott (1976) also included upland sites
and found densities of Costa Rican leaf litter her-
Herpetofaunal Diversity in Cameroon and Panama 143
petofaunas almost six times higher than those re-
ported by Brown and Alcala (1961) for the same
elevations on Cuernos de Negros, Philippine is-
lands. Scott (1976) attributed these differences to
greater litterfall and faster decomposition rates in
Neotropical forests. Finding no such difference in
ecosystem function, Inger (1980a) suggested that
population levels in the Indo-Malayan forests are
kept below those achieved in Neotropical forests
primarily by a reduced food supply. The latter
would result from the synchronized mast fruiting
of the dipterocarp trees dominating these forests,
which reduces the number of seed-eating insects
and associated arthropod predators on the forest
?oor. In a brief review of the topic, May (1980)
favored Inger's explanation, but emphasized the
need for a con?rmation of the postulated arthro-
pod density differences.
While the cited studies revealed consistent dif-
ferences between Central America and southeast
Asia in diversity and density of lowland forest am-
phibians and reptiles, Afrotropical herpetofaunas
remained virtually excluded from such compari-
sons, as data sets equivalent to those from the other
two continents were scarce. Scott (1982) presented
the ?rst inter-site comparison, based on a sample
of 15 forest litter plots and 66 person-hours of col-
lecting effort in a Cameroonian lowland forest on
white-sand soil. The herpetofaunal species richness
in the African leaf litter samples was about half that
found in equivalent-sized samples from lowland
forests of Borneo and Costa Rica (Scott 1982).
Densities of individuals were ca 60 percent of those
found in Central America, but six times the den-
sities on Borneo. Using simple life history data on
habitat, activity period, breeding site, and size class,
Lawson (1992) assessed the similarity in ecological
structure of the herpetofaunal assemblages of Ko-
rup, Cameroon, and Santa Cecilia, Ecuador. Frogs
exhibited little overlap in distribution among life
history types, a ?nding attributed to differences in
types of breeding sites available; squamates showed
such a dissimilarity, although they were ecologically
more diverse in Korup. The two sites had similar
species numbers, but this comparison was not stan-
dardized for area or effort. On a broad level, Duell-
man (1993) and Bauer (1993) provided compre-
hensive comparisons of the amphibian and reptile
faunas of Africa and South America. Standardized
to a 106-km2 scale, amphibian species density in
montane rain forests of South America was 1.7
times that of Africa, while for lowland forests, den-
sity in Africa was 1.2 times that of South America
(Duellman 1993). For reptiles, Bauer (1993) com-
piled continent-wide totals of taxa and country by
country summaries for the major groups, but did
not include standardizations for area and vegetation
types.
In this paper, we compare local species richness,
evenness, and density of amphibians and reptiles in
an Afrotropical and a Central American upland
forest. We use two original data sets obtained by
the same sampling method from Mount Kupe in
Cameroon, and from Bosque Protector Palo Seco
in western Panama. As Voris (1977) has pointed
out, comparisons of diversity between sites often
are biased by unresolved differences in the length
of the collecting period, the number of major hab-
itats sampled, and the size of the area censused,
thus affecting sample sizes and total numbers of
species. We accounted for these concerns by ad-
justing both data sets in a way that total sampling
effort, forest type, elevational range, and season
were comparable.
METHODS
STUDY SITES.?Mount Kupe (48459N) in the south-
west province of Cameroon, is a steep-sided, cone-
shaped mountain 2064 m in height and situated
ca 100 km northeast of Mount Cameroon. It forms
part of the Cameroon Highlands, an extensive vol-
canic mountain range in western Cameroon, run-
ning from Mount Cameroon in the southwest tip
of the country (ca 500 km toward the northeast to
the Bamenda and Adamawa Highlands). At the
time of the sampling, the upper slopes of the
mountain (between 900 m and the summit) were
covered by ca 2100 ha of undisturbed closed can-
opy submontane forest, characterized by a fairly
uniform structure with a sparse ground layer and
a thin understory. Below 900 m, the forest has been
logged or severely degraded except for a few patches
on the southwestern and southern slopes. In the
primary forest, we found permanent streams be-
tween 900 and 1500 m and at 1900 m. The single
standing body of water found within the primary
forest was a puddle on a log in a treefall. Mount
Kupe receives a mean annual rainfall of 4891 mm
(Suchel 1972), with monthly precipitation never ,
70 mm. The rainy season lasts for seven months
(April?October).
The Bosque Protector Palo Seco (88479N) in
Bocas del Toro province of Panama, is situated on
the Caribbean slope of the Cordillera Central. It is
a vast area of primary forest extending vertically
from the lowlands up to the continental divide,
with ridgetops and peaks at ca 1400 to 2200 m.
144 Hofer and Bersier
TABLE 1. Sampling characteristics in two tropical upland forests: Bosque Protector Palo Seco, Panama, and Mount Kupe,
Cameroon.
Palo Seco, Panama Mount Kupe, Cameroon
Elevational range (m)
Total transect length (m)
Number of sampling bouts
Person-hours of sampling
Number of days
Start day
800?1600
2610
32
9.8 h/bout
935
4 May 1998
900?1700
2820
56
3.8 h/bout
35
9 May 1994
Horizontally, Palo Seco extends from the main road
that crosses the divide and links the two provinces
of Chiriqu?? and Bocas del Toro farther west to Cos-
ta Rica.
Despite the status of a protected forest, human
impact is increasing, with pastures along the valley
bottoms and plantations on the adjacent slopes. Es-
timated from regional climate maps (Instituto Geo-
gra?co Nacional Tommy Guardia 1988), Bocas del
Toro province receives an annual rainfall from ca
3000 mm in the lowlands to 5000 mm at higher
elevations. Other than on the Paci?c slope, rainfall
is abundant throughout the year, and without a
pronounced dry season. We found permanent
streams at all elevations sampled, whereas puddles
along an unpaved road outside the forest were the
only standing water located. As on Mount Kupe,
most stream bottoms are bedrock, with moderate
to steep gradients, rapids, and splash zones. Most
herpetological work in western Panama has focused
on the Paci?c side and the vicinity of Reserva La
Fortuna, but the Palo Seco area has received little
attention from herpetologists.
DATA ACQUISITION.?At both sites, the sampling
method adopted was `` cruise collecting''; (i.e., three
to ?ve people walked slowly along a transect, mov-
ing ?oor debris, turning logs and stones, ripping
apart rotten wood, digging soil in the root system
of big trees and under logs, and inspecting the herb
and shrub layer up to ca 10 m; Inger & Colwell
1977). In riparian zones, the streambed also was
examined. The data on Mount Kupe were acquired
between March and November 1994, in the pri-
mary forest on the western slope of the mountain
between 900 m and the summit; procedures are
outlined in more detail in Hofer et al. (1999). Data
in the Palo Seco area were acquired between April
and June 1998. Fieldwork was restricted to the pri-
mary forest between 800 and 1600 m elevation at
the eastern edge of the forest reserve. The transect
samples were taken along 430 m of a trail main-
tained by workers from the Instituto de Recursos
Hidra?ulicos y Electri?cacio?n and by the local citi-
zens, along 1360 m of trails opened by our ?eld
crew and along 820 m of streamsides. Basic infor-
mation on sampling at both study sites is sum-
marized in Table 1.
On Mount Kupe, animals we did not collect
as vouchers were marked and released at the end
of each sampling bout, and recaptured animals
were excluded from all analyses. The abundance
data of two chameleon species we failed to mark
reliably were retained in the data set. The mean
recapture rate of all species reliably marked was
2.75 percent. Due to a drastic decline in amphibian
populations in Costa Rica and adjacent western
Panama (see Discussion), our research permits re-
stricted collecting efforts to the minimum number
of individuals necessary for accurate species iden-
ti?cation, and banned marking of individuals. For
the latter reason, the abundance of some species
may be overestimated. Assuming a similar mean
recapture rate as on Mount Kupe, this sampling
error would be ?ve individuals. Voucher specimens
from the two sites were deposited at the Natural
History Museum of Berne, the Alexander Koenig
Zoological Research Institute and Zoological Mu-
seum in Bonn, and in the collections of the Mount
Kupe Forest Project, Nyasoso, Cameroon, and
those of the C??rculo Herpetolo?gico de Panama?.
ANALYSIS.?Customarily, tropical herpetofaunas
have been compared on the basis of species rich-
ness, evenness, density, and dominance. We re-
stricted our analyses to the ?rst three measures, and
as suggested by Gotelli and Graves (1996), used
indices that had a probabilistic basis and tended to
be unbiased by sample size. First, we applied an
interpolation procedure: species richness of the two
samples was compared by rarefaction (Sanders
1968, Hurlbert 1971, Simberloff 1972), whereby
samples were standardized for abundance. Second,
we extrapolated to total species richness by ?tting
a Michaelis?Menten equation (Raaijmakers 1987)
to the species accumulation curves, and by com-
Herpetofaunal Diversity in Cameroon and Panama 145
FIGURE 1. Species accumulation curves for (a) frogs
and (b) lizards. Due to small sample sizes, no curves were
drawn for the snakes. Error bars indicate 6 1 SD.
puting Chao's (1984) nonparametric estimator. As
an evenness measure, we computed Hurlbert's
(1971) probability of an interspeci?c encounter.
Means and standard errors of this index were esti-
mated by a bootstrap procedure with 1000 itera-
tions (Efron & Tibshirani 1993). Due to the small
number of snakes obtained on Mount Kupe, we
excluded the snakes from all estimates of species
richness.
As a consequence of the ?eld methods chosen,
two properties of the data set had to be accounted
for. First, because trails were searched repeatedly in
the course of sampling both sites, trails could not
be treated as an equivalent to leaf litter plots of
previous studies (e.g., Inger & Colwell 1977, Scott
1982, Lieberman 1986). We therefore used samples
standardized by time effort to calculate animal den-
sities (number of frogs, lizards, or snakes encoun-
tered per person-hour of sampling). For each sam-
pling bout, we computed the time-based density;
from these densities, means and standard errors
were estimated for both sites. Second, samples
based on cruise collecting encompassed a wider ar-
ray of species than litter plots and usually included
taxa associated chie?y with microhabitats above the
forest ?oor. We therefore split three taxonomic
groups (frogs, lizards, and snakes) into an `` arbo-
real'' (species known to feed in vegetation) and a
`` terrestrial'' subset, and again computed the param-
eters for these six categories. Because such splitting
led to very small sample sizes for some subsets, we
do not present the results in tabular form, but refer
to them in the Discussion.
We accounted for differences between sites and
sampling efforts in two ways. First, we restricted
the analysis to data acquired within primary forest
(including riparian habitats). Furthermore, we ad-
justed the elevational range and the lengths of sam-
pling periods by reducing the larger sample (Mount
Kupe). This resulted in data sets accumulated over
the same number of days starting with the onset of
the rainy season. Thus, our density and local spe-
cies richness estimates were based on data sets ob-
tained by the same methodology from comparable
forest types, elevational ranges, and seasons. Sec-
ond, differences in sampling effort (Table 1) were
further taken into account by using rarefaction
methods.
For the extrapolations that predicted the total
regional species richness, we left the elevational
ranges adjusted, but used all data available for the
entire collecting period at both sites. We based the
accumulation curves on a similar number of sam-
pling bouts (some chronologically adjacent sam-
pling bouts were pooled). We followed Colwell and
Coddington's (1994) procedure to generate species
accumulation curves, performing 100 randomiza-
tions of the order of sample bouts. The Michaelis?
Menten equation was ?tted directly by use of a
nonlinear regression module in the SPSS package
(SPSS 1990). We used the sum of absolute values
of the residuals as the loss function, to avoid giving
too much weight to outliers. Con?dence intervals
of Michaelis?Menten parameters were computed
by a bootstrap procedure included in SPSS (1990).
RESULTS
The species list from Palo Seco is given in the Ap-
pendix, the corresponding data from Mount Kupe
are published in Hofer et al. (1999). Rarefaction
of such data entails several assumptions (Gotelli &
Graves 1996). First, the communities compared
must be taxonomically similar, come from similar
habitats, and be sampled with similar techniques,
concerns we accounted for as explained previously.
Second, sample size must be suf?cient to correctly
characterize the parent distribution. From inspec-
tion of the species accumulation curves (Fig. 1),
the frog and lizard sample sizes appear adequate.
Finally, the spatial distribution of individuals must
146 Hofer and Bersier
TABLE 2. Results of the runs tests (Zar 1974) performed
to evaluate clumping of conspeci?cs within
sampling bouts. For both sites, frogs and lizards
were analyzed separately for four bouts selected
at random from those that contained .7 spec-
imens.
Bout
Number of runs
Ob-
served Expected P
Frogs Mount Kupe 1
2
3
4
7
18
8
10
5.99
19.67
8.44
8.66
0.93
0.15
0.33
0.85
Palo Seco 1
2
3
7
7
5
7.42
6.93
5.83
0.37
0.51
0.19
Lizards Mount Kupe 1
2
3
4
9
9
7
5
9.17
8.35
6.89
5.80
0.42
0.69
0.53
0.21
Palo Seco 1
2
3
4
8
12
8
6
6.50
11.30
7.79
5.27
0.92
0.68
0.56
0.75
TABLE 3. Distances between empirical species accumu-
lation curves and those obtained by 100 ran-
dom assignments of individuals to sampling
bouts. Distances are expressed in units of SD
(N 5 100). The higher the value, the stronger
the departure from the homogeneity of the hab-
itat.
Distance in SD units
x? Maximum
Frogs Mount Kupe
Palo Seco
0.45
0.16
0.63
0.33
Lizards Mount Kupe
Palo Seco
0.77
1.33
1.46
1.95
FIGURE 2. Rarefaction curves for (a) frogs and (b)
lizards. Due to small sample sizes, no curves were drawn
for the snakes. Envelopes indicate the 95 percent con?-
dence limits.
be random. In the context of an elevational gra-
dient, this assumption stet likely to have been vi-
olated to some extent, since many species exhibited
gaussian-like abundance curves along the gradient;
however, the rarefaction model is mostly affected
by clumped distributions of conspeci?cs (Simber-
loff 1986). We controlled statistically for this prop-
erty by a runs test (Zar 1974), performed at each
site on a random selection of four sampling bouts
with . 7 individuals. The tests were run separately
for frogs and lizards. The power of the tests was
evaluated to ascertain that rejection of H0 was not
due to small sample size, which resulted in the
elimination of one sampling bout for the frogs at
Palo Seco. We found no indication of clumping of
conspeci?cs (Table 2). The ?tting of a Michaelis?
Menten equation to the species accumulation
curves assumes homogeneity of the habitat. The
homogeneity can be assessed by comparing the em-
pirical species accumulation curves to those ob-
tained by a random assignment of individuals to
sampling bouts (Colwell & Coddington 1994). In
a homogeneous habitat, the empirical curves will
?t the theoretical ones; in a heterogeneous one,
they will lie below. We found no strong departure
from the assumption of homogeneity, the empirical
curves lying at most 1.95 SDs below the theoretical
ones (Table 3).
Based on equal sample sizes, Palo Seco exhib-
ited a signi?cantly higher richness in frog and lizard
species than Mount Kupe (Fig. 2). The two ex-
trapolation methods yielded divergent estimates of
local species richness, especially for frogs, but var-
iance around these estimates was large (Table 4).
Despite their differences, the species accumulation
curves (Fig. 1) produced similar estimates to those
of the Michaelis?Menten equation, except for the
number of lizard species which was higher on
Mount Kupe (Table 4). With the Chao estimator,
differences between the two sites were accentuated:
however, based on nonoverlapping 95 percent con-
?dence intervals, the higher number of lizard spe-
cies on Mount Kupe was the only signi?cant dif-
Herpetofaunal Diversity in Cameroon and Panama 147
TABLE 4. Diversity and density parameters in two tropical upland forests. Expected species richness for equal sample sizes
was estimated by rarefaction; the sizes of the smaller samples are given in parentheses. The number of species
at both sites was extrapolated by ?tting the Michaelis?Menten equation, and by computing Chao's (1984)
estimator. Evenness is expressed as the probability of an interspeci?c encounter. Densities refer to numbers of
individuals per person-hour of sampling. When appropriate, the 95 percent con?dence intervals (ci) are added.
Asterisks (*) indicate signi?cant differences between Panama and Cameroon (P # 0.05). Due to small sample
sizes, snakes were omitted from all species richness estimates.
Palo Seco, Panama Mount Kupe, Cameroon
Observed number of species
Frogs
Lizards
Snakes
21
11
13
23
9
3
Estimate 95% ci Estimate 95% ci
Species richness based on rarefaction
Frogs (N 5 82)
Lizards (N 5 111)
21
11
?*
?*
16.1
8.8
15.4?16.7
8.5?9.1
Species richness extrapolated
(a) Fitted Michaelis?Menten equation
Frogs
Lizards
38.1
13.6
37.6?38.6
13.4?13.8*
37.7
16.6
37.0?38.4
16.4?16.8
(b) Chao's (1984) estimator
Frogs
Lizards
53.3
13.0
41.5?65.0
10.8?15.2*
44.0
19.5
40.2?47.8
15.9?23.1
Probability of an interspeci?c encounter
Frogs
Lizards
0.85
0.77
0.80?0.91
0.71?0.82
0.79
0.65
0.75?0.81
0.57?0.73
Density of individuals (N/sampling hour)
Frogs
Lizards
Snakes
0.25
0.35
0.14
0.16?0.35
0.23?0.47
0.08?0.20*
2.33
0.57
0.02
1.65?3.00
0.36?0.77
0.00?0.04
ference. The probability of an interspeci?c encoun-
ter among frogs and lizards was higher in Palo
Seco. Although the differences were not signi?cant,
the 95 percent con?dence intervals overlapped only
marginally, particularly for lizards (Table 4). Stan-
dardized to the number of specimens encountered
per person-hour of sampling, there was no differ-
ence in lizard density (t-test, two-tailed; P 5 0.14);
however, frog density was nine times higher on
Mount Kupe (t-test, two-tailed; P , 0.0001), and
snake density seven times higher in the Palo Seco
forest (t-test, two-tailed; P , 0.0001).
DISCUSSION
AMPHIBIAN DECLINE IN CENTRAL AMERICA.?Because
no quantitative data are available for the Palo Seco
area prior to an amphibian decline reported for Cos-
ta Rica and adjacent Panama (Lips 1998, 1999), the
effect of this recent disturbance on the abundance
and species richness of amphibians and reptiles ob-
served today is unknown; however, the watershed of
the R??o Chiriqu?? on the Paci?c side of Panama,
where Lips (1999) found a sudden and massive de-
cline in anuran abundance and diversity in late
1996, is separated only by a narrow ridge from the
nearest watercourse of the Palo Seco area, hardly suf-
?cient to prevent spreading of the suspected fungal
pathogen to the adjacent Atlantic side. Furthermore,
our frog density estimates were as low as those found
by Lips (1999) after the decline. We therefore con-
sider it probable that the phenomenon also affected
frog populations in Palo Seco, accounting for the
remarkable difference in density observed between
this site and Mount Kupe. The difference is largely
attributable to higher numbers of individuals (of
species) dwelling on the forest ?oor (leaf litter and
riparian) of Mount Kupe. Effects on species richness
and evenness are less comprehensible, because these
properties tend to be biased if some species show a
particularly strong response to the pathogen. Lips
(1998, 1999) found streamside anurans with an
aquatic stage to be more affected than other taxa.
The density of these species in Palo Seco was 0.05
individuals/person-hour of sampling, while on
Mount Kupe it was 0.7.
SPECIES RICHNESS AND EVENNESS.?Standardized for
sample size, frog and lizard species numbers were
signi?cantly higher in Panama. Frog species rich-
ness in the Palo Seco forest was 1.3 times greater
than on Mount Kupe, but below the value evalu-
148 Hofer and Bersier
ated by Duellman (1993) on a continent-wide 106-
km2 scale; in that study, amphibian species density
in montane rain forests of South America was 1.7
times that of Africa. Inequalities in seasonality and
dry season length, factors invoked to explain dif-
ferences in species richness between other sites (In-
ger 1980b, Scott 1982), were presumably of minor
importance in our case. High annual rainfall and
the lack of a pronounced dry season at both sites
should minimize potential effects of climatic prop-
erties. The higher species richness in the Palo Seco
forest, when standardized for sample size, may re-
sult simply from a species?area relationship and an
island effect (MacArthur & Wilson 1967). As part
of an extended forest range covering the entire Ca-
ribbean slope of the Cordillera Central from sea
level to ca 2300 m, Palo Seco supports more species
than the relatively isolated forest block on Mount
Kupe, which is situated in a highland area where
ca 50 percent of the anuran species and at least 40
percent of the lizards are endemic. Of the 46 spe-
cies of amphibians and reptiles endemic to Panama
(R. Iba?n?ez, pers. comm.), 5 amphibian (Dendro-
bates speciosus, Eleutherodactylus emcelae, E. museo-
sus, Bolotiglossa minutula, and Caecilia volcani) and
2 lizard species (Anolis casildae and A. exsul) were
found at Palo Seco, along with 5 undescribed taxa
that may be endemic to the area.
Estimates of total species richness did not differ
between the two sites for frogs, but lizard species are
probably more numerous on Mount Kupe. Mount
Kupe is situated in an area known for exceptional
herpetofaunal diversity. The Cameroon Highlands
may exhibit the highest level of herpetofaunal en-
demism in all of mainland Africa; more than 60
amphibians species are restricted to this region (Jen-
kins & Hamilton 1992) and a large number of liz-
ard taxa are undescribed. The adjacent Korup Na-
tional Park is among the most herpetologically di-
verse areas in the world (Lawson 1992). Due to col-
onization from two directions (South America and
the northwest), however Panama probably has the
most diverse herpetofauna in Central America. (R.
Iba?n?ez pers. comm.). Duellman (1993) has ex-
plained that the higher amphibian species richness
in South America results, in part, because of an in-
?ux from Central America of taxa inhabiting humid
environments, while no equivalent dispersal has oc-
curred into sub-Saharan Africa.
An intriguing result of our study was the dis-
crepancy between rarefaction and extrapolation es-
timates for the lizards; interpolation indicated higher
species richness for Palo Seco, while both extrapo-
lation methods found the opposite. This inconsis-
tency can be explained by inter-site differences in
evenness, differences in the degree of heterogeneity
of the habitats, or both. On one hand, the more
uneven the distribution of species abundances, the
sooner species are eliminated in a rarefaction pro-
cedure. On the other hand, given the same species
abundance pro?les, the more heterogeneous a hab-
itat, the higher the probability of ?nding new species
during the entire sampling period; consequently, the
species accumulation curve in a heterogeneous hab-
itat will not attain an asymptote as rapidly as in a
homogeneous one. Thus higher estimates of species
richness will be produced. We found that Palo Seco
exhibited a slightly higher degree of heterogeneity
than Mount Kupe; thus, differences in habitat het-
erogeneity cannot explain the con?icting estimates.
More likely, they resulted from a difference in even-
ness between the two sites, suggested by the higher
probability of an interspeci?c encounter among liz-
ards in Palo Seco (Table 4). This outcome may have
re?ected divergent community structures, in that the
Mount Kupe lizard assemblage was dominated by a
few abundant species. It further demonstrates that
the use of different estimators of species richness can
reveal subtle differences in community organization
otherwise easily overlooked.
DENSITY.?The remarkable inequality in snake
abundance resulted from a much higher density of
arboreal species in Palo Seco. The species most
commonly encountered in Panama were the arbo-
real colubrids Sibon dimidiatus and Imantodes cen-
choa, while on Mount Kupe, the small leaf litter
colubrid Buhoma depressiceps was observed most
frequently. The conspicuous difference in relative
representation of arboreal and terrestrial taxa in the
two snake faunas may have resulted from the lack
of a lineage of arboreal gastropod-feeders in the
African snake fauna, a niche ?lled by a group of
xenodontine colubrids in the Neotropics (in Palo
Seco, represented by the genus Sibon). In a quali-
tative comparison of the equatorial amphibians and
reptiles in Africa and South America, Laurent
(1973) found several examples of empty niches on
both continents. An impact of phylogeny and his-
torical events on contemporary patterns of com-
munity organization was also suggested by Cadle
and Greene (1993) to explain differences in com-
position and species richness among Neotropical
rain forest snake assemblages.
Murphy et al. (1994) compared snake densities
from several tropical areas based on catch per day.
A lack of detailed information on sampling effort
and crew sizes for most sites prevented standardi-
Herpetofaunal Diversity in Cameroon and Panama 149
zations to catch per person-day, and the numbers
of people involved in sampling undoubtedly ac-
counted in part for observed differences. Despite
its inherent inaccuracy, the stet-per-stet measure re-
vealed that Palo Seco and Mount Kupe fell at op-
posite ends of the range reported by others. The
2.1 encountered in Palo Seco is close to the 2.25
of Dunn's (1949) large snake collection obtained
in Panama and greater than the rates from three
South American lowland sites: 0.39 snakes/d in
Santa Cecilia, Ecuador (Duellman 1978) and Kar-
tabo, Guiana (Beebe 1946), and 0.47 snakes/d in
Manaus, Brazil (Zimmerman & Rodriguez 1990).
Our encounter rates at Palo Seco also exceed rates
from Southeast Asia (0.97 in lowland sites on Bor-
neo [Murphy et al. 1994] and Thailand [Inger &
Colwell 1977]). With 0.2 snakes/d, Mount Kupe
fell at the lower end of this range. Janzen (1976)
has suggested that the biomass of African reptiles
is depressed by increased predator pressure, a factor
that may have contributed to the strikingly low
snake density on Mount Kupe.
Unlike the snakes, the lizard faunas at the two
sites were similar both in density and in relative
representation of arboreal and terrestrial taxa. Frog
density was higher on Mount Kupe, but, provided
that the current frog density in the Palo Seco forest
resulted from a recent disturbance depressing pop-
ulation levels in western Panama, the difference ul-
timately may become less pronounced.
Together with Scott's (1982) estimates, our re-
sults suggest that frog and lizard densities of African
forests may be intermediate to Central American
and Asian sites, but closer to the former; however,
additional quantitative data from African forests are
needed to con?rm such a trend. The ?nding of a
consistent pattern may stimulate research related to
the mast fruiting hypothesis (Inger 1980a).
Our results suggest that there is no simple re-
lationship between species richness and density of
individuals. Within the samples at each site, the
two parameters showed a signi?cant positive cor-
relation (r 5 0.60, P (0.001 and r 5 0.85, P
(0.001 for all species at Mount Kupe and Palo
Seco, respectively), a result also found by Lieber-
man (1986) for litter plots at La Selva, Costa Rica.
When comparing the two sites, however, the higher
frog species richness at Palo Seco was not coupled
with higher frog density, while the higher number
of snake species observed at this site was. Attempts
to link herpetofaunal density and species richness
between sites have led to contradictory conclusions.
Scott (1976) has suggested that density and species
richness of leaf litter herpetofaunas are inversely
correlated. From his Table 1 (p. 43), we found the
trend to be strongly affected by a single site (Sa-
rawak, Borneo). Removal of this site resulted in a
correlation in the opposite direction, but neither
correlation was signi?cant. Fauth et al. (1989)
found a signi?cantly positive correlation among
several Costa Rican sites. Part of the con?icting
results may stem from major differences in site
characteristics and in overall geographic range cov-
ered by the sites compared. Even so, we doubt that
species richness and density are linked in a system-
atic way (Begon et al. 1996); instead, they result
from different processes in which their relative im-
portance depends strongly on the regions consid-
ered, a fact that is dif?cult to account for in com-
parisons involving both parameters.
ACKNOWLEDGMENTS
Fieldwork in Cameroon was supported by grants from
the Swiss Development Corporation, the Swiss Academy
of Sciences, and the Natural History Museum of Berne.
The Mount Kupe Forest Project provided logistic help
and housing in Nyasoso. E. J. Ebung, E. H. Njume, and
N. S. Epie assisted the whole, and C. Wild and I. C.
Ojiawum, parts of the ?eldwork. C. Wild introduced U.
Hofer to the study area. U. Hofer greatly appreciates the
support of the Bakossi people stet Nyasoso; in particular,
K. E. Epie and E. E. Ewang. J.-L. Amiet, J.-L. Perret, W.
Bo?hme, A. Schmitz, and B. Hughes helped with the iden-
ti?cation of the collected specimens. Fieldwork in Panama
was supported by the Natural History Museum of Berne.
L. Indermaur, M. A. Aguirre, A. Gonza?les, and O. Sa-
mudio assisted the data acquisition. R. Iba?n?ez D. and the
C??rculo Herpetolo?gico de Panama? helped with the iden-
ti?cation of the collected specimens. For logistic support,
U. Hofer is indebted to M. A. Aguirre, R. Iba?n?ez D., N.
Go?mez, R. Borrell, the Smithsonian Tropical Research
Institute, the Instituto de Recursos Naturales y Renova-
bles, and the Instituto de Recursos Hidra?ulicos y Electri-
?cacio?n. For help and constructive criticism of the man-
uscript, we thank R. F. Inger, N. J. Scott Jr., R. Iba?n?ez
D., B. Benrey, and an anonymous reviewer. L.-F. Bersier
was supported by the Swiss National Science Foundation
grant 31-52566.97 and the Novartis Foundation.
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APPENDIX. Amphibians and reptiles recorded in the Bosque Protector Palo Seco, Bocas del Toro Province, Panama,
between 800 and 1600 m, April?June 1998. The abundance ?gures given are those used for further
analyses and refer to the numbers of animals taken during the timed sampling bouts. Taxa with no
abundances given were encountered outside sampling bouts, belong to orders not found on Mount Kupe
(Plethodontidae and Caeciliidae), or were only found in disturbed habitats (*), and therefore not included
in the analyses. Total number of frog, lizard, and snake species was 82, 111, and 44, respectively.
Amphibia Reptilia
Bufonidae Gekkonidae
Bufo coniferus* Lepidoblepharis xanthostigma 4
B. marinus* Gymnophthalmidae
Centronelidae Ptychoglossus plicatus 4
Centrolene prosoblepon 3 Polychrotidae
Hyalinobatrachium vireovittatum 3 Anolis aquaticus 13
Dendrobatidae A. biporcatus 5
Colostethus nubicola 1 A. casildae 3
Dendrobates speciosus 2 A. exsul 2
Hylidae A. humilis 44
Agalychnis spurrelli 3 A. limifrons 9
Hyla debilis 1 A. pachypus 25
H. lancasteri 1 Anolis sp. A 1
H. picadoi 1 Anolis sp. B 1
Smilisca phaeota*
Leptodactylidae
Eleutherodactylus bransfordii 4 Colubridae
E. caryophyllaceus 27 Amastridium veliferum 1
Eleutherodactylus cf. diastema Chironius grandisquamis 2
E. crassidigitus 2 Colubridae sp. nov. 2
E. cruentus 11 Dendrophidion paucicarinatum
E. diastema 4 Geophis brachycephalus 1
E. emcelae 1 Imantodes cenchoa 11
E. ?tzingeri 1 Leptodeira septentrionalis 2
E. gollmeri Liophis epinephalus 1
E. melanostictus 1 Sibon argus 3
E. museosus 1 S. dimidiatus 17
E. pardalis 6 S. nebulatus 2
E. podiciferus 3 Urotheca decipiens 1
E. ridens 1 U. euryzona
Eleutherodactylus sp. nov. 5 Xenodon rabdocephalus*
Elapidae
Micrurus alleni*
Plethodontidae Viperidae
Bolitoglossa colonnea Bothriechis lateralis
B. minutula Bothrops asper*
Bolitoglossa sp. nov. Lachesis stenophrys 1
Caeciliidae
Caecilia volcani
Dermophis mexicana