What is driving declines of montane endemic amphibians? New insights from Mount Bamboutos, Cameroon
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What is driving declines of montane endemic
amphibians? New insights from Mount Bamboutos,
Cameroon
A . M . T C H A S S E M F . , T . M . D O H E R T Y-B O N E , M . M . K A M E N I N .
W . P . T A P O N D J O U N . , J . L . T A M E S S E and L . N . G O N W O U O
Abstract Amphibians on African mountains are threatened Preserving a network of connected forest patches is there-
by habitat loss and fragmentation, pollution, disease and fore critical to save the endemic amphibians of Mount
climate change. In particular, there have been recent reports Bamboutos.
of declines of montane endemic frogs in Cameroon. Mount
Keywords Africa, amphibians, anurans, Cameroon, caeci-
Bamboutos, although home to numerous species of endemic
lians, endemic species, forest degradation, mountains
amphibians, has no official protection and its amphibian
populations have so far not been studied quantitatively. Supplementary material for this article is available at
We surveyed frog assemblages on this mountain along a https://doi.org/./S
gradient of forest modification over a -year period. Through
visual encounter surveys stratified across forest and farm-
land, we found that threatened montane amphibian species
Introduction
are closely associated with forested areas, particularly
the Critically Endangered Leptodactylodon axillaris and
Endangered Leptodactylodon perreti, Astylosternus ranoides
and Cardioglossa oreas. Using the updated inventory of
A mphibians are threatened globally, with over one-third
of all known species at risk of extinction and half show-
ing population declines (Stuart et al., ; IUCN, ).
amphibians, which includes species with broader ranges Threats include habitat alteration, loss and fragmenta-
across Africa, we found % of amphibian species on tion, pollution, overexploitation, disease, invasive species,
Mount Bamboutos to be threatened. We did not record climate change and combinations of these factors (Beebee
several species present in historical records, which suggests & Griffiths, ). Habitat loss, degradation and fragmen-
they may have disappeared from this mountain, includ- tation, such as through conversion to and intensification
ing Cardioglossa pulchra, Phrynobatrachus steindachneri, of agriculture (Stuart et al., ), can leave amphibians
Phrynobatrachus werneri, Sclerophrys villiersi, Werneria vulnerable to predation and desiccation and thus are im-
bambutensis and Wolterstorffina mirei. The pattern of portant drivers of amphibian declines (Cushman, ).
change detected in the amphibian community is consistent Conversion to agriculture is also often accompanied by use
with declines on other mountains in the country, with a of agrochemicals and other pollutants that have the potential
loss of Phrynobatrachus, Werneria and Cardioglossa spp., to negatively affect amphibians (Mann et al., ).
but persistence of Astylosternus, Arthroleptis and Leptodact- Responses of African amphibians to habitat change
y-lodon. The observed relationships of land-use patterns are poorly understood because of a paucity of studies
and amphibian diversity suggest that ongoing land-use across the continent, especially in forested areas (Lawson &
changes could extirpate the remaining montane endem- Klemens, ; Gardner et al., a; Brito, ). However,
ic frog species, particularly L. axillaris and L. perreti. some studies have been carried out across the continent,
showing that amphibian diversity and abundance differ
between primary forest, selectively logged forests and
A. M. TCHASSEM F.* (Corresponding author), M. M. KAMENI N.* and L. N.
GONWOUO* Laboratory of Zoology, Faculty of Sciences, University of Yaoundé
forestry plantations in Côte d’Ivoire, Madagascar and Ghana
I, P.O. Box 812, Yaoundé, Cameroon (Ernst et al., ; Hillers et al., ; Ofori-Boateng et al.,
E-mail arnaudtchassem@yahoo.fr ; Riemann et al., ), and between natural wooded
T. M. DOHERTY-BONE Conservation Research & Action for Amphibians of savannah and areas converted for agriculture in East
Cameroon, Royal Zoological Society of Scotland, Edinburgh, UK
Africa (Gardner et al., b). Some African amphibian
W. P. TAPONDJOU N.* Department of Ecology and Evolutionary Biology, species are threatened because their sole habitat is subject to
University of Kansas, Lawrence, USA
development, such as Nimbaphrynoides occidentalis, which
J. L. TAMESSE Department of Biological Science, Higher Teacher Training
College, Yaoundé, Cameroon
is under threat from mining activities (Sandberger-Loua
et al., ). The impact of agrochemicals and other pollu-
*Also at: Cameron Herpetology—Conservation Biology Foundation, Yaoundé,
Cameroon tants, another major threat besides habitat loss, has been
Received June . Revision requested August . rarely studied in Africa (Schiesari et al., ), with some
Accepted November . First published online December . exceptions in Nigeria (Akani et al., ).
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use,
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https://doi.org/10.1017/S0030605318001448
Oryx, 2021, 55(1), 23–33 © 2019 Fauna & Flora International doi:10.1017/S003060531800144824 A. M. Tchassem F. et al.
A significant number of African amphibians endemic and Oku (Gountié Dedzo et al., ). The climate of
to individual mountains or mountain ranges are threat- Mount Bamboutos is characterized by dry (November–
ened with extinction because of their small range sizes March) and wet (April–October) seasons. Mean annual
(Poynton et al., ; Largen & Spawls, ). For example, rainfall is , mm and mean temperature is . °C at an
% of Cameroonian amphibians categorized as Vulner- altitude of , m (Kengni et al., ). The natural vege-
able, Endangered or Critically Endangered on the IUCN tation is montane forest and grassland, much of which has
Red List are restricted to highland areas (IUCN, ). been replaced by crop fields, Eucalyptus plantations or pas-
Threats to Afromontane endemic amphibians have rarely ture. Human communities living on the mountain include
been quantified, although such studies are required urgently Fulani (sometimes referred to as Mbororo) and Mbouda
as these regions are undergoing both rapid development and peoples.
climate change (Beniston et al., ; Burgess et al., ). In
addition to the threats posed by habitat loss and pollution,
less understood factors such as pathogens are correlated Methods
with the recently reported declines of amphibians in
Cameroonian mountain ranges (Hirschfeld et al., ). Field surveys
Research into the status of and threats to African montane
amphibians is therefore urgently needed. To obtain an updated assessment of the amphibian species
The amphibian fauna of Cameroon is relatively well- composition, status and habitat requirements on Mount
studied (Perret, ; Amiet, ), and species have Bamboutos, we conducted field surveys every months dur-
been assessed as threatened with extinction (.%; IUCN, ing March –May , with a total of surveys across
). Many of these occur in the country’s highlands, and all seasons. Surveys were stratified between forest, grassland
the majority are montane endemics (Gartshore, ; Bergl and cultivated areas. We designated six discrete plots per
et al., ). Detailed inventories have been compiled and land-use type, with a minimum distance of m between
updated for several Cameroonian mountains in the past them, which we revisited during each survey period. We
decades (Amiet, , ; Herrmann et al., , ; chose sample sites at an altitude of ,–, m, to
Doherty-Bone & Gvoždík, ), but not for the more focus on land-use effects and minimize variation caused
severely deforested mountains in the Bamenda High- by altitude. Because the landscape on Mount Bamboutos
lands, particularly Mount Bamboutos. This mountain is fragmented, we could not locate plots of a homogenous
hosts several threatened amphibian species endemic to the land-use type that were large enough to allow for a m
Cameroon Volcanic Line, most notably the Critically buffer from the plot boundary to eliminate possible edge
Endangered egg frog Leptodactylodon axillaris. The species effects (sensu Gardner et al., a). We thus interpreted
is possibly endemic to this particular mountain (Amiet, survey data with caution, notably treating single occurrences
); although specimens suspected to be L. axillaris have of a species as potential vagrants (Barlow et al., ). At
been found on nearby Mount Oku, their identity has yet each survey we recorded number of surveyors, search
to be confirmed (Doherty-Bone & Gvoždík, ). Other time, elevation, species and number of individuals of each
rare species recorded from this mountain include the species observed.
Endangered Werneria bambutensis and Wolterstorffina We conducted day and night-time surveys in the desig-
mirei (Perret, ; Gartshore, ). Despite harbouring nated sample sites using visual and acoustic encounter
amphibian species of conservation concern, Mount Bam- surveys. This involved searching of microhabitats, such as
boutos is not officially protected (Bergl et al., ). The lifting rocks and logs, peeling bark from trees, moving
objectives of our study were to () update the amphibian in- fallen debris and inspecting tree stems during the day
ventory of this mountain, () assess the trend of remaining (.–.) and at night (.–.) along streams and
amphibian populations, and () identify habitat require- ponds, and in the surrounding vegetation (Crump & Scott,
ments of amphibian species to gain a better understand- ; Rödel & Ernst, ). Individual anurans were also
ing of the threats posed by deforestation and agricultural located by their vocalization. Anurans were captured by
encroachment. hand. Local farmers were invited to alert AMTF to any
amphibians they encountered, and some volunteered
amphibian specimens to the field researchers. These
Study area specimens were included in the final species inventory,
but not the habitat use analysis. Specimens were identified
Mount Bamboutos is situated in western Cameroon (Fig. ), to species level in the field and released immediately.
encompassing c. km, mostly at an altitude of . , m Voucher specimens were collected for later examination
(Bergl et al., ). The massif is the third tallest mountain when species identity was uncertain, or for studies of
of the Cameroon Volcanic Line after Mounts Cameroon systematic biology. Collection was restricted to no more
Oryx, 2021, 55(1), 23–33 © 2019 Fauna & Flora International doi:10.1017/S0030605318001448
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https://doi.org/10.1017/S0030605318001448Endemic amphibians of Mount Bamboutos 25
FIG. 1 (a) Topography of the Bamenda Highlands and (b) location of survey sites on Mount Bamboutos.
than five specimens per putative species, totalling speci- linear models, with R function glm, were used to evaluate
mens of species. Voucher specimens were euthanized the influence of habitat (forest, crop fields, pasture–
using an overdose of tricaine mesylate or chlorobutanol. grassland) on the relative abundance of species, notably
To understand habitat conversion and intensity of those observed on at least five separate occasions, to ensure
land use, we qualitatively monitored land management the model was informative. This method is more robust
during the survey, which included semi-structured inter- compared to more commonly used non-parametric tests
views with local farmers on their use of the landscape. We (such as Kruskal–Wallis tests). Generalized linear models
questioned a total of farmers, including from the accommodate the error distribution of the data, in this
Fulani community ( women, men) and Mbouda case count data (number of individuals), which typically fit
( women, men), on their creation of farms and their a Poisson distribution (O’Hara & Kotze, ). We incorpo-
use of forest products and agrochemicals (see Supplementary rated parameters such as season, year and elevation in the
Material for full questionnaire). generalized linear models to assess the influence of potential
confounding factors on the response variable (abundance of
frogs). We then applied an information criterion analysis
Data analysis to the models and used the resulting Akaike’s information
criterion (AIC) to assess the best-performing model based
We compared the data collected during our study to previ- on incorporation of the potentially competing explanatory
ous surveys (Perret, ; Amiet, , ; Gartshore, factors (Mazerolle, ).
; Hirschfeld et al., ), cross-checked the final species
inventory against the IUCN Red List of Threatened Species,
and calculated the proportion of threatened species Results
following Böhm et al. (). To assess the value of different
habitats for amphibian community composition (beta Amphibian diversity and conservation assessment
diversity), we performed a PERMANOVA analysis, using
function adonis in the R .. package vegan (R Core We found a total of individuals of amphibian species
Team, ), testing the significance of the Bray–Curtis during the – survey period (Table ). Ten speci-
dissimilarity based on permutations (Anderson, ; mens were volunteered by farmers: one caecilian Herpele
Riemann et al., ). Square root transformed amphibian squalostoma, one Astylosternus ranoides, two A. rheophilus
species abundance data were subjected to ordination and six Leptopelis nordequatorialis, originating from farms
analysis using non-metric dimensional scaling plots of adjacent to forest patches. The total species inventory of
Bray–Curtis dissimilarities, with function metaMDS in Mount Bamboutos based on our surveys and published
vegan, to view similarities in amphibian community struc- information comprises species (Table ), although we
ture between land-use types. We used function simper in found only species in our – surveys. We did not
vegan to identify the species contributing most to the dif- record Cardioglossa pulchra, Phrynobatrachus steindachneri,
ferences between land-use types (Clarke, ). Generalized Phrynobatrachus werneri, Sclerophrys villiersi, Werneria
Oryx, 2021, 55(1), 23–33 © 2019 Fauna & Flora International doi:10.1017/S0030605318001448
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https://doi.org/10.1017/S003060531800144826 A. M. Tchassem F. et al.
TABLE 1 An updated amphibian species inventory for Mount Bamboutos.
IUCN Red
Species List category1 Endemicity2 Sources
Arthroleptis cf. perreti EN BamH This study
Astylosternus ranoides EN BamH Amiet (1977); this study
Astylosternus rheophilus VU CNH Amiet (1977); Hirschfeld et al. (2016); this study
Cardioglossa oreas EN BamH Amiet (1972); this study
Cardioglossa pulchra EN CNH Hirschfeld et al. (2016)
Leptodactylodon axillaris CR BamH Amiet (1980); Cruz et al. (2013);
Hirschfeld et al. (2016); this study
Leptodactylodon perreti EN BamH Amiet (1980); this study
Leptopelis nordequatorialis LC CNH This study
Sclerophrys maculata LC PanAfr Hirschfeld et al. (2016); this study
Sclerophrys villiersi EN CH Hirschfeld et al. (2016)
Werneria bambutensis EN CH Amiet (1972); Hirschfeld et al. (2016)
Wolterstorffina mirei EN BamH Perret (1972); Hirschfeld et al. (2016)
Phrynobatrachus steindachneri VU CNH Mertens (1968); Hirschfeld et al. (2016)
Phrynobatrachus werneri LC CNH Gartshore (1986)
Ptychadena cf. mascariensis ‘D’ LC PanAfr This study
Herpele squalostoma LC CongB This study
LC, Least Concern; VU, Vulnerable; EN, Endangered; CR, Critically Endangered.
PanAfr, species with pan-African ranges; CongB, species with ranges restricted to Congo Basin forest; CNH, species restricted to highlands of Cameroon
and Nigeria; CH, species restricted to the highlands of Cameroon; BamH, species restricted to the Bamenda Highlands of Cameroon (includes Mounts
Bamboutos, Oku, Lefo and Mbam).
bambutensis and Wolterstorffina mirei. These are mon- particular stream in a now deforested area, where L. axillaris
tane endemic species, and were last observed on Mount had been recorded in , failed to detect this species (Cruz
Bamboutos in (Hirschfeld et al., ), except for et al., ). We observed the Endangered A. ranoides on
P. werneri (last observed in ; Gartshore, ) and only four separate occasions and found that it was margin-
S. villiersi (last observed in ; Hirschfeld et al., ). ally more abundant in forest than cultivated land, with fewer
All but one of the species not located are categorized observations in pasture. Where the species was recorded in
as threatened (one Vulnerable, four Endangered) on the pasture areas, it occurred always within m of the nearest
IUCN Red List, and % of the species in the complete forest edge. The Vulnerable A. rheophilus and Endangered
inventory are categorized as threatened. In addition to Cardioglossa oreas were exclusively found in forest.
the caecilian H. squalostoma, we found three species not Amphibian community structure varied significantly
previously recorded on the mountain: L. nordequatorialis, across land-use types (PERMANOVA: P = .), with non-
Ptychadena cf. mascariensis ‘D’ and a frog corresponding metric dimensional scaling of community dissimilarity
to Arthroleptis perreti, similar to specimens observed on showing little overlap of amphibian communities between
Mount Oku. However, the species accumulation curve the three habitat types (Fig. ). Analysis with simper showed
over time does not show a plateau, indicating the species that species contributing most to dissimilarities between
inventory may be incomplete (Fig. ). forest and cultivated land were L. perreti and L. nordequa-
torialis, whereas between pasture and forest these were
L. perreti, S. maculata and A. ranoides (Table ). Between
Field surveys pasture and cultivated land, L. nordequatorialis, P. cf.
mascariensis ‘D’ and A. ranoides contributed most to the
Based on surveyor hours divided equally amongst land- dissimilarity.
use types, the majority of amphibians were found in forests For those species with sufficient records for generalized
( individuals) followed by agricultural areas ( indivi- linear modelling (i.e. observed on at least five occasions),
duals) and pasture (three individuals). Most species (eight) habitat had a significant influence on their occurrence
were found in forest, four species in cultivated areas and (L. perreti, A. rheophilus, L. nordequatorialis and P. cf.
three in pasture (Table ). The Endangered L. perreti and mascareniensis ‘D’; Table ). Season and elevation also
Critically Endangered L. axillaris were found exclusively significantly influenced the model for L. perreti and L.
in forest habitats. Leptodactylodon axillaris was found in nordequatorialis. Habitat, season and elevation combined
only one particular forest patch at , m altitude, sharing provided the model with the best fit (i.e. the lowest AIC)
breeding sites in small streams with L. perreti. Surveys of one for L. perreti, with ΔAIC = compared to a model that
Oryx, 2021, 55(1), 23–33 © 2019 Fauna & Flora International doi:10.1017/S0030605318001448
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https://doi.org/10.1017/S0030605318001448Endemic amphibians of Mount Bamboutos 27
FIG. 2 Species accumulation curve for amphibians on Mount FIG. 3 Non-metric dimensional scaling plot of amphibian
Bamboutos based on historical and contemporary records. community structure divided by land-use type on Mount
Bamboutos, based on visual encounter surveys with equal search
effort per land-use type (Stress = .; PERMANOVA:
TABLE 2 Summary of amphibian species (total per habitat type P = .). Ellipses show groupings of sites based on class
across all survey techniques) encountered during this study standard deviations of species assemblages constrained by
(–). land use.
Cultivated
Species land Pasture Forest
eucalyptus) farming. All Mbouda farmers surveyed now
A. cf. perreti 0 1 0
practise agriculture primarily as a commercial activity,
A. ranoides 2 2 4
A. rheophilus 0 0 18 whereas Fulani are subsistence farmers. Informants (Fulani
C. oreas 0 0 3 and Mbouda; n = ) claimed that the economic importance
H. squalostoma 0 0 1 of small-scale forest use had diminished by % over the
L. axillaris 0 0 4 past decade. Their forest use included the extraction of
L. perreti 0 0 163 both timber and non-timber forest products (e.g. bamboo
L. nordequatorialis 45 0 3 for house construction), and was declining relative to food
P. mascareniensis 16 0 1
crop production. Interviewees perceived that encroachment
S. maculata 1 1 0
Total 65 4 197
of cultivation had been exacerbated by new families settling
No. of species1 4 3 8 on Mount Bamboutos over the previous decade. This land-
Mean no. of specimens 0.50 0.37 1.00 use change was accompanied by increased use of agrochem-
per sampling event1 icals, which we observed across cultivated areas following
the planting of seeds. Chemicals used were predominately
Data from visual encounter surveys (equal survey effort per habitat) only.
pesticides against weeds and potato blight (see Table for
a list of chemicals); we did not observe use of fertilizers.
included only habitat. For the other three species the best- Pesticides were frequently prepared within or next to
performing model included only habitat. Year of survey had streams, without protective equipment, and chemicals often
little influence on the significance or fit of the models, spilt from the containers. The majority of interviewed
suggesting stability over the -year survey period. farmers (%) had not received a basic education and are
thus unlikely to understand product labels on packaging
relating to recommended dosages and safety measures.
Human use of the landscape Most local people interviewed (%) expressed favourable
attitudes towards conservation, but stated financial support
We frequently observed creation of new crop farms was necessary to enable them to abstain from clearing nat-
throughout –, up to an altitude of , m and pre- ural habitats. We observed diversion of water from streams
ceded by the clearance of forest. We also noted a shift from in the forest at eight sites, mostly at ,–, m altitude.
subsistence-oriented (bananas, raffia palms, fruit trees, yams) The water is used to irrigate fields and is extracted with
to cash-crop oriented (carrots, onions, potatoes, maize, beans, suction pipes, with a particularly high number of pipes
Oryx, 2021, 55(1), 23–33 © 2019 Fauna & Flora International doi:10.1017/S0030605318001448
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https://doi.org/10.1017/S003060531800144828 A. M. Tchassem F. et al.
TABLE 3 Results of the similarity percentage analysis (using simper), showing the importance of dissimilarity for different amphibian
species by habitat type based on visual encounter surveys on Mount Bamboutos.
Proportional Cumulative
contribution proportional
Taxon Mean ± SD individuals per survey to dissimilarity contribution
Forest vs cultivated land Forest Cultivated land
L. perreti 2.26 ± 1.81 0 ±0 0.44 0.44
L. nordequatorialis 0 ±0 0.60 ± 1.19 0.29 0.73
P. cf. mascariensis ‘D’ 0.01 ± 0.12 0.22 ± 0.68 0.13 0.86
A. rheophilus 0.22 ± 0.61 0 ±0 0.07 0.93
A. ranoides 0.06 ± 0.33 0.03 ± 0.24 0.03 0.96
Forest vs pasture Forest Pasture
L. perreti 2.26 ± 1.81 0 ±0 0.49 0.50
A. ranoides 0.06 ± 0.33 0.03 ± 0.24 0.16 0.66
S. maculata 0 ±0 0.01 ± 0.12 0.10 0.77
A. cf. perreti 0 ±0 0.01 ± 0.12 0.10 0.88
A. rheophilus 0.22 ± 0.61 0 ±0 0.08 0.95
Pasture vs cultivated land Pasture Cultivated land
L. nordequatorialis 0 ±0 0.60 ± 1.19 0.37 0.38
A. ranoides 0.03 ± 0.24 0.03 ± 0.24 0.18 0.57
P. cf. mascariensis ‘D’ 0 ±0 0.22 ± 0.68 0.17 0.74
S. maculata 0.01 ± 0.12 0.01 ± 0.12 0.12 0.87
A. cf. perreti 0.01 ± 0.12 0 ±0 0.12 1.00
used during the dry season (mean of pipes per stream). Mount Oku ( species; Doherty-Bone & Gvoždik, ),
Only the Fulani community graze livestock in the area, despite Bamboutos being larger ( km) than Oku
and livestock herders set bushfires in pasture areas during ( km; Bergl et al., ). It is possible that during the
January–March. The practice aims to promote regrowth of historical agricultural encroachment into the forest and
new grass at the onset of the wet season. Interviewees from grasslands of Mount Bamboutos, many species were ex-
the Fulani community, which is dominated by livestock tirpated prior to the arrival of amphibian biologists. In
owners, were reluctant to answer questions on the use of addition, the degraded sites are at high altitudes, making
fire because the practice is illegal (Décret No //PM it unlikely that colonization by low- and mid-elevation
DU Août, ). species could compensate for the loss of montane and
forest-adapted species. More sampling is needed at lower
Discussion altitudes on Mount Bamboutos to include mid- and low-
elevation species in the inventory and provide a more accu-
We reappraised the amphibian diversity of Mount Bam- rate calculation of the proportion of threatened species.
boutos through both examining the published literature As observed on Mount Oku in the North-West Region and
and undertaking a multi-season survey over years. We Mount Manengouba in the South-West and Littoral Regions
found additional species not previously recorded on the during – (Hirschfeld et al., ; Doherty-Bone &
mountain, but also noted a decline in several montane Gvoždik, ), we did not locate P. steindachneri (which has
endemic amphibian species, consistent with reports from since been found to consist of a species complex that in-
other mountains in the highlands of Cameroon (Hirschfeld cludes P. jimzimkusi; Zimkus & Gvoždik, ) in our surveys.
et al., ). An assessment of habitat requirements suggests Prior to its reported decline on these other mountains, this
that the remnant forest of Mount Bamboutos is a key habitat species was abundant. Phrynobatrachus werneri is another
for the remaining species of conservation concern, although species of the same genus that had previously been recorded
it is substantially reduced in size and of degraded quality. on Mount Bamboutos, but has not been observed there in
Rapid encroachment of cultivated areas is accompanied by recent surveys. Doherty-Bone & Gvoždik () have pro-
water abstraction, use of agrochemicals, livestock grazing posed that the conservation status of these Phrynobatrachus
and fire, factors that exacerbate long-term degradation of species should be reassessed and moved to a higher extinc-
remnant amphibian habitat. tion risk category. Although we observed C. oreas, we did
The total amphibian species inventory of Mount Bam- not observe C. pulchra or the mountain toads W. bambutensis
boutos is low ( species) in comparison to neighbouring and W. mirei. The causes of this are unclear, but these species
Oryx, 2021, 55(1), 23–33 © 2019 Fauna & Flora International doi:10.1017/S0030605318001448
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https://doi.org/10.1017/S0030605318001448Endemic amphibians of Mount Bamboutos 29
TABLE 4 Generalized linear models comparing parameters influencing abundance of amphibian species on Mount Bamboutos, showing
degrees of freedom (df), deviance residual, P-value, Akaike information criterion (AIC) and difference of AIC from the best-performing
model.
Model parameters df Deviance residual P-value AIC ΔAIC
Leptodactylodon perreti
Habitat × Elevation × Season × Year 87 109.47 0.99 299 9
Habitat × Elevation × Season 95 117.14 0.99 290 0
Habitat × Elevation 99 129.77 1.00 295 5
Habitat × Season 100 130.18 0.99 293 3
Season × Elevation 101 222.03 0.02 383 93
Habitat × Year 100 133.78 0.99 297 7
Habitat 102 133.88 , 0.001 293 3
Elevation 103 229.59 , 0.001 387 97
Season 103 252.23 0.03 409 119
Year 103 256.22 0.42 413 123
Astylosternus rheophilus
Habitat × Elevation × Season × Year 87 55.34 0.99 115 21
Habitat × Elevation × Season 95 61.22 0.99 105 11
Habitat × Elevation 99 64.09 1.00 100 6
Habitat × Season 100 61.43 0.99 96 2
Season × Elevation 101 71.95 0.54 104 10
Habitat 102 64.01 , 0.01 94 0
Elevation 103 75.16 0.32 103 9
Season 103 73.74 0.12 102 8
Year 103 76.16 0.95 104 10
Leptopelis nordequatorialis
Habitat × Elevation × Season × Year 87 38.95 0.99 123 16
Habitat × Elevation × Season 95 45.62 0.99 114 7
Habitat × Elevation 99 51.19 1.00 111 4
Habitat × Season 100 48.59 0.99 107 0
Season × Elevation 101 138.70 0.54 195 88
Habitat 102 52.95 , 0.001 107 0
Elevation 103 144.24 , 0.001 196 87
Season 103 151.63 , 0.01 204 97
Year 103 160.54 0.70 212 105
Ptychadena cf. mascariensis ‘D’
Habitat × Elevation × Season × Year 87 31.04 0.99 91
Habitat × Elevation × Season 95 35.43 0.99 80 1
Habitat × Elevation 99 45.54 0.98 82 3
Habitat × Season 100 46.81 0.18 81 2
Season × Elevation 101 72.61 , 0.01 105 26
Habitat 102 49.12 , 0.001 79 0
Elevation 103 82.33 0.87 111 32
Season 103 80.77 0.20 109 29
Year 103 82.04 0.57 110 30
have also declined on Mounts Oku and Manengouba decline it would be through an endemic emergence induced
(Hirschfeld et al., ; Doherty-Bone & Gvoždik, ). by changes in environmental conditions (Hirschfeld et al.,
The decline of anurans on Oku and Manengouba coincided ). The role of climate change in this emergence is unclear,
with an increased prevalence of amphibian chytrid fungus although evidence from Cameroonian mountains suggests
Batrachochytrium dendrobatidis (Hirschfeld et al., ). upslope displacement of mountain frogs and population
This pathogen was also found on one specimen of declines following climatic extremes (Doherty-Bone, ).
Astylosternus sp. in , after retrospective sampling of The observation of the caecilian H. squalostoma, a species
museum specimens collected during – on Mount known from low to mid elevations (, m; Herrmann et al.,
Bamboutos (Hirschfeld et al., ). Batrachochytrium ), provides the highest elevational record to date for this
dendrobatidis was first recorded in eastern and southern species, at , m. The species occurs in both forested and
Cameroon in , which indicates that if it caused the disturbed areas, including intensively cultivated and urban
Oryx, 2021, 55(1), 23–33 © 2019 Fauna & Flora International doi:10.1017/S0030605318001448
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https://doi.org/10.1017/S003060531800144830 A. M. Tchassem F. et al.
TABLE 5 Agrochemicals commonly used by farmers on Mount Bamboutos.
Chemicals Target crop Target pest & usage
Fungicides
Penncozeb 80 WP or Cleanzup Blue 80 WP Seed potatoes Disease control; applied every 10 days throughout the crop season
by ground boom
Tomatoes Anthracnose fungus
Onions Onions leaf blight (leaf spot)
Celery Regular applications at 3–5 day intervals in plant beds from first
emergence of plants until plants are planted out in field
Carrots Control of various diseases
Herbicides
Agil 100 EC Carrots Broad-spectrum control of annual & perennial grass weeds
Cleanfarm 360 SL Carrots, Control of weeds & insects pests
potatoes
Insecticides & nematicides
Furadent Super 10 G, Vydate 10 G, Bastion Super Celery, Insect eggs & larvae
& Rugby 10 G carrots,
potatoes,
onions
locations (Kouete et al., ; T.M. Doherty-Bone & L.N. where specialized species with small ranges are replaced by
Gonwouo, unpubl. data). Cameroonian caecilians at high generalized species with broad ranges (Ernst et al., ;
elevations typically belong to the genus Crotaphatrema Ofori-Boateng et al., ).
(Doherty-Bone et al., ). The individual found during We found few amphibians in pasture, and the ab-
our survey is not a misidentified Crotaphatrema sp. (the sence of montane endemic species such as Astylosternus,
number of annuli suggests it is H. squalostoma; Wilkinson Cardioglossa and Leptodactylodon sp. was particularly
et al., ). It is possible that H. squalostoma is either noticeable in these areas. The forests on Bamboutos have
tolerant of the climate at higher elevations, or that the been reduced to isolated patches separated by cultivated
climate on Mount Bamboutos is changing and thus now grassland (pasture), crop fields or plantations. Habitat frag-
accommodates species adapted to lowland conditions. mentation can isolate subpopulations (Cushman, ) and
This is the first quantitative study of the value of vari- diminish genetic diversity. Given that threatened, forest-
ous land-use types for amphibians in the highlands of dependent species have not been found to utilize this habi-
Cameroon. We found that several montane endemic frog tat, grassland potentially acts as a barrier to dispersal.
species appear to be sensitive to forest loss, especially when Pasture could even be an ecological sink because frogs enter-
forest is converted for intensive agricultural production. This ing grassland in an attempt to reach other forest patches risk
included species that were hypothesized to be relatively desiccation and predation (e.g. Rothermel, ). This may
resilient to forest loss, such as A. rheophilus (Doherty-Bone partly explain the limited number of observations of the
& Gvoždik, ). Absence of this species in agricultural Critically Endangered L. axillaris, which was found in
areas could therefore be caused by aspects of land management only one forest patch. Protection of this patch is urgent:
such as use of agrochemicals and fire, and replacement of although farmers had previously avoided cutting this par-
natural vegetation by crop monocultures. We also observed ticular patch, in October clearance had begun.
that species adapted to high montane grasslands, notably Cultivation on Bamboutos is causing visible soil erosion,
L. nordequatorialis (Gartshore, ; endemic to highlands probably resulting in run-off of nutrients, sediments and
of Cameroon and Nigeria), can survive in agricultural agrochemicals into lower streams where tadpoles of many
areas: we found more individuals of L. nordequatorialis in frog species develop. Pesticides can be lethal to amphibians
cultivated areas than in grasslands on Mount Bamboutos. (Mann et al., ; Stechert et al., ) and we frequently
However, the species’ vulnerability to conversion of observed them being applied on Mount Bamboutos.
montane grassland to cultivation should be more thoroughly Because agrochemicals were used so widely, it was not
assessed, particularly its ability to tolerate agrochemicals. possible to stratify the survey to understand their impacts.
Other species found in cultivated areas were those that are Potential future studies could include experimental chal-
distributed widely across Africa, such as the toad S. maculata lenges of frogs and their larvae to realistic concentra-
and grass frog P. cf. mascariensis ‘D’. This phenomenon is tions of different agrochemicals (e.g. Stechert et al., ),
typical for forest disturbance, particularly in the tropics, although care would need to be taken to choose relevant
Oryx, 2021, 55(1), 23–33 © 2019 Fauna & Flora International doi:10.1017/S0030605318001448
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https://doi.org/10.1017/S0030605318001448Endemic amphibians of Mount Bamboutos 31
study species that are not already threatened. An alternative with assistance from TMD-B, LNG; project supervision: JLT. All
way to study this would be to locate sites where agrochem- authors reviewed and approved the final manuscript.
icals are applied in a gradient of concentrations. Similarly, it
Conflict of interest None.
is unclear how amphibians are affected by water abstraction
for irrigation. This practice should be investigated further, Ethical standards This research abided by the Oryx guidelines
given its likely effect on the depth, temperature and perma- on ethical standards and the ethical guidelines of the British Herpeto-
nency of streams harbouring developing larvae. logical Society (2017). Collecting amphibians during fieldwork was
permitted by the Cameroon Ministry of Scientific Research and
Livestock grazing is prominent on Mount Bamboutos,
Innovation (13/MINRESI/B00/C00/C10/C10) and the Ministry of
and grassland is burned widely by livestock herders. This Forestry and Wildlife (629PRS/MINFOF/SG/DFAP/SDVEF/SC).
probably has a detrimental effect on montane endemic
amphibians. Apart from indirect impacts of degradation of
forest, water and prey, fire can kill less mobile amphibians
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