ArticlePDF Available

Rediscovery of the Liberian Nimba toad, Nimbaphrynoides liberiensis (Xavier, 1978) (Amphibia: Anura: Bufonidae), and reassessment of its taxonomic status

Authors:

Abstract

We report on the search and rediscovery of the Liberian Nimba toad, Nimbaphrynoides liberiensis, 30 years after its original description. A small surviving population could be traced in the surroundings of the type locality Mount Alpha, Liberia. The type locality was meanwhile destroyed by open cast mining. Similar to the Guinean Nimba toad, Nimbaphrynoides occidentalis, the Liberian toad lives exclusively in open, savanna like habitats above 1200 m a.s.l. The presumably few surviving individuals and the small and patchy distribution classify the Liberian toads as Critically Endangered (Stuart et al. 2008). A morphological, acoustical and genetic comparison of Liberian and Guinean populations revealed only minor, but distinct morphological (size, colour) differences. Genetically and acoustically the two taxa were indistinguishable. We therefore propose to consider the two populations as conspecific and to consider Nimbaphrynoides liberiensis (Xavier, 1978) as junior synonym of Nimbaphrynoides occidentalis (Angel, 1943). Because of the morphological differences we propose to treat the Liberian population as a subspecies of the Guinean toad and herein introduce the new name: Nimbaphrynoides occidentalis liberiensis.
56 Accepted by M. Vences: 24 Dec. 2009; published: 10 Feb. 2010
ZOOTAXA
ISSN 1175-5326 (print edition)
ISSN 1175-5334 (online edition)
Copyright © 2010 · Magnolia Press
Zootaxa 2355: 5668 (2010)
www.mapress.com/zootaxa/Article
Rediscovery of the Liberian Nimba toad, Nimbaphrynoides liberiensis (Xavier,
1978) (Amphibia: Anura: Bufonidae), and reassessment of its taxonomic status
LAURA SANDBERGER1, ANNIKA HILLERS1, JOSEPH DOUMBIA2, NÉMA-SOUA LOUA3,
CHRISTIAN BREDE4 & MARK-OLIVER RÖDEL1,5
1Museum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin,
Herpetology, Invalidenstr. 43, 10115 Berlin, Germany. E-mails: laura.sandberger@mfn-berlin.de; annika.hillers@mfn-berlin.de;
mo.roedel@mfn-berlin.de
2Centre d'Étude et de Recherche en Environnement (CÉRE), Université de Conakry, BP 3817, Conakry, Guinée.
E-mail: joevero76@yahoo.fr
3Société des Mines de Fer de Guinée, Cité Chemin de Fer, Immeuble Faranah, BP 2046, Kaloum, Conakry, Republic of Guinea.
E-mail: nsloua@yahoo.fr
4Medizinische Klinik und Poliklinik II, Zentrum für Experimentelle Molekulare Medizin, Zinklesweg 10, 97078 Würzburg, Germany.
E-mail: brede_c@medizin.uni-wuerzburg.de
5Corresponding author. E-mail: mo.roedel@mfn-berlin.de
Abstract
We report on the search and rediscovery of the Liberian Nimba toad, Nimbaphrynoides liberiensis, 30 years after its
original description. A small surviving population could be traced in the surroundings of the type locality Mount Alpha,
Liberia. The type locality was meanwhile destroyed by open cast mining. Similar to the Guinean Nimba toad,
Nimbaphrynoides occidentalis, the Liberian toad lives exclusively in open, savanna like habitats above 1200 m a.s.l. The
presumably few surviving individuals and the small and patchy distribution classify the Liberian toads as Critically
Endangered (Stuart et al. 2008). A morphological, acoustical and genetic comparison of Liberian and Guinean
populations revealed only minor, but distinct morphological (size, colour) differences. Genetically and acoustically the
two taxa were indistinguishable. We therefore propose to consider the two populations as conspecific and to consider
Nimbaphrynoides liberiensis (Xavier, 1978) as junior synonym of Nimbaphrynoides occidentalis (Angel, 1943). Because
of the morphological differences we propose to treat the Liberian population as a subspecies of the Guinean toad and
herein introduce the new name: Nimbaphrynoides occidentalis liberiensis.
Key words: Conservation status, Guinea, Liberia, mining, montane grassland, Nimbaphrynoides occidentalis,
Nimbaphrynoides occidentalis liberiensis, taxonomy
Introduction
In 1943 F. Angel described a new toad species from Mount Nimba as Nectophrynoides occidentalis. He first
believed that this toad was ovo-viviparous, but soon new data on the spectacular, truly viviparous
reproductive biology of this unique toad became known (e.g. Angel & Lamotte 1944, 1948; current
knowledge summarized by Xavier 1986). This toad was exclusively recorded from a few km² of montane
grasslands on the Guinean part of Mount Nimba (Lamotte 1959; Lamotte & Sanchez-Lamotte 1999; Hillers et
al. 2008; very recently we detected one site on the Ivorian part of the mountain, L. Sandberger et al. unpubl.
data). The Nimba mountain range includes parts being positioned in nowadays Guinea, Ivory Coast and
Liberia (Lamotte 1998; Lamotte & Roy 2003). Due to rich deposits of iron ore the mountains were in the
focus of mining prospecting activities since the 1950s (Lamotte 1983).
In the course of iron ore prospecting in the Liberian part of the Nimba range M. Coe detected Nimba toads
on Liberia’s highest mountain, the Mount Alpha in 1964. These toads were subsequently described by F.
Xavier as a new likewise viviparous species, Nectophrynoides liberiensis (Xavier 1978; Fig. 1). This
Zootaxa 2355 © 2010 Magnolia Press · 57
LIBERIAN NIMBA TOAD, NIMBAPHRYNOIDES LIBERIENSIS
description was mainly based on morphological differences to N. occidentalis, i.e. N. liberiensis females may
be as large as 35 mm, N. occidentalis females rarely surpass 24 mm (however: N. occidentalis holotype: 27.5
mm). Additional arguments for the species description were small colour differences (i.e. the presence of
brown dots on the belly of most of the Liberian toads) and hybridization experiments (Xavier 1978).
More recently, both Nimba toads were placed in an own genus, Nimbaphrynoides by Dubois (1987) and
classified as being Critically Endangered (Stuart et al. 2008). However, newer data on the two toads are rare
(N. occidentalis: Lamotte & Sanchez-Lamotte 1999; Hillers et al. 2008) or completely missing (N.
liberiensis). The type locality of N. liberiensis meanwhile was explored for iron ore (1960 to early 1990) and
what formerly was Mount Alpha, now is an open cast mining pit (Fig. 2). We aimed to verify if the Liberia
Nimba toad still exists and if so, to reassess its taxonomic status.
Material and methods
In order to search for Liberian Nimba toads we visited the area of the former Mount Alpha and its
surroundings near Yekepa three times in 2007 (28 June, 22 July, 23–25 August) and once in 2008 (25–27
May). We investigated heavily impacted areas (e.g. old mining pit), less impacted areas (further away from
the main mining site and old mining roads), open as well as forested areas, by carefully checking the
vegetation and potential hiding places, between app. 900 m a.s.l up to the remaining mountain tops (1375 m
a.s.l.). Searches were undertaken between 9:30 am and 4:30 pm. We employed visual encounter searches
along transects (e.g. Rödel & Ernst 2004; N = 15) and standardized plot searches (N = 4) as described by
Hillers et al. (2008). We thus investigated all potential and accessible habitats of the Liberian Nimba toad in
this region. Geographic positions of study sites were recorded with a GPS receiver (Garmin 72). In total we
searched for app. 63 man-hours. All investigated localities are shown in Fig. 3 and summarized in the
appendix.
Toe-tips were taken for genetic comparisons and stored in 96% ethanol. Additionally, we collected a few
vouchers. These were anesthetised in a chlorobutanole solution and subsequently preserved in 75% ethanol.
Tissue samples and vouchers are kept in the herpetological collection of the Museum für Naturkunde, Berlin
(N. liberiensis: ZMB 73871-73877; five females, one male, one juvenile). The type series of N. liberiensis
was investigated in the collection of the Muséum National d’Histoire Naturelle, Paris (holotype: MNHN
1978.3088; paratypes: 1978.3089–3103; 1978.3111–3114; 1978.3116–3126; 16 females, 14 males; juveniles
of the type series not investigated). These toads were compared to the N. occidentalis type series (holotype:
MNHN 1944.149; para- and paratopotypes: 1944.151–152, 1944.154–159; nine females; three juveniles not
investigated), N. occidentalis specimens stored in Berlin (ZMB 70660, 73878-73890; 12 females; six males)
and to snout-vent length (SVL) measures taken in 2007 and 2008 in the field (N. occidentalis: N = 603,
females: 469, males: 134; N. liberiensis N = 68, females: 44, males: 24). For the morphological comparison
we measured SVL, head width (HW), femur length (FL), tibia length (TB) and food length incl. longest toe
(FoL). With the exception of SVL, measures have been taken from museum vouchers only. All measures were
taken with a dial calliper (± 0.1 mm) and are given in millimetres. For statistical comparison we carried out t-
tests (all data showed a normal distribution and homogeneity in variance). All calculations were carried out
with the freeware software package R.
In 2007 we succeeded in recording advertisement calls of one N. liberiensis male. In 2008 we recorded the
calls of 11 N. occidentalis males. Calls were recorded with a R-09 24bit WAVE/ MP3 recorder (ERIDOL by
Roland, sample rate: 44.1 kHz, record mode: wav_24bit) and a microphone (ECM-950). These calls were
analysed with the programme Avisoft SAS Lab Pro 4.5 (R. Specht, Berlin, Germany).
DNA was extracted using High Pure PCR Template Preparation kits (Roche) following manufacturer’s
instructions. We used primers 12SA and 12SB to amplify part of the 12S gene and 16SA and 16SB for the
partial 16S rRNa gene; all primers are from Palumbi (1991). The cytochrome b (cyt b) gene was amplified
with the primers CBJ10933 and Cytb-C from Bossuyt & Milinkovitch (2000). Standard PCR protocols were
used and PCR products were purified using High Pure PCR Product Purification kits (Roche). Purified
SANDBERGER ET AL.58 · Zootaxa 2355 © 2010 Magnolia Press
templates were directly sequenced using an automated sequencer (ABI 3100). In total, we sequenced 16 tissue
samples (nine N. liberiensis, seven N. occidentalis) for 12S (390bp), 12 (five N. liberiensis, seven N.
occidentalis) for 16S (552 bp) and 10 specimens (four N. liberiensis, six N. occidentalis) for cyt b (608 bp; see
Table 3). Sequences were validated using SEQUENCE NAVIGATOR (Applied Biosystems). We aligned
them using the Clustal W option in MEGA 4.1 (Tamura et al. 2007). The alignment was subsequently checked
by eye and refined if necessary. Uncorrected pair-wise sequence divergence was calculated using PAUP*
4beta10 (Swofford 2002).
FIGURE 1. Dorsal and ventral view of (left) the holotype of Nimbaphrynoides liberiensis (MNHN 1978.3088; SVL
29.2 mm) and (right) the holotype of Nimbaphrynoides occidentalis (MNHN 1944.149; SVL 27.5 mm).
Results
We rediscovered the Liberian Nimba toad, both north and south of the old LAMCO (Liberian-American-
Swedish Minerals Company) mining pit. In total we detected 30 toads (14 adults: five females, six males,
three subadults, 16 juveniles) in 2007. In 2008 we encountered a total of 22 toads, 17 females (16 being
pregnant), and five males.
Zootaxa 2355 © 2010 Magnolia Press · 59
LIBERIAN NIMBA TOAD, NIMBAPHRYNOIDES LIBERIENSIS
Most individuals were found south of former Mount Alpha and each year only one female was found
north of it. At several localities we could not find any toads (Fig. 3). We observed toads only within the less
impacted parts, where mining was abandoned after 10 years. They were absent from strongly impacted
localities, i.e. where mining took place for more than 30 years. All places with toads had soil that was not or
little compacted, i.e. holes and cracks were visible. At sites without such structures no toads could be traced.
All toads were recorded in open areas at 1200 m a.s.l. and above.
FIGURE 2. Type locality of Nimbaphrynoides liberiensis (the meanwhile destroyed Mount Alpha, above) and a
degraded habitat south of the mining pit, currently used by the Liberian Nimba toad.
SANDBERGER ET AL.60 · Zootaxa 2355 © 2010 Magnolia Press
FIGURE 3. Sites investigated for Nimba toads and current distribution of Nimbaphrynoides liberiensis. Black dots
(plots) and triangles (transects) indicate where we encountered Liberian Nimba toads. At white dots (plots) and triangles
(transects) we failed to record them. The black box and the arrow indicate the water filled mining pit of the LAMCO
mine, the former Mount Alpha (compare Fig. 2). Note erosion left and right of the mining pit. The area indicated by the
dotted line was less intensively minded (10 years only) than Mount Alpha (1960 to early 1990). The grey line north of
the mining pit indicates a further area investigated (nine man-hours) for Nimba toads without success (map adopted from
Spot_Image Jannuary 2005).
For the SVL comparison we used museum vouchers and measurements taken in the field. Females were
significantly larger than males in both taxa (N. occidentalis females: mean length 20.5 mm, N = 490; males:
18.0 mm, N = 149, p< 0.05; N. liberiensis females: 28.7 mm, N = 65; males: 22.4 mm, N = 39, p< 0.001; Fig.
4). N. liberiensis were significantly larger than N. occidentalis (males: p< 0.001; females: p< 0.001),
respectively. Even after being corrected for size (FoL/SVL) N. liberiensis females (N = 19) and males (N =
13) had significantly longer feet than N. occidentalis (females N = 12, males N = 6; p< 0.05). Other
morphological parameters did not differ between taxa (Table 1). To account for the possibility of geographic
clinal variation we correlated all SVL field measures from 2007 and 2008 (Nfemales = 483, Nmales = 143) with
latitude. Analyses were done with respect to sex, but irrespective of the taxa. We found no geographic
correlation.
The colouration of adults in both taxa was variable (Figs. 1, 5 & 6). Most individuals had white venters
and brown to black backs without a distinct border between the two colours. The back may be uniform in
colouration or lighter and darker browns may be irregularly mixed. Heads had always, at least on the snout
and the eye-lids, lighter areas. The legs were always light brown with irregularly bordered darker stripes or
dots. Juveniles had brighter coloured backs than adults. Juveniles of both taxa had a black, white bordered,
lateral line, starting at the snout-tip, passing through the eyes and extending to the groin area. Their back had
Zootaxa 2355 © 2010 Magnolia Press · 61
LIBERIAN NIMBA TOAD, NIMBAPHRYNOIDES LIBERIENSIS
a golden-brownish ground colour and may carry irregular or symmetrical shaped blackish spots and figures.
Their legs were yellow to brown with white stripes. With age and increasing size their backs and legs became
darker, the contrast between differently coloured areas fainted. In comparison N. liberiensis females seemed
to comprise the most uniform, N. occidentalis, the most contrasting individuals. None of the several hundred
investigated N. occidentalis was found to have brown dots on the belly or throat. In contrast, some living N.
liberiensis had small to large light brown dots on their venter (Fig. 5). These dots seemed to be generally more
conspicuous in alcohol preserved material. In some of the latter specimens the venter was nearly completely
brown.
TABLE 1. Mean values of morphological measures of Nimbaphrynoides occidentalis and N. liberiensis (only museum
vouchers included) and t-test results between the two taxa. The sexes were compared separately. All measures had been
standardized against snout-vent length prior to comparisons. Only feet (FoL) of N. liberiensis were significantly larger
than those of N. occidentalis. For abbreviations compare Material & Methods; N = sample size; n.s. = not significant.
Both species start uttering advertisement calls at approximately the middle of the rainy season, i.e. July.
Main calling activity is however later at the beginning or middle of September. The advertisement call was
very faint, short and resembled a metallic “bing” (Fig. 7). We got recordings of this call of one N. liberiensis
male and eleven N. occidentalis males, thus allowing for descriptive analyses only. The advertisement call had
two distinct parts: it started with a slightly higher frequency and more energy and ended with lower energy
and slightly lower frequency. The longer end part was more variable than the first one. The frequencies of the
calls (total call and each part separately) of N. liberiensis (mean[total call] = 3568 Hz; mean[first part of call]
= 3565 Hz; mean[rest of call] = 3477 Hz) were slightly higher than the frequencies of N. occidentalis
(mean[total call] = 3141 Hz; mean[first part of call] = 3319 Hz; mean[rest of call] = 2775 Hz). The other call
parameters (number of pulses, lengths of the call and call parts, proportion of the energy of the second to the
first part) did not differ notably (Table 2). In N. occidentalis we recorded a second, relatively uniform
“rasping” call, mostly heard during aggressive encounters between males as well as during mating. When
uttered during antagonistic encounters this call seemed to chase an intruder away, without physical combat.
This call was considerable longer than the advertisement call (0.126 sec compared to 0.018 sec). The mean
frequency (3177 kHz) was similar to the advertisement call (Fig. 7). This call may start or, more often, end
with the advertisement call. Schiøtz (1964) reported a third call type for N. occidentalis, a slow chirp with a
sex variable species mean Nt-value df p
females HW occidentalis 0.32 12 -1.8169 16.907 n.s.
liberiensis 0.30 21
males occidentalis 0.32 6-0.8399 5.775 n.s.
liberiensis 0.30 15
females FL occidentalis 0.44 12 1.4185 25.586 n.s.
liberiensis 0.47 21
males occidentalis 0.45 61.3183 5.388 n.s.
liberiensis 0.48 15
females TL occidentalis 0.42 12 1.2579 23.932 n.s.
liberiensis 0.44 21
males occidentalis 0.44 61.5919 5.291 n.s.
liberiensis 0.48 15
females FoL occidentalis 0.65 12 3.7655 16.996 <0.05
liberiensis 0.73 19
males occidentalis 0.64 63.4065 5.789 <0.05
liberiensis 0.73 13
SANDBERGER ET AL.62 · Zootaxa 2355 © 2010 Magnolia Press
wave-like frequency modulation. He believed that this call type could be an initial call. We so far never heard
such a call.
We detected minor genetic differences between the two taxa. They were largest between the two taxa and
lowest within N. liberiensis (Table 3). However, even the largest difference between the two taxa, found in cyt
b, was only about 2%.
TABLE 2. Comparison of advertisement call (A in Fig. 7) parameters of one Nimbaphrynoides liberiensis and eleven N.
occidentalis males. The call consists of two parts, a first part (first) which is louder and higher than the second part (rest).
The latter is the more variable part of the call. For all parameters the mean and range (in parentheses) is given for the
total call, the first part and the second part of the call (rest). Length of a call and length between calls is given in seconds
[s]; main frequency given in hertz [Hz]. The energy of the first part of the call (Energyfirst) is given as relative value to the
energy of the rest of the call (Energyrest) as Energyfirst/ Energyrest.
FIGURE 4. Sex dependant snout-vent-lengths comparisons of Nimbaphrynoides occidentalis (black) and N. liberiensis
(white). N. liberiensis were significantly larger than N. occidentalis (see text).
species occidentalis liberiensis
# pulses 4.9 (3–7) 6.6 (3–13)
length [s] total call 0.018 (0.012–0.026) 0.020 (0.009–0.041)
first 0.004 (0.003–0.005) 0.005 (0.003–0.011)
rest 0.007 (0.015–0.022) 0.045 (0.005–0.255)
time to next 107.012 (48.000–471.000) 104.220 (21.960–252.000)
frequency [Hz] total call 3141 (2020–4560) 3567 (2390–5570)
first 3319 (2190–4560) 3565 (2430–5570)
rest 2775 (2020–4000) 3477 (2390–4500)
Energyfirst/ Energyrest 4.021 (0.555–11.730) 5.386 (0.324–22.220)
Zootaxa 2355 © 2010 Magnolia Press · 63
LIBERIAN NIMBA TOAD, NIMBAPHRYNOIDES LIBERIENSIS
TABLE 3. Genetic distances (uncorrected p-distance) in percent between Nimbaphrynoides occidentalis and N.
liberiensis and within each taxon, for 12S, 16S and cytb sequences. Given are mean, minimum (min) and maximum
(max) values. Below we listed all voucher and tissue samples with their corresponding GenBank accession numbers;
n.v.= no voucher collected.
Discussion
The description of N. liberiensis was mainly based on small morphological (size) and colour (dots on belly
and throat) differences to N. occidentalis (Angel 1943; Xavier 1978). These differences could be confirmed
herein. Additionally, F. Xavier undertook hybridization experiments between the two taxa in her Paris
laboratory. She found that none of the offspring survived when fathered by a Liberian and mothered by a
Guinean toad (of 15 pairings only one female gave birth, however to dead young). In contrast, 80% of the
offspring fathered and mothered by N. liberiensis were borne alive (Xavier 1978). However, F. Xavier
apparently did not try to breed a N. occidentalis female with a N. liberiensis male. The failure of getting
offspring could be due to the fact that the sizes did not fit. This species has to have internal fertilization and
size relation between sexes may thus be an important feature to assure successful fertilization. However, we
don’t believe that this is a very convincing argument (compare Fig. 5). In fact we found only very minor
genetic differences in mitochondrial gene sequences, in loci usually used for DNA-barcoding in amphibians
(compare Vieites et al. 2009). As also another important character for species delimitation in anurans, the
advertisement call, did not differ, hybridization between the two taxa seems potentially possible.
Xavier (1978) gave habitat descriptions for three localities. They were described as being open, having
steep slopes, loose stones or crevices and positioned near mining roads (presumably recorded here because of
easier access). We could find the Liberian toad exclusively in open areas (Fig. 2), and as already stated by
Xavier (1978), only above 1200 m a.s.l. and at sites with holes and cracks in the ground. The original sites
Sequence comparison 12S 16S cyt b
mean min max mean min max mean min max
Between taxa 0.002 00.005 0.002 00.004 0.020 0.016 0.023
Within liberiensis 0.001 00.005 0 0 0 0 0 0
Within occidentalis 0.001 00.003 0.002 00.005 0.007 00.013
Taxon Vou che r # Tissue # GB16S GB12S GBCytb
liberiensis ZMB 73875 MOG012 GU322838 GU322821 GU322850
ZMB 73876 MOG013 GU322839 GU322822 GU322851
n.v. MTN245 GU322840 GU322823 GU322858
n.v. MTN246 GU322841 GU322824 GU322859
n.v. MTN247 GU322842 GU322825
n.v. MTN248 GU322826
n.v. 07_204_Lib GU322828
n.v. 07_205_Lib GU322829
n.v. 07_215_Lib GU322830
occidentalis ZMB 73881 MOG018 GU322843 GU322831 GU322852
ZMB 73882 MOG019 GU322844 GU322832 GU322853
ZMB 73886 MTN83 GU322849 GB322837 GU322857
n.v. MTN15 GU322845 GU322833 GU322854
n.v. MTN16 GU322846 GU322834 GU322855
n.v. MTN22 GU322847 GU322835
n.v. MTN78 GU322848 GU322836 GU322856
SANDBERGER ET AL.64 · Zootaxa 2355 © 2010 Magnolia Press
FIGURE 5. Life coloration of Nimbaphrynoides liberiensis; above: comparison of Nimbaphrynoides females, N.
occidentalis (left) and N. liberiensis (right; ZMB 73875); centre: amplectant couple of N. liberiensis (female: ZMB
73873; male: ZMB 73874) and juvenile N. liberiensis (inlet left, ZMB 73877); below: two N. liberiensis with darker
spots on throat and belly.
Zootaxa 2355 © 2010 Magnolia Press · 65
LIBERIAN NIMBA TOAD, NIMBAPHRYNOIDES LIBERIENSIS
FIGURE 6. Female (above), male (below) and juvenile (inlet) of Nimbaphrynoides occidentalis.
SANDBERGER ET AL.66 · Zootaxa 2355 © 2010 Magnolia Press
FIGURE 7. Oscillogram and waveform of the advertisement calls (A) of Nimbaphrynoides liberiensis and N.
occidentalis and a presumed aggressive call of N. occidentalis (B, compare text).
were given as: mining plateau, Mount Alpha and mining road. Now the mining plateau and Mount Alpha are
mostly reduced to altitudes below 1200 m a.s.l. (Fig. 2) and we failed to record any toads at these sites.
Although many areas seem to equal the ones described by Xavier (1978), we only recorded the Liberian toad
at some localities and always in comparatively low densities (see Lamotte 1959; Hillers et al. 2008). Most
area above 1200 m a.s.l. is heavily altered, either offering only very compacted soil without hiding places or
consisting of loose gravel. It is very likely that the toads need good, i.e. deep and solid hiding places,
especially in order to survive the long dry season (compare Lamotte 1959). The main population now seems
to be restricted to areas south of the old mining pit. North of it we only detected two females. It seems unlikely
that the toads may migrate between these two sites as 1) the habitat in-between is extremely degraded and 2)
lays below 1200 m a.s.l. It is a good sign that these toads were capable to survive this extreme habitat
alteration. However, due to the very small and isolated habitat patches, combined with presumably very small
population sizes, the Liberian Nimba toad must be still considered Critically Endangered. Its remaining
habitats should be carefully monitored and maintained.
Remains the question whether the two Nimba toad taxa should be considered representing different
species or not. The genetic differences between Guinean and Liberian populations are minute and far below
what usually are taken to differentiate between anuran species (Rödel et al. 2003, 2009; Vences et al. 2005). In
contrast, the morphological differences (size and ventral pattern) are sufficient to correctly assign at least most
specimens to one or the other name. Furthermore, we are aware of the possibility that the observed genetic
similarity could originate from mitochondrial introgression which is not uncommon in amphibians, as has
been shown e.g. in newts (Babik et al. 2003) or the frog genera Meristogenys and Ameerega (Shimada et al.
2008; Brown & Twomey 2009). In these species nuclear genes revealed the existence of distinct differences
on the species level. Unfortunately we failed to amplify nuclear genes of the Nimba toads. Both toad taxa,
living exclusively in open, savanna like montane habitats, are separated by a distance of about 7.5 km,
comprising a forested mountain ridge. Although it is thus unlikely that both toad taxa are in frequent genetic
exchange; the observed genetic, acoustic and morphological differences altogether are too small to justify the
maintenance of two different species names. However, to account for the existence of the small genetic and
morphological differences, we propose to maintain a separate name for the Liberian population, although in
the rank of a subspecies: Nimbaphrynoides occidentalis liberiensis.
Zootaxa 2355 © 2010 Magnolia Press · 67
LIBERIAN NIMBA TOAD, NIMBAPHRYNOIDES LIBERIENSIS
Acknowledgements
We thank the “Forestry Development Authority”, namely J. Woods and T. Freeman in Liberia to allow
research on the Liberian part of the Nimba range. The Guinean authorities, particularly the “Ministère de
l’Agriculture, de l’Elevage, de l’Environnement et des Eaux et Fôrets”, represented by C.S. Kourouma,
permitted work on the Guinean part of Mount Nimba. The “Centre de Gestion de l’Environnement du Nimba-
Simandou”, the “Projet des Nations Unies de Développement” and the three “Comités Villageois de
Surveillance” allowed us to work within the World Heritage Site. The research permit in Guinea was issued
by the “Ministere de l'Education Nationale et de la Recherche Scientifique/ Direction Nationale de la
Recherche Scientifique et Technologique ” (No. 095; MNRS/DNRST). The ”Ministère du Developement
Durable et de l'Environement/ Direction Nationale des forets et faune” permitted the capture and collection of
the Guinean Nimba Toad (permis sceintifique de capture, No. 02/2008). We thank Arcelor-Mittal and
especially M. Majumdar, for accommodation, food and the permission to search at the old LAMCO mine in
Liberia. We are grateful to the “Société des Mines de Fer de Guinée” and its stuff for the financial support, and
for all the other help and support, especially to J. Suter and C. Halpin. A. Ohler and A. Dubois facilitated the
examination of the type material in the Paris collection. S. Soubzmaigne took the picture of the N. liberiensis
holotype. We especially thank the “Bundesamt für Naturschutz”, Bonn for issuing CITES import permits
(Nimbaphrynoides occidentalis; E-3117/07 and E-4074/08; Nimbaphrynoides liberiensis; E-4509/07). The
respective export permits were issued by “Le Directeur Nationale de la Protection de la Nature”(2007/ 00314)
and “L’organe de Gestion CITES Guinée” (2008/ 0049) in Guinea (Nimbaphrynoides occidentalis) and by the
“Forestry Development Authority” in Liberia (01, Nimbaphrynoides liberiensis). Last but not least we are
much indebted to our field assistants B. Doré, K. Camara and F. Gbêmou for their excellent work and good
humour.
References
Angel, F. (1943) Description d’un nouvel amphibien anoure, ovo-vivipare de la Haute-Guinée Française (Materiaux de la
mission Lamotte, au Mont-Nimba) (2e note). Bulletin du Muséum national d’Histoire naturelle, 15, 167–169.
Angel, F. & Lamotte, M. (1944) Un crapaud vivipare d’Afrique Occidentale Nectophrynoides occidentalis Angel.
Annales des Sciences naturelles, Zoologie, 6, 63–89.
Angel, F. & Lamotte, M. (1948) Nouvelles observations sur Nectophrynoides occidentalis Angel. Remarques sur le
genre Nectophrynoides. Annales des Sciences naturelles, Zoologie, 11, 115–147.
Babik, W., Szymura, J.M. & Rafinski, J. (2003) Nuclear markers, mitochondrial DNA, and male secondary sexual traits
variation in a newt hybrid zone (Triturus vulgaris x T. montandoni). Molecular Ecology, 12, 1913–1930.
Bossuyt, F. & Milinkovitch, M.C. (2000) Convergent adaptive radiations in Madagascan and Asian ranid frogs reveal
covariation between larval and adult traits. Proceedings of the National Academy of Sciences, USA, 97, 6585–6590.
Brown, J.L. & Twomey, E. (2009) Complicated histories: three new species of poison frogs of the genus Ameerega
(Anura: Dendrobatidae) from north-central Peru. Zootaxa, 2049, 1–38.
Dubois, A. (1987 ‘1986’) Miscellanea taxinomica batrachologica (I). Alytes, 5, 7–95.
Hillers, A., Loua, N.-S. & Rödel, M.-O. (2008) Assessment of the distribution and conservation status of the viviparous
toad Nimbaphrynoides occidentalis on Monts Nimba, Guinea. Endangered Species Research, 5, 13–19.
Lamotte, M. (1959) Observations écologiques sur les populations naturelles de Nectophrynoides occidentalis (Fam.
Bufonidae). Bulletin Biologique, 4, 355–413.
Lamotte, M. (1983) The undermining of Mount Nimba. Ambio, 12, 174–179.
Lamotte, M. (1998) Le mont Nimba. Réserve de la biosphère et site du patrimoine mondial (Guinée et Côte d'Ivoire).
Initiation à la géomorphologie et à la biogéographie. UNESCO publishing, Paris, 153 pp.
Lamotte, M. & Roy, R. (2003) Le peuplement animal du Mont Nimba (Guinée, Côte d'Ivoire, Liberia). Mémoires du
Musée national Histoire naturelle, 190, 1–724.
Lamotte, M. & Sanchez-Lamotte, C. (1999) Adaptation aux particularités climatiques du cycle biologique d’un anoure
tropical, Nectophrynoides occidentalis Angel, 1943 (Bufonidae). Alytes, 16, 111–122.
Palumbi, S.R. (1991) Nucleic Acids II: the Polymerase Chain Reaction. In: Hillis, D.M., Moritz, C. & Mable, B.K. (Eds)
Molecular Systematics. 2nd edition, Sinauer Associates, Sunderland, pp. 205–247.
Rödel, M.-O., Boateng, C.O., Penner, J. & Hillers, A. (2009) A new cryptic Phrynobatrachus species (Amphibia: Anura:
SANDBERGER ET AL.68 · Zootaxa 2355 © 2010 Magnolia Press
Phrynobatrachidae) from Ghana, West Africa. Zootaxa, 1970, 52–63.
Rödel, M.-O. & Ernst, R. (2004) Measuring and monitoring amphibian diversity in tropical forests. I. An evaluation of
methods with recommendations for standardization. Ecotropica, 10, 1–14.
Rödel, M.-O., Kosuch, J., Veith, M. & Ernst, R. (2003) First record of the genus Acanthixalus Laurent, 1944 from the
Upper Guinean rain forest, West Africa, with the description of a new species. Journal of Herpetology, 37, 43–52.
Schiøtz, A. (1964) The voices of some West African amphibians. Videnskabelige Meddelelser fra Dansk Naturhistorisk
Forening, 127, 35–83.
Shimada, T., Matsui, M., Yambun, P., Lakim, M. & Mohamed, M. (2008) Detection of two cryptic taxa in Meristogenys
amoropalamus (Amphibia, Ranidae) through nuclear and mitochondrial DNA analyses. Zootaxa, 1843, 24–34.
Stuart, S., Hoffman, M., Chanson, J., Cox, N. Berridge, R. Ramani, P. & Young, B. (2008) Threatened amphibians of the
World. Lynx Editions, Barcelona, 758 pp.
Swofford, D.L. (2002) PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods). 4.0 Beta for UNIX or
OpenVMS. Sinauer Associates, Sunderland, Massachusetts.
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007) MEGA 4: Molecular Evolutionary Genetics Analysis (MEGA)
software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.
Vences, M., Thomas, M., Bonett, R.M. & Vieites, D.R. (2005) Deciphering amphibian diversity through DNA
barcoding: changes and challenges. Philosophical Transactions of the Royal Society, B Biological Sciences, 360,
1859–1868.
Vieites, D.R., Wollenberg, K.C., Andreone, F., Köhler, J., Glaw, F. & Vences, M. (2009) Vast underestimation of
Madagascar’s biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy
of Sciences, USA, 106, 8267–8272.
Xavier, F. (1978) Une espèce nouvelle de Nectophrynoides (Anura, Bufonidae) des Monts Nimba, N. liberiensis n.sp. I –
description de l’espèce. Bulletin de la Société Zoologique de France, 103, 431–441.
Xavier, F. (1986) La reproduction des Nectophrynoides. In: Grassé, P.-P. & Delsol, M. (Ed) Traité de Zoologie, anatomie,
systématique, biologie. Tome XIV, Batraciens, fascicule IB. Masson, Paris, pp. 497–513.
Appendix. Study sites searched for Nimbaphrynoides liberiensis. Given are the area ID, the location (south or north of
the LAMCO mine, former mount Alpha, compare Fig. 3), latitude, longitude, altitude, search date, the number of
encountered adults (n° ad), juveniles (n° juv) and total number of toads (n° an). P1–P4 represent standardized plot
searches (25 m² see Hillers et al. 2008 for exact description), R01–R15 represent random transects.
Area location latitude longitude altitude date n° ad n° juv n° an
P1 South 7.53468 -8.50143 1293 23/08/2007 2 0 2
P2 South 7.52675 -8.51113 1295 24/08/2007 0 1 1
P3 South 7.52168 -8.51470 1323 24/08/2007 0 0 0
P4 South 7.51698 -8.52158 1329 24/08/2007 0 0 0
R01 North 7.52168 -8.52937 1267 27/07/2007 0 1 1
R02 North 7.52723 -8.50968 1318 27/07/2007 210 12
R03 South 7.51698 -8.52158 1246 23/08/2007 4 4 8
R04 South 7.51698 -8.52158 1288 23/08/2007 5 0 5
R05 South 7.51928 -8.51819 1375 24/08/2007 0 0 0
R06 South 7.54545 -8.48682 1240 25/08/2007 0 0 0
R07 South 7.54936 -8.48716 1190 25/08/2007 0 0 0
R08 South 7.54639 -8.48284 1186 25/08/2007 1 0 1
R09 South 7.53442 -8.50091 1249 25/05/2008 0 0 0
R10 South 7.53408 -8.50194 1281 25/05/2008 16 016
R11 North 7.54944 -8.47970 1302 26/05/2008 0 0 0
R12 North 7.54785 -8.48130 1234 26/05/2008 1 0 1
R13 North 7.54731 -8.48258 1180 26/05/2008 0 0 0
R14 South 7.52808 -8.50989 1313 27/05/2008 5 0 5
R15 South 7.51685 -8.52131 1324 27/05/2008 0 0 0
... While the amphibian fauna of Mounts Nimba ranks among the most species rich and most intensively studied of the amphibian faunas in West Africa , almost all research has been done on the Guinean and Liberian parts of the mountain range (e.g., Lamotte 1958a,b, 1963;Xavier 1978;Rödel et al. 2010;Sandberger et al. 2010;Sandberger-Loua et al. 2018a;Schäfer et al. 2019), and none has ever focused exclusively on the Ivorian part of the mountains. One particular research focus was on the viviparous toad Nimbaphrynoides occidentalis (Angel, 1943), which is a flagship species for the conservation of the area (e.g., Lamotte 1959;Lamotte and Sanchez-Lamotte 1999;Hillers et al. 2008a;Xavier 2009;Sandberger-Loua et al. 2010, 2018b. ...
... While the amphibian fauna of Mounts Nimba ranks among the most species rich and most intensively studied of the amphibian faunas in West Africa , almost all research has been done on the Guinean and Liberian parts of the mountain range (e.g., Lamotte 1958a,b, 1963;Xavier 1978;Rödel et al. 2010;Sandberger et al. 2010;Sandberger-Loua et al. 2018a;Schäfer et al. 2019), and none has ever focused exclusively on the Ivorian part of the mountains. One particular research focus was on the viviparous toad Nimbaphrynoides occidentalis (Angel, 1943), which is a flagship species for the conservation of the area (e.g., Lamotte 1959;Lamotte and Sanchez-Lamotte 1999;Hillers et al. 2008a;Xavier 2009;Sandberger-Loua et al. 2010, 2018b. However, although much research effort has been directed to the amphibian fauna of the Nimba Mountains, as indicated by the accumulation of tens of thousands of amphibian vouchers at the Muséum National d'Histoire Naturelle in Paris, new records and new species descriptions continue to be published from the Guinean and Liberian parts of Mounts Nimba Barej et al. 2015;Sandberger-Loua et al. 2018a). ...
... (Lamotte 1959;Lamotte and Sanchez-Lamotte 1999;Hillers et al. 2008;Sandberger-Loua et al. 2016. The toads live in montane grasslands above 1,200 m asl, where they go into dormancy during the dry season (Lamotte 1959;Hillers et al. 2008;Sandberger et al. 2010). Nimbaphrynoides occidentalis comprises two subspecies isolated by a forested mountain ridge: the larger N. occidentalis liberiensis is restricted to one site in Liberia, while N. occidentalis occidentalis occurs in a few sub-populations in Guinea and Ivory Coast (Sandberger et al. 2010). ...
Article
Full-text available
This article provides the first assessment and commented checklist of the anuran diversity of the Ivorian part of the Mount Nimba Integrated Nature Reserve (MNINR), West Africa. During a period of 81 days from 18 June 2018 to 17 May 2019, covering both the rainy and dry seasons, 53 amphibian species were recorded. Among these species, 30.2% were endemic to either the Upper Guinea forest zone or smaller areas within that biodiversity hotspot. The amphibian fauna of the Ivorian slope of the MNINR is very similar to those of the Guinean side of Mounts Nimba and the Guinean Simandou Range. Based on the current IUCN Red List data, several recorded species are of high conservation concern: the Critically Endangered Nimbaphrynoides occidentalis; the Endangered Hyperolius nimbae; and the Near Threatened Leptopelis macrotis, Leptopelis occidentalis, and Odontobatrachus arndti. Of particular interest among the survey records were the poorly known Ptychadena arnei, P. pujoli, and P. submascareniensis. The records of Ptychadena retropunctata and Arthroleptis crusculum represent first country records for Ivory Coast, while the records of Odontobatrachus arndti and Phrynobatrachus fraterculus are the second records for the country. In contrast to the Guinean and Liberian parts of Mounts Nimba, the Ivorian part had never been mined or explored for mining, nor do such plans currently exist. As a result, the study area still holds intact mountain forests that include rare and unique habitats with exceptional biodiversity, which need to be preserved for future generations. Consequently, conservation strategies should minimize bush-fires in mountain grasslands, e.g., to protect the viviparous toad N. occidentalis. At lower elevations, it is important to encourage local activities concerning reforestation of the previously forested areas and the conservation of the (sacred) village forests.
... The Nimba Mountains as a Center of Bat Diversity and Endemism: The Nimba Mountains are well known as a center of biodiversity and endemism (Brosset, 2003;Lamotte and Roy, 2003;Wieringa and Poorter, 2004;Sandberger et al., 2010;Denys and FIGURE 11. Bayesian phylogenetic reconstruction of subgenus Chrysopteron using an alignment of 634 base pairs of mitochondrial gene cytochrome b. ...
Article
Full-text available
The genus Myotis is a diverse group of vespertilionid bats found on nearly every continent. One clade in this group, the subgenus Chrysopteron, is characterized by reddish to yellowish fur and, in some cases, visually striking dichromatic wing pigmentation. Here, we describe a new dichromatic species of Myotis (Chrysopteron) from the Nimba Mountains in Guinea. The new species is superficially similar to Myotis welwitschii, but phylogenetic analyses based on cytochrome b data indicated that it is actually more closely related to M. tricolor. Discovery of this new taxon increases the number of Myotis species known from mainland Africa to 11 species, although patterns of molecular divergence suggest that cryptic species in the Chrysopteron clade remain to be described. This discovery also highlights the critical importance of the Nimba Mountains as a center of bat diversity and endemism in sub-Saharan Africa.
... Nimba (Coe et al. 1975;Lamotte and Roy 2003). Indeed, two species of freshwater crabs (Liberonautes lugbe and L. nimba), a dragonfly (Paragomphus kiautai), and one of the world's viviparous frog species (Nimbaphrynoides occidentalis), are all endemic to Mt. Nimba (Lamotte and Roy 2003;Sandberger et al. 2010). Plant species diversity is also high, with a significant number of plants endemic to Mt. Nimba (Marshall and Hawthorne 2013;Wieringa and Poorter 2004). ...
Preprint
The Upper Guinea rainforest zone in West Africa is considered a biodiversity hotspot and contains important habitats for threatened and endemic mammals, yet this region remains poorly known particularly for small mammals. The aim of this study was to survey small mammals in a Liberian and Guinean cross-border conservation area, the Ziama-Wonegizi-Wologizi landscape. We recorded a total of 52 small mammal species, including 26 bats, 15 rodents, 10 shrews, one otter-shrew, of which one rodent species was new to science (Colomys sp. nov.). We also documented the first country records of the bats Chaerephon aloysiisabaudiae, Pseudoromicia brunnea and Pipistrellus inexspectatus from Guinea, and the shrews Crocidura douceti and Crocidura grandiceps from Liberia. Furthermore, we recorded the recently described bat Nyc-ticeinops happoldorum from Wologizi and Ziama, and we documented the presence of Micropotamogale lamottei at Wologizi, which represents the fourth known locality for this globally threatened species. Finally, the forests of Wologizi and Ziama support numerous threatened species. The results of our survey demonstrate the importance of this region for small mammals and support the creation of a transboundary protected area that will encompass the entire forest landscape.
... But males of Rhinella rubescens (Lutz, 1925) (Chaparro et al., 2007 become sexually mature even earlier than R. arenarum and R. diptycha, and can be considered ready to reproduce approximately after 200 days (age class 0þ) after metamorphosis (Arantes et al. 2015). Other toads such the Central American Incillus valliceps (Wiegmann, 1833) (Frost et al., 2009 (Blair, 1953) or males of the viviparous toad Nimbaphrynoides occidentalis (Angel, 1943) (Sandberger-Loua et al., 2010 (Castanet et al., 2000) can reach sexual maturity within the first year after metamorphosis. The same applies for ranid frogs such as Rana latastei Boulenger, 1879 (Guarino et al., 2003), or Lithobates septentrionalis (Baird, 1854) (Fouquette & Dubois, 2014) (Leclair & Laurin, 1996) and the dicroglossid Hoplobatrachus tigerinus (Daudin, 1862) (Dubois, 1992) (Gramapurohit et al., 2004) but also in tropical caecilian amphibians such as Geotrypetes seraphini occidentalis (Dum eril, 1859) (Parker, 1936) males mature in less than a year (Scholz et al., 2010). ...
... Likewise, the French Jean Guibé and Maxime Lamotte dealt predominantly with the fauna of the Guinean part of Mount Nimba, but included Liberian material in their papers (Guibé andLamotte 1958a, 1963). From the Liberian part of Mount Nimba a second species of viviparous toad, Nimbaphynoides liberiensis, was described (Xavier 1978), which was, however, later synonymized with the Guinean populations (Sandberger et al. 2010). Further Liberian records and new species were published by Parker (1936) and Taylor and Weyer (1958). ...
Article
Full-text available
In March and April 2018 we surveyed amphibians and reptiles in two Proposed Protected Areas (PPAs) in Liberia. In the Krahn-Bassa Proposed Protected Area (KBPPA) in eastern Liberia 36 species of amphibians and 13 species of reptiles were recorded. In the Foya Proposed Protected Area (FPPA) in western Liberia 39 species of amphibians and 10 species of reptiles were recorded. The encountered herpetological communities in both sites were typical for West African rainforests. However, some species indicated disturbances, in particular at the edges of the study areas, the surrounding villages and plantations, and old artisanal gold mining sites within forests. Of particular conservation interest was the discovery of a high percentage of typical rainforest specialists with ranges restricted to the western part of the Upper Guinea rainforest biodiversity hotspot. Outstanding discoveries in KBPPA were two new species of puddle frogs, and the first country record for the arboreal, parachuting lizard Holaspisguentheri . Remarkable records in FPPA comprise a new species of stiletto snake, a new puddle frog and records of various frog species typically breeding in undisturbed rainforest streams, such as Odontobatrachusnatator and Conrauaalleni . Both study areas comprise an important proportion of the remaining rainforests in the Upper Guinea forest zone. The new discoveries indicate that within this biogeographic area, southeastern and western Liberian rainforest may still hold various undiscovered species and species of conservation concern. Further surveys in KBPPA and FPPA and nearby forests should clarify the distribution and conservation status of the new taxa. This study also emphasizes that the western part of the Liberian forests comprise at least partly a herpetofauna which differs from that of the East of the country. The recorded threatened amphibian species are all specialized on relatively undisturbed rainforests and they all have only small geographic ranges. The remaining parts of undisturbed or little disturbed forests thus have high importance for the long-term survival of these species. In conclusion the study areas have a high conservation potential and should be urgently protected from any further forest loss degradation and uncontrolled hunting.
... Dubois (1986) revised the genus Nectophrynoides, which at that time comprised oviparous, lecitotrophic viviparous and matrotrophic viviparous species and placed them, according to their reproductive mode, into four different genera: Spinophrynoides (for the oviparous Ethiopian S. osgoodi, now placed in Altiphrynoides and feared to be extinct; Gower et al. 2013), Altiphrynoides (for the direct developing A. malcolmi from Ethiopia), Nectophrynoides (now 13 lecitotrophic pueriparous species all from Tanzania, one extinct in the wild), and Nimbaphrynoides (now one species from the Nimba mountains in Guinea, Ivory Coast and Liberia). The Nimbaphrynoides population from Liberia was described as a separate species (Xavier 1978), but because of high genetic and acoustic similarity is now considered to be a sub-species of N. occidentalis (Sandberger et al. 2010). Based on morphological data it was assumed that N. occidentalis is more closely related to Altiphrynoides than to Nectophrynoides (Wake 1980b, Grandison 1981, and most closely related to Didynamipus sjostedti (Grandison 1981, Graybeal andCannatella 1995), a small, probably direct developing forest toad from Cameroon (Gonwouo et al. 2013). ...
Article
Full-text available
Amphibians, and anurans in particular, show the highest diversity of reproductive modes among tetrapods. Nevertheless, viviparity is scarce in anurans and its occurrence is even more often assumed rather than confirmed. Probably the best studied viviparous amphibian is the Nimba toad, Nimbaphrynoides occidentalis. During more than 40 years of research, the Nimba toad’s reproductive morphology, endocrine activity of the ovary as well as the pituitary gland, and to some extent the ecological impact (seasonality, humidity, food availability) on reproduction was examined. Due to the Nimba toad’s unique reproductive mode, summaries are usually included in reviews discussing amphibian reproduction and articles on reproductive biology often discuss the exceptional reproductive system of Nimba toads. However, to our knowledge a detailed synthesis, summarising all the different original studies on the toad’s reproduction, is so far missing. In this paper we review and summarise all available initial publications, which often have been published in French and/or are difficult to access. A short overview is given of the climatic and environmental conditions experienced by Nimba toads and the key findings supporting a “true” viviparous reproduction with matrotrophy (maternal provision of nutrition during the gestation) and pueriparity (birth of juveniles). Then foetal development (morphological, gonad and pituitary development), and the female (ovary, oviduct, pituitary and their endocrine interactions) and the male reproductive system (testes and pituitary) are reviewed. Finally, the reproductive cycle and its link to the Nimba mountains’ seasonality and ecological/ conservation implications are discussed.
Article
Full-text available
The eyes of frogs and toads (Anura) are among their most fascinating features. Although several pupil shapes have been described, the diversity, evolution, and functional role of the pupil in anurans have received little attention. Studying photographs of more than 3200 species, we surveyed pupil diversity, described their morphological variation, tested correlation with adult habits and diel activity, and discussed major evolutionary patterns considering iris anatomy and visual ecology. Our results indicated that the pupil in anurans is a highly plastic structure, with seven main pupil shapes that evolved at least 116 times during the history of the group. We found no significant correlation between pupil shape, adult habits, and diel activity, with the exception of the circular pupil and aquatic habits. The vertical pupil arose at least in the most recent common ancestor of batrachians, and this morphology is present in most early-diverging anuran clades. Subsequently, a horizontal pupil, a very uncommon shape in vertebrates, evolved in most neobatrachian frogs. This shape evolved into most other known pupil shapes, but it persisted in a large number of species with diverse life histories, habits and diel activity patterns, demonstrating a remarkable functional and ecological versatility.
Article
Aim The diversity of brood size across animal species exceeds the diversity of most other life‐history traits. In some environments, reproductive success increases with brood size, whereas in others it increases with smaller broods. The dominant hypothesis explaining such diversity predicts that selection on brood size varies along climatic gradients, creating latitudinal fecundity patterns. Another hypothesis predicts that diversity in fecundity arises among species adapted to different microhabitats within assemblages. A more recent hypothesis concerned with the consequences of these evolutionary processes in the era of anthropogenic environmental change predicts that low‐fecundity species might fail to recover from demographic collapses caused by rapid environmental alterations, making them more susceptible to extinctions. These hypotheses have been addressed predominantly in endotherms and only rarely in other taxa. Here, we address all three hypotheses in amphibians globally. Location Global. Time period Present. Major taxa studied Class Amphibia. Methods Using a dataset spanning 2,045 species from all three amphibian orders, we adopt multiple phylogenetic approaches to investigate the association between brood size and climatic, ecological and phenotypic predictors, and according to species conservation status. Results Brood size increases with latitude. This tendency is much stronger in frogs, where temperature seasonality is the dominant driver, whereas salamander fecundity increases towards regions with more constant rainfall. These relationships vary across continents but confirm seasonality as the key driver of fecundity. Ecologically, nesting sites predict brood size in frogs, but not in salamanders. Finally, we show that extinction risk increases consistently with decreasing fecundity across amphibians, whereas body size is a “by‐product” correlate of extinction, given its relationship with fecundity. Main conclusions Climatic seasonality and microhabitats are primary drivers of fecundity evolution. Our finding that low fecundity increases extinction risk reinforces the need to refocus extinction hypotheses based on a suggested role for body size.
Article
Genome size varies widely among organisms and is known to affect vertebrate development, morphology, and physiology. In amphibians, genome size is hypothesized to contribute to loss of late-forming structures, although this hypothesis has mainly been discussed in salamanders. Here we estimated genome size for 22 anuran species and combined this novel data set with existing genome size data for an additional 234 anuran species to determine whether larger genome size is associated with loss of a late-forming anuran sensory structure, the tympanic middle ear. We established that genome size is negatively correlated with development rate across 90 anuran species and found that genome size evolution is correlated with evolutionary loss of the middle ear bone (columella) among 241 species (224 eared and 17 earless). We further tested whether the development of the tympanic middle ear could be constrained by large cell sizes and small body sizes during key stages of tympanic middle ear development (metamorphosis). Together, our evidence suggests that larger genomes, slower development rate, and smaller body sizes at metamorphosis may contribute to the loss of the anuran tympanic middle ear. We conclude that increases in anuran genome size, although less drastic than those in salamanders, may affect development of late-forming traits.
Article
We describe three new species of poison frogs discovered on recent expeditions throughout Central Peru. Two of these were discovered from the Serranía de Contamana, a small mountain range near the town of Contamana on the Río Ucayali in Central Peru. The first of these species is similar in appearance to Ameerega petersi, but the two species differ in call and size, have allopatric distributions, and are not close relatives according to a Bayesian phylogeny. This species is also similar morphologically to A. pongoensis, although the latter lacks flash marks above the groin and has a distinct advertisement call. Our phylogenetic data suggest that this species is closely related to A. bassleri, a species which is much larger and usually possesses a brightly-colored yellow or orange dorsum. The second new species has a red dorsum and is similar in appearance to A. bassleri, A. cainarachi, and the third new species described herein, but can be distinguished by its unusual advertisement call. The third new species in this paper was discovered in the upper Huallaga Valley near the towns of Tocache and Juanjui. This species resembles certain populations of A. bassleri and the second new species (mentioned above), but can be diagnosed by its advertisement call which is significantly slower than its closest relatives; approximately one-half the speed of A. bassleri and one-quarter the speed of the second new species. Finally, we discuss the biogeography of the A. bassleri clade in light of these new discoveries. The biogeography of this clade is consistent with the disturbance-vicariance hypothesis, and climatic fluctuations were likely a major driver in the divergence and speciation of this group. We also present a phylogeny with increased sampling in the A. petersi clade and discuss the taxonomy of the group.
Article
The same geologic and geomorphic traits responsible for Mount Nimba's impressive relief, scenic beauty, and biological diversity could bring about its destruction, for it is actually a mountain of iron ore. If mining continues to eat away at this extraordinary site, an irreplaceable part of our world heritage might well be lost.-from Author
Article
We identified three distinct sympatric lineages of frogs among specimens previously considered a single species (Meristogenys amoropalamus Matsui), based on 909 bp of mitochondrial DNA (12S rRNA and cytochrome b). To seek evidence of reproductive isolation between these lineages, we first analyzed a 249-bp fragment of the nuclear proopiomelanocortin (POMC) gene and found five haplotypes, of which two were limited to lineage 1 and three belonged to lineages 3 and 4. In a subsequent phylogenetic analysis of a 1313-bp fragment of nuclear POMC, Rag-1, and rhodopsin, lineage 1 was again distinct, while lineages 3 and 4 could not be differentiated. The results of the nuclear gene analyses suggest that lineage 1 is strongly isolated reproductively from lineages 3 and 4, which are not isolated from each other. This conclusion conforms to groupings based on larval morphology. These results indicate that frogs morphologically identified as M. amoropalamus should be split into two sympatric species, one of which contains two mitochondrial lineages that have presumably been retained via deep coalescence.