Content uploaded by Luca Luiselli
Author content
All content in this area was uploaded by Luca Luiselli on Nov 10, 2022
Content may be subject to copyright.
Citation: Segniagbeto, G.H.;
Dekawole, J.K.; Ketoh, G.K.; Dendi,
D.; Luiselli, L. Herpetofaunal
Diversity in a Dahomey Gap
Savannah of Togo (West Africa):
Effects of Seasons on the Populations
of Amphibians and Reptiles.
Diversity 2022,14, 964. https://
doi.org/10.3390/d14110964
Academic Editors: Michael Wink and
Geraldo Jorge Barbosa De Moura
Received: 2 October 2022
Accepted: 8 November 2022
Published: 10 November 2022
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
published maps and institutional affil-
iations.
Copyright: © 2022 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
diversity
Article
Herpetofaunal Diversity in a Dahomey Gap Savannah of Togo
(West Africa): Effects of Seasons on the Populations of
Amphibians and Reptiles
Gabriel HoinsoudéSegniagbeto 1, Jeanne Kafui Dekawole 1, Guillaume Koffivi Ketoh 1, Daniele Dendi 1,2,3
and Luca Luiselli 1,2,3,*
1Laboratory of Ecology and Ecotoxicology, Faculty of Sciences, University of Lomé, Lomé01 BP 1515, Togo
2Institute for Development, Ecology, Conservation and Cooperation, via G. Tomasi di Lampedusa 33,
I-00144 Rome, Italy
3Department of Animal and Environmental Biology, Rivers State University of Science and Technology,
Port Harcourt P.M.B. 5080, Nigeria
*Correspondence: l.luiselli@ideccngo.org or lucamaria.luiselli@uniroma3.it
Abstract:
The Dahomey Gap is a human-derived savannah zone, interspersed by patches of moist
tropical forest, that separates the forest zone into two blocks, the Upper Guinean and the Lower
Guinean forests. Community ecology aspects of amphibians and reptiles are still relatively unexplored
in this ecological zone of West Africa. Here, the overall species richness and the variation of the
diversity metrics (dominance, evenness) of a whole herpetofaunal community in Togo was studied,
with emphasis on the effects of the seasons (wet and dry) on the population structure. Overall, we
observed 998 amphibian individuals from 27 species: 148 individuals belonging to 11 species during
the dry season and 849 individuals belonging to 25 species during the wet season. For reptiles, we
observed 517 individuals belonging to 44 species: 323 individuals belonging to 41 species during the
dry season and 194 individuals belonging to 28 species during the wet season. The analyses on the
diversity metrics showed opposite patterns between amphibians and reptiles in each season. Indeed,
the dry season rank–abundance curve was systematically higher in reptiles than in amphibians for
each rank of abundance, while the opposite pattern occurred in the wet season rank–abundance
curve. Singletons and doubletons were much more numerous in the reptiles. Concerning the diversity
indices, the Dominance index was significantly higher in amphibians during the dry season than in
all other pairwise comparisons, whereas the Shannon’s index was significantly lower in dry season
amphibians and significantly higher in wet season reptiles. Evenness index was significantly lower
in reptiles than in amphibians and the mean number of individuals was significantly higher in
amphibians by wet season compared to dry season amphibians or reptiles during both seasons. The
ecological implications of these data are discussed. Most species were of minor conservation concern.
Keywords: amphibia; reptilia; community ecology; West African savannah; diversity metrics
1. Introduction
The so-called “Dahomey Gap” situated along the West African Gulf of Guinea coast
in Benin, Togo, and eastern Ghana is a human-derived vegetation zone that originated
in historical times and that is a savannah-like vegetation zone interspersed by patches of
moist tropical forest. This human-derived vegetation zone is ecologically very important as
it separates the forest zone that covers much of the south of the region into two separate
forest regions, i.e., the Upper Guinean and the Lower Guinean forests [1].
Compared to the Upper and Lower Guinean forests, the organismal communities of
the Dahomey Gap savannahs have been far less intensely studied, probably because the
general perception is that these savannahs are poorly speciose and of lesser conservation
interest, as they are human-derived and broadly altered by human activities. However,
Diversity 2022,14, 964. https://doi.org/10.3390/d14110964 https://www.mdpi.com/journal/diversity
Diversity 2022,14, 964 2 of 15
some studies focusing on the community composition and resource partitioning patterns
of Dahomey Gap turtles [
2
,
3
] and lizards [
4
] are available, with other more comprehensive
studies on the distribution records and taxonomy of the Togolese species [
5
–
9
]. Nonetheless,
no previous study has reported any inventory of the species and the diversity metrics of
a whole community of reptiles and amphibians at a given area within the Dahomey
Gap savannah region. Thus, we still do not know much about (i) the overall species
richness and (ii) the variation of the diversity metrics (dominance, evenness) of the whole
herpetofauna communities of the Dahomey Gap by seasons (wet and dry). This study is the
first contribution aiming at investigating these two aspects within a same article. Indeed,
the objective of this study is (1) to carry out the most complete herpetological inventory
possible in both the dry and the wet seasons, (2) to evaluate the quantitative differences
between amphibians and reptiles in terms of diversity metrics, (3) to evaluate the effects of
the season on the diversity metrics and the community composition of both amphibians
and reptiles, and (4) to evaluate the presence and relative sighting frequency of priority
species for conservation according to IUCN [10].
More specifically, because the African savannah habitats are strongly seasonal with
prolonged droughts during the dry months [11–13], we hypothesize that:
(a)
The various diversity metrics should be very different between amphibians and
reptiles, given their divergent tolerance to the climatic conditions (especially rainfall)
between dry and wet seasons, and because of their different role within the savannah
trophic chains. That is, the mean number of amphibian individuals per species should
be higher than the mean number of reptile individuals per species, given that these
latter are high-rank predators in the savannah trophic chains (for instance, some
snakes, see [14]).
(b) Amphibians should be more impacted than reptiles by the dry season months, as they
are more linked to water bodies and humidity threshold than reptiles. That is, the
number of amphibian species and individuals should be significantly lower by dry
season, with consequent increase in the dominance and decrease in the evenness of
the assemblage, whereas the same inter-seasonal difference should be less evident in
reptiles.
(c)
In reptiles, dominance and evenness should be relatively independent on season,
although excessive heat and drought may also depress the reptilian assemblages.
2. Materials and Methods
2.1. Study Area
The present study was conducted in Togo (West Africa) as part of a herpetological
fauna assessment relating to the construction of a hydroelectric dam on the Mono River in
an area between the locality of Tetetou in the south and the Nangbeto dam in the north
(Figure 1). Ecologically, the study area is located in the Guinean lowland climate zone,
within the Benin-Togolese plain east of the Atakora range.
The main habitats are shrub savannahs with sparse woodlands, with main vegetation
being dominated by Combretaceae and Andropogoneaceae such as Daniellia oliveri,Termi-
nalia macroptera,Combretum spp., Pterocarpus erinaceus,Parkia biglobosa,Vitellaria paradoxa,
etc. There are also scattered islands of semi-deciduous dry forests as well as forest galleries
along the main rivers and streams, whose main species are Cynometra megalophylla,Parinari
congensis,Pterocarpus santalinoides, etc. This common vegetation in the region includes some
endangered tree species such as Pterocarpus erinaceus, for example.
Savannah and dry forest habitats are under pressure at the study area from rampant
agricultural expansion and population growth leading to deforestation and degradation of
environments for planting and crops and for harvesting firewood.
Diversity 2022,14, 964 3 of 15
Diversity 2022, 14, x FOR PEER REVIEW 3 of 15
Savannah and dry forest habitats are under pressure at the study area from rampant
agricultural expansion and population growth leading to deforestation and degradation
of environments for planting and crops and for harvesting firewood.
Figure 1. Map of southern Togo, showing the study area. The land use is also included.
2.2. Protocol
The study was carried out from 1 to 14 October 2021 (end of the wet season) and 28
February to 14 March 2022 (end of the dry season). During each season, a total of 105 man-
hours were spent in the field.
Visual Encounter Surveys (VES) were carried out to assess the specific herpetofauna
richness of the study area as this method assures a good determination of the communities
of species at the local level, and to estimate the relative abundances of species within a
community [15]. We explored all the available habitat types, including temporary pools,
gallery forests, rivers, but also savannas and some fallow land. Reptiles were inventoried
in all the habitats present in the study area.
The search techniques consisted of a visual sweep of the terrain and the inspection of
potential shelters: the leaves, trunks and branches of trees for arboreal species, bodies of
water for aquatic species, all potential shelters for terrestrial species (plant debris, trees,
burrows), ground shelters for burrowing species. Signs of presence were noted (drop-
pings, burrows, footprints, manifestations, moults, shells, skeletons). The search for both
amphibians and reptiles took place day (for at least 4 h per day) and night (for at least 3 h
per day), with a significant portion of reptile species having nocturnal activity. At night,
flashlights were used to observe specimens in the field. We conducted surveys also fol-
lowing hard rains as these are usually very productive in tropical forest habitats. Local
guides also helped in collecting herpetofauna individuals. For amphibians, the fieldwork
was mainly concentrated in habitats with the presence of water. The different individuals
were mostly noted opportunistically during the visual surveys. The songs of male am-
phibians observed at night were used for the identification and counting of species.
The identifications of the different species were carried out following the identifica-
tion keys/criteria of [16,17] for snakes, and [18] for other reptiles. For amphibians, species
Figure 1. Map of southern Togo, showing the study area. The land use is also included.
2.2. Protocol
The study was carried out from 1 to 14 October 2021 (end of the wet season) and
28 February to 14 March 2022 (end of the dry season). During each season, a total of
105 man-hours were spent in the field.
Visual Encounter Surveys (VES) were carried out to assess the specific herpetofauna
richness of the study area as this method assures a good determination of the communities
of species at the local level, and to estimate the relative abundances of species within a
community [
15
]. We explored all the available habitat types, including temporary pools,
gallery forests, rivers, but also savannas and some fallow land. Reptiles were inventoried
in all the habitats present in the study area.
The search techniques consisted of a visual sweep of the terrain and the inspection
of potential shelters: the leaves, trunks and branches of trees for arboreal species, bodies
of water for aquatic species, all potential shelters for terrestrial species (plant debris,
trees, burrows), ground shelters for burrowing species. Signs of presence were noted
(droppings, burrows, footprints, manifestations, moults, shells, skeletons). The search for
both amphibians and reptiles took place day (for at least 4 h per day) and night (for at
least 3 h per day), with a significant portion of reptile species having nocturnal activity.
At night, flashlights were used to observe specimens in the field. We conducted surveys
also following hard rains as these are usually very productive in tropical forest habitats.
Local guides also helped in collecting herpetofauna individuals. For amphibians, the
fieldwork was mainly concentrated in habitats with the presence of water. The different
individuals were mostly noted opportunistically during the visual surveys. The songs of
male amphibians observed at night were used for the identification and counting of species.
The identifications of the different species were carried out following the identification
keys/criteria of [
16
,
17
] for snakes, and [
18
] for other reptiles. For amphibians, species
Diversity 2022,14, 964 4 of 15
identifications were carried out following the identification keys/criteria of [
19
]. The
taxonomy follows [20].
On the different sites, for each sighting, we recorded, in an Excel spreadsheet: (i) species
name, (ii) date of observation, (iii) number of individuals, (iv) age and sex (if determinable),
(v) habitat and habitat quality, (vi) sign of presence (seen/heard), (vii) GPS coordinates,
(viii) photograph number if individual is photographed, etc.
2.3. Statistical Analyses
Several distinct measures of community diversity were calculated for both amphibians
and reptiles [21,22]:
(a)
Species richness, the total number of taxa recorded into each plantation type at each
study area and during the wet or the dry season;
(b)
Dominance,
D=1−impson index (1)
and ranges from 0 (all taxa are equally present) to 1 (one taxon dominates the commu-
nity completely);
(c)
Shannon H’ index, varying from 0 for communities with only a single taxon to high
values for communities with many taxa, each with few individuals [
22
]. Shannon’s
index (H’) is
H’ = −S(fr) ×[ln(fr)], (2)
where Sis the total number of amphibian or reptile species recorded, fr =n/N,nis the
number of individuals of each species in each season and Nis the total number of
individuals of each taxon (amphibians or reptiles) in the study area.
(d)
Pielou’s Evenness index, calculated as
e=H’/Hmax, (3)
where
Hmax =lnS, (4)
with H’ representing Shannon’s index, and Sthe total number of amphibian or reptile
species recorded. Hmax corresponds to the maximum value of diversity (i.e., when all
species are equally represented in our samples [21]).
(e)
Chao-1 index that calculated the predicted number of species at a given site given the
observed sample size and the observed number of species. Chao-1 index is
Chao-1 =S+F1(F1 −1)/(2(F2 +1), (5)
where F1 is the number of singleton species and F2 the number of doubleton species.
A singleton is a species occurring only once in the total sample, and doubleton is a
species occurring just twice in the total sample.
The various indices were calculated using the raw data for the two seasons, because
the survey field effort was identical at each season (hence unbiased). Bootstrap analysis was
applied to generate upper and lower confidence intervals of all indices, with 1000 random
samples being generated, each with the same total number of individuals as in each original
sample [22].
We performed individual rarefaction curves to evaluate the completeness of the
samples done by season and for both amphibians and reptiles. This module estimates how
many taxa you would expect to find in samples with a smaller total number of individuals.
In other words, by this method, it is possible to read out the number of expected taxa
for any smaller sample size [
23
]. We also graphically compared diversities in the several
samples (i.e., in both amphibians and reptiles and in both seasons) by the diversity profile
models [
24
]. We also used diversity profiles because they are not subjected to any issues
that may arise from the arbitrary choice of a given diversity index to describe a given
Diversity 2022,14, 964 5 of 15
study community. We bootstrapped the data (giving a 95% confidence interval) with
2000 replicates.
We evaluated the statistical differences in the diversity indices between seasons and be-
tween taxa (amphibians versus reptiles) using One-Way Analysis of Similarities (ANOSIM).
ANOSIM is roughly analogous to an ANOVA in which the univariate response variable
is replaced by a dissimilarity matrix, i.e., with distances that were converted to ranks.
Significance was computed by permutation of group membership, with 9999 replicates,
and Bray–Curtis was used as distance measure. We used a sequential Bonferroni correction
for post hoc pairwise comparisons between all pairs of groups. ANOSIM was performed
in R-software, using Vegan package [25].
Differences in the mean number of individuals per species by season and by taxon
(amphibians versus reptiles) were analyzed by one-way ANOVAs. All other analyses were
performed using PAST software, with alpha set at 5%.
3. Results
3.1. Amphibians
The checklist of the amphibians and their conservation status is given in Table 1.
Overall, we observed 803 individuals belonging to 24 species (Figure 2): 145 individuals
belonging to 10 species during the dry season and 658 individuals belonging to 23 species
during the wet season (Table 1). An additional three species were not directly observed but
were cited in the literature (Table 1). Saturation curves revealed that the plateau phase was
reached in both seasons (Figure 3a), with 12 species predicted to occur in the area by dry
season and 26 by wet season according to Chao-1 index. Diversity indices revealed a much
higher diversity and evenness by wet season than by dry season (Table 2), and diversity
profile curves showed that the two seasonal samples were very different from each another
(Figure 3b). There were no singletons and only one doubleton (Kassina cassinoides). Several
species were very abundant, with Phrynobatrachus latifrons, Ptychadena sp., Ptychadena
oxyrhynchus, and Sclerophrys regularis being the most common.
Diversity 2022, 14, x FOR PEER REVIEW 8 of 15
Figure 2. Some of the amphibian species recorded in the present study.
Figure 3. Saturation curves and diversity profiles (with 95% confidence intervals) for amphibians
and reptiles during the dry and wet seasons. Saturation curves are (a) for amphibians and (c) for
reptiles. Diversity profiles are (b) for amphibians and (d) for reptiles.
Figure 2. Some of the amphibian species recorded in the present study.
Diversity 2022,14, 964 6 of 15
Table 1.
Number of individuals of reptiles and amphibians (including both alive and dead specimens)
observed at the study area, during the wet and the dry season, including their IUCN (2022) Red List
status, and the type of record.
Family Species Type of
Record
Observed
Number in Dry
Season
Observed
Number in Wet
Season
IUCN
(2022)
Amphibia
Arthroleptidae Arthroleptis poecilonotus O 0 21 LC
Arthroleptidae Leptopelis spiritusnoctis O 8 35 LC
Arthroleptidae Leptopelis viridis O 0 3 LC
Bufonidae Sclerophrys maculatus O 0 51 LC
Bufonidae Sclerophrys regularis O 25 110 LC
Hyperoliidae Afrixalus dorsalis O 0 30 LC
Hyperoliidae Afrixalus vittiger O 0 23 LC
Hyperoliidae Afrixalus weidholzi O 0 3 LC
Hemissotidae Hemisus marmoratus O 3 1 LC
Hyperoliidae Hyperolius concolor O 0 50 LC
Hyperoliidae Hyperolius igbettensis O 0 40 LC
Hyperoliidae Hyperolius nitidulus O 0 18 LC
Hyperoliidae Kassina fusca B LC
Hyperoliidae Kassina cassinoides O 0 2 LC
Hyperoliidae Kassina senegalensis O 0 17 LC
Phrynobatrachidae Phrynobatrachus latifrons O 20 17 LC
Phrynobatrachidae Phrynobatrachus natalensis O 5 0 LC
Pipidae Xenopus fischbergi O 0 36 LC
Pipidae Xenopus tropicalis B LC
Ranidae Amniana galamensis O 3 16 LC
Dicroglossidae Hoplobratrachus occipitalis O 0 32 LC
Ptychadenidae Ptychadena bibroni O 16 1 LC
Ptychadenidae Ptychadena oxyrhynchus O 30 56 LC
Ptychadenidae Ptychadena pumilio O 6 43 LC
Ptychadenidae Ptychadena sp. O 24 46 LC
Ptychadenidae Ptychadena tellinii O 5 7 LC
Microhylidae Phrynomantis microps B LC
TOTAL 145 658
Reptilia
Pelomedusidae Pelusios castaneus O 32 18 LC
Pelomedusidae Pelomedusa subrufa olivacea O 23 16 LC
Testidinidae Kinixys nogueyi O 9 11 VU
Tryonichidae Cyclanorbis senegalensis O 2 48 VU
Tryonichidae Trionyx triunguis O 21 0 VU
Crocodylidae Crocodylus suchus O 6 2 VU
Crocodylidae Osteolaemus tetraspis E VU
Leptotyphlopidae Leptotyphlops bicolor B LC
Typhlopidae Typhlops punctatus B LC
Pythonidae Python regius O 3 0 LC
Pythonidae Python sebae O 2 0 LC
Atractaspididae Atractaspis aterima B LC
Atractaspididae Atractaspis dahomeyensis B LC
Atractaspididae Atractaspis irregularis O 2 0 LC
Colubridae Afronatrix anoscopus B LC
Colubridae Amblyodipsas unicolor B LC
Colubridae Chamaelycus fasciatus B LC
Colubridae Crotaphopeltis hotamboeia O 3 2 LC
Colubridae Dasypeltis fasciata O 0 1 LC
Diversity 2022,14, 964 7 of 15
Table 1. Cont.
Family Species Type of
Record
Observed
Number in Dry
Season
Observed
Number in Wet
Season
IUCN
(2022)
Colubridae Dasypeltis gansi O 2 0 LC
Colubridae Grayia smithii O 1 0 LC
Colubridae Lamprophis fuliginosus O 3 0 LC
Colubridae Lamprophis lineatus O 6 0 LC
Colubridae Lycophidion irroratum O 0 1 LC
Colubridae Lycophidion semicinctum B LC
Colubridae Mehelya crossii B LC
Colubridae Mehelya poensis B LC
Colubridae Meizodon coronatus B LC
Colubridae Meizodon regularis B LC
Colubridae Philothamnus irregularis O 2 0 LC
Colubridae Philothamnus semivariegatus O 2 0 LC
Colubridae Prosymna meleagris B LC
Colubridae Psammophis elegans O 2 1 LC
Colubridae Psammophis phillipsi B LC
Colubridae Psammophis sibilans B LC
Colubridae Rhamnophis aethiopissa B LC
Colubridae Rhamphiophis oxyrhynchus O 3 0 LC
Colubridae Scaphiophis albopunctatus B LC
Colubridae Telescopus variegatus B LC
Colubridae Toxicodryas blandingii B LC
Colubridae Toxicodryas pulverulenta B LC
Elapidae Dendroaspis viridis O 2 1 LC
Elapidae Elapsoidea semiannulata B LC
Elapidae Naja melanoleuca O 2 3 LC
Elapidae Naja nigricollis O 0 1 LC
Viperidae Bitis arietans O 2 3 LC
Viperidae Causus maculatus O 5 2 LC
Viperidae Echis ocellatus O 6 2 LC
Agamidae Agama agama O 44 36 LC
Agamidae Agama parafricana B LC
Agamidae Agama sankaranica O 3 0 LC
Chamaeleonidae Chamaeleo gracilis B LC
Chamaeleonidae Chamaeleo senegalensis O 2 2 LC
Gekkonidae Cnemaspis spinicollis B LC
Gekkonidae Hemidactylus albituberculatus O 1 0 LC
Gekkonidae Hemidactylus angulatus O 10 7 LC
Gekkonidae Hemidactylus mabouia O 9 10 LC
Gekkonidae Hemidactylus matschiei O 4 1 LC
Gekkonidae Hemitheconyx caudicinctus O 3 1 LC
Gekkonidae Lygodactylus conraui O 2 0 LC
Lacertidae Heliobolus nitidus O 3 0 LC
Scincidae Mochlus guineensis O 12 0 LC
Scincidae Panaspis togoensis O 5 3 LC
Scincidae Trachylepis affinis O 18 8 LC
Scincidae Trachylepis maculilabris O 7 4 LC
Scincidae Trachylepis perrotetii O 8 15 LC
Scincidae Trachylepis quinquetaeniata O 20 14 LC
Varanidae Varanus exanthematicus O 2 1 LC
Varanidae Varanus niloticus O 6 3 LC
Varanidae Varanus ornatus B LC
TOTAL 300 217
Legend: IUCN (2022): LC: Least Concern, VU: Vulnerable. Type of record: O = observed; B = reported in the
literature but not directly observed in the wild; E = species reported by village survey.
Diversity 2022,14, 964 8 of 15
Diversity 2022, 14, x FOR PEER REVIEW 8 of 15
Figure 2. Some of the amphibian species recorded in the present study.
Figure 3. Saturation curves and diversity profiles (with 95% confidence intervals) for amphibians
and reptiles during the dry and wet seasons. Saturation curves are (a) for amphibians and (c) for
reptiles. Diversity profiles are (b) for amphibians and (d) for reptiles.
Figure 3.
Saturation curves and diversity profiles (with 95% confidence intervals) for amphibians
and reptiles during the dry and wet seasons. Saturation curves are (
a
) for amphibians and (
c
) for
reptiles. Diversity profiles are (b) for amphibians and (d) for reptiles.
Table 2.
Diversity indices for amphibian and reptile communities at the study area during the wet
and the dry season.
Dry Wet Dry Wet
Amphibia Reptilia
Species richness 10 23 41 28
Number of individuals 145 658 323 194
Dominance 0.1339 0.08656 0.05867 0.08864
Shannon 2.184 2.75 3.199 2.749
Evenness 0.7398 0.6256 0.5978 0.5578
Chao-1 12 26 41 33
All amphibian species were non-threatened by IUCN (2022) and not protected in Togo
(Table 1).
Diversity 2022,14, 964 9 of 15
3.2. Reptiles
The checklist of the reptiles and their conservation status is given in Table 1. Overall,
we observed 517 individuals belonging to 44 species (Figure 4): 300 individuals belonging
to 41 species during the dry season and 217 individuals belonging to 28 species by wet
season (Table 1). In addition, 25 species were not directly observed during our field surveys
but are cited in the available literature (Table 1). The sightings of a gekkonid species
(Hemidactylus matschiei) represented a considerable extension to its known distribution
within Togo (Figure 5). Saturation curves revealed that the plateau phase was reached
in both seasons (Figure 3c), with 41 species predicted to occur in the area during the
dry season and 33 during the wet season according to Chao-1 index. In other words,
Chao-1 estimates revealed that our sampling was more efficient during the dry season.
Diversity indices revealed a much higher diversity and evenness during the dry season
(Table 2), and diversity profile curves showed that the two seasonal samples were similar
(Figure 3d). There were five singletons (four snakes: Dasypeltis fasciata,Grayia smithii,
Lycophidion irroratum,Naja nigricollis; one lizard: Hemidactylus albituberculatus) and seven
doubletons (the snakes Dasypeltis gansi,Atractaspis irregularis,Hapsidophrys smaragdinus,
Philothamnus irregularis,Philothamnus semivariegatus,Python sebae, and the lizard Lygodactylus
conraui), thus showing that the distribution of local rarity was much different from that
of sympatric amphibians. The most common species were two lizards (Agama agama and
Trachylepis quinquetaeniata) and three turtles (Cyclanorbis senegalensis,Pelusios castaneus and
Pelomedusa subrufa).
Diversity 2022, 14, x FOR PEER REVIEW 9 of 15
3.2. Reptiles
The checklist of the reptiles and their conservation status is given in Table 1. Overall,
we observed 517 individuals belonging to 44 species (Figure 4): 300 individuals belonging
to 41 species during the dry season and 217 individuals belonging to 28 species by wet
season (Table 1). In addition, 25 species were not directly observed during our field sur-
veys but are cited in the available literature (Table 1). The sightings of a gekkonid species
(Hemidactylus matschiei) represented a considerable extension to its known distribution
within Togo (Figure 5). Saturation curves revealed that the plateau phase was reached in
both seasons (Figure 3c), with 41 species predicted to occur in the area during the dry
season and 33 during the wet season according to Chao-1 index. In other words, Chao-1
estimates revealed that our sampling was more efficient during the dry season. Diversity
indices revealed a much higher diversity and evenness during the dry season (Table 2),
and diversity profile curves showed that the two seasonal samples were similar (Figure
3d). There were five singletons (four snakes: Dasypeltis fasciata, Grayia smithii, Lycophidion
irroratum, Naja nigricollis; one lizard: Hemidactylus albituberculatus) and seven doubletons
(the snakes Dasypeltis gansi, Atractaspis irregularis, Hapsidophrys smaragdinus, Philothamnus
irregularis, Philothamnus semivariegatus, Python sebae, and the lizard Lygodactylus conraui),
thus showing that the distribution of local rarity was much different from that of sympat-
ric amphibians. The most common species were two lizards (Agama agama and Trachylepis
quinquetaeniata) and three turtles (Cyclanorbis senegalensis, Pelusios castaneus and Pelome-
dusa subrufa).
In conservation terms, most reptile species were non-threatened by IUCN (2022) but
five are listed as VU in the IUCN Red List (Table 1).
Figure 4. Some of the reptile species recorded in the present study.
Figure 4. Some of the reptile species recorded in the present study.
Diversity 2022,14, 964 10 of 15
Diversity 2022, 14, x FOR PEER REVIEW 10 of 15
Figure 5. Hemidactylus matschiei, a rare gekko species that is known to occur only in Togo and Nige-
ria. Our records considerably extend their known distribution within Togo.
3.3. Comparisons between Amphibians and Reptiles
Comparing the rank–abundance diagrams, we can notice remarkable trajectory dif-
ferences between amphibians and reptiles and between seasons (Figure 6). In amphibians,
the curves were very different between seasons with a high dominance of the two most
abundant taxa in the wet season, otherwise with a relatively smooth evenness among all
other species (Figure 6A). On the other hand, in reptiles, the curves were similar between
seasons, although with constantly higher abundances for all species sharing a same rank
during the dry season (Figure 6B). Interestingly, the seasonal patterns were opposite be-
tween taxa: the dry season curve was systematically higher than the wet season curve for
a same given rank in the reptiles but was systematically lower for a same rank in the am-
phibians (Figure 3).
Concerning the diversity indices:
(i) Dominance index was significantly higher in amphibians during the dry season than
in all other pairwise comparisons, i.e., wet season amphibians and both seasons’ rep-
tiles (ANOSIM: mean rank within seasons types = 102.4; mean rank between taxa =
1361.4; R = 0.311, P = 0.0012);
(ii) Shannon’s index was significantly lower in dry season amphibians and significantly
higher in wet season reptiles (ANOSIM: mean rank within seasons types = 116.3;
mean rank between taxa = 118.3; R = 0.246, P = 0.0023);
(iii) Evenness index was significantly lower in reptiles than in amphibians (ANOSIM:
mean rank between taxa = 99.4; R = 0.221, P = 0.023).
The mean number of individuals was significantly different between amphibians and
reptiles and between seasons (one-way ANOVA: F3,138 = 15.24, P = 0.0001), and Tukey HSD
post hoc tests showed that the number of individuals was significantly higher in amphib-
ians during the wet season compared to dry season amphibians or reptiles during both
seasons.
Figure 5.
Hemidactylus matschiei, a rare gekko species that is known to occur only in Togo and Nigeria.
Our records considerably extend their known distribution within Togo.
In conservation terms, most reptile species were non-threatened by IUCN (2022) but
five are listed as VU in the IUCN Red List (Table 1).
3.3. Comparisons between Amphibians and Reptiles
Comparing the rank–abundance diagrams, we can notice remarkable trajectory differ-
ences between amphibians and reptiles and between seasons (Figure 6). In amphibians,
the curves were very different between seasons with a high dominance of the two most
abundant taxa in the wet season, otherwise with a relatively smooth evenness among all
other species (Figure 6A). On the other hand, in reptiles, the curves were similar between
seasons, although with constantly higher abundances for all species sharing a same rank
during the dry season (Figure 6B). Interestingly, the seasonal patterns were opposite be-
tween taxa: the dry season curve was systematically higher than the wet season curve
for a same given rank in the reptiles but was systematically lower for a same rank in the
amphibians (Figure 3).
Concerning the diversity indices:
(i)
Dominance index was significantly higher in amphibians during the dry season than
in all other pairwise comparisons, i.e., wet season amphibians and both seasons’
reptiles (ANOSIM: mean rank within seasons types = 102.4; mean rank between taxa
= 1361.4; R = 0.311, P = 0.0012);
(ii)
Shannon’s index was significantly lower in dry season amphibians and significantly
higher in wet season reptiles (ANOSIM: mean rank within seasons types = 116.3;
mean rank between taxa = 118.3; R = 0.246, P = 0.0023);
(iii)
Evenness index was significantly lower in reptiles than in amphibians (ANOSIM:
mean rank between taxa = 99.4; R = 0.221, P = 0.023).
The mean number of individuals was significantly different between amphibians and
reptiles and between seasons (one-way ANOVA: F
3,138
= 15.24, P = 0.0001), and Tukey
HSD post hoc tests showed that the number of individuals was significantly higher in
amphibians during the wet season compared to dry season amphibians or reptiles during
both seasons.
Diversity 2022,14, 964 11 of 15
Diversity 2022, 14, x FOR PEER REVIEW 11 of 15
Figure 6. Rank–abundance diagram for amphibians (A) and reptiles (B) at the study area in Togo
during the dry and wet seasons.
4. Discussion
4.1. General Considerations
If we consider the taxa whose presence is likely, the Togolese herpetological fauna
consists of 60 species of amphibians [9] and 160 species of reptiles [6–8]. This study reveals
that about 50% of Togolese amphibians do occur at the study area, whereas the fraction is
much lower for the reptiles. Considering that (i) Guinea savannah is the dominant vege-
tation type in both the study area and Togo in general, and that (ii) this vegetation type is
quite homogeneous all throughout the Dahomey Gap in terms of ecological characteris-
tics, the percentages of locally found species appear to be relatively low. We suggest that
this result was due to the strong anthropization of the study area, given that our analytical
approach (saturation curves and Chao-1 estimates) confirmed that we detected the great
majority of the species potentially occurring at the study area from a statistical point of
view.
Overall, the encountered amphibian species formed communities that are typical of
West African savannahs [26]. In Togo, they have a wide distribution over all the different
ecological zones of the country [9]. These are often arboreal (Hyperolidae) or terrestrial-
aquatic (Ptychadenidae) species. Most of the species belonging to the Hyperolidae family
Figure 6.
Rank–abundance diagram for amphibians (
A
) and reptiles (
B
) at the study area in Togo
during the dry and wet seasons.
4. Discussion
4.1. General Considerations
If we consider the taxa whose presence is likely, the Togolese herpetological fauna con-
sists of 60 species of amphibians [
9
] and 160 species of reptiles [
6
–
8
]. This study reveals that
about 50% of Togolese amphibians do occur at the study area, whereas the fraction is much
lower for the reptiles. Considering that (i) Guinea savannah is the dominant vegetation
type in both the study area and Togo in general, and that (ii) this vegetation type is quite
homogeneous all throughout the Dahomey Gap in terms of ecological characteristics, the
percentages of locally found species appear to be relatively low. We suggest that this result
was due to the strong anthropization of the study area, given that our analytical approach
(saturation curves and Chao-1 estimates) confirmed that we detected the great majority of
the species potentially occurring at the study area from a statistical point of view.
Overall, the encountered amphibian species formed communities that are typical of
West African savannahs [
26
]. In Togo, they have a wide distribution over all the different
ecological zones of the country [
9
]. These are often arboreal (Hyperolidae) or terrestrial-
aquatic (Ptychadenidae) species. Most of the species belonging to the Hyperolidae family
were active only in the wet season, whereas the species of the Ptychadenidae family showed
Diversity 2022,14, 964 12 of 15
a higher capacity to adapt to less humid conditions and so they were also frequently
observed during the dry season.
In general, the species of reptiles occurring at the study area were typically West
African savannah species [
7
,
8
,
16
–
18
]. For instance, the community composition of our
turtle assemblage was very similar to that observed in the Dahomey Gap savannahs in
both Ghana [
3
] and Benin [
2
]. However, in our study area, we found at a single site
(Nagbeto dam) Trionyx triunguis that is usually very rare in savannah water bodies [
3
]. We
suppose that the presence of gallery forests along the river banks may explain the presence
of this otherwise rare turtle at the study area [
7
]. Concerning lizards, the great majority
of the species recorded in the present study were also recorded in previous studies on
the lizard communities of Togo savannahs [
4
]. As the study area was at least partially
anthropized by agricultural activities and human settlements, the destruction of habitats
has certainly contributed to the proliferation of generalist savannah species, although in
the best-preserved site places (with remnants of a forest ecosystem, notably at Kpetuhoe)
forest taxa were also observed.
Ecologically, among the species of reptiles listed, we found a dominance of terrestrial
species, with aquatic species that were locally abundant (Pelusios castaneus, Pelomedusa
subrufa olivacea, Cyclanorbis senegalensis) and arboreal species that occurred especially in
the gallery forests growing along the banks of the Mono and Ra rivers (Dendroaspis viridis,
Philothamnus irregularis and Philothamnus semivariegatus, for example). Although these latter
were seen more rarely than terrestrial and aquatic species, it should be noted that this is
likely an outcome of their highly elusive habits while hiding on trees.
Although the study area did not contain any endemic species, during this survey, we
observed a very rare species, Hemidactylus matschiei (at Gbanvikpli and at Amoukpli). This
gekko species is known to occur only in Togo and Nigeria, exclusively in the few sites
where the savannah zone is naturally associated with the forest zone. It was described
in 1901 [
27
], and a specimen of the species was recently collected by Trape from the
type locality (Yégué) [
18
]. This new collection makes it possible to enhance the known
distribution area for this species.
4.2. Diversity Metrics
Consistently with our a priori hypotheses, we observed that the diversity metrics were
remarkably different between amphibians and reptiles, and that there were clear seasonal
directions of these differences. First, the number of sympatric species was much higher
in reptiles. As said above, this could not be surprising given that the species richness of
reptiles is much higher than that of amphibians in Togo in general (see references given
above).
Second, the mean number of individuals per species was lower in reptiles than in
amphibians, thus mirroring our a priori hypothesis (a) in the Introduction. More specifically,
(i) the number of amphibian individuals peaked strongly during the wet season, thus by far
outnumbering those of reptiles, and (ii) the number of individuals of the larger predators
(Python sebae, Bitis arietans, other large snakes) was always low. Pattern (i) had a clear
seasonal effect of the abundance of water and available food resources for amphibians
during the wet months, and pattern (ii) shows that the number of large predators is
relatively lower in the Dahomey Gap savannah habitats compared to smaller predators.
It should be remarked that pattern (i) confirms our a priori hypothesis (b) that am-
phibian populations should be more negatively affected than reptiles by the dry season
climatic conditions. In fact, we recorded a total of 513 more amphibian individuals in the
wet season than in the dry season. As predicted, the inter-seasonal differences in amphibian
population size also affected the diversity metrics, with the consequent increase in the
dominance and decrease in the evenness of the seasonal assemblages.
As predicted in our hypotheses (b) and (c), the same inter-seasonal differences were
less evident in reptiles: the difference between the two seasons was only 83 individuals
Diversity 2022,14, 964 13 of 15
(in favor of the dry season), and the values of dominance and evenness were much less
different between the seasons than in amphibians.
Interestingly, the distribution of local rarity was intriguingly different: there were
several singletons and doubletons in reptiles but very few in amphibians. In this case,
the relative species richness of the two groups cannot explain this pattern: indeed, 0% of
amphibian species were singletons and just 3.7% were doubletons. Conversely, 11.4% of
reptiles were singletons, and 13.6% were doubletons. These differences were so strong
that could not be due to chance. We suppose that (i) many reptile species are indeed
rarer at the study area (also possibly an effect of a resource partitioning patterns for food
or space; see [
28
,
29
]), and (ii) they are more elusive than amphibians, especially during
the wet season. Overall, we obtained indirect evidence at least for pattern (ii): indeed,
some singletons/doubletons are usually abundant species with a niche that is not shared
by any potential competitor at the study area (for instance, the strictly aquatic fish- and
frog-eater Grayia smithii, [
30
], or the frequently snake-eater Naja nigricollis [
31
–
33
] or the
gigantic Python sebae [
14
,
34
]), thus making us theorize that in their apparent rarity there
are no competitive mechanisms with other sympatric species. However, if we observe
more carefully within seasons (in savannah habitat, the available resource is certainly
more limited in the dry than in the wet season), we can notice some aspects that suggest
the occurrence of resource partitioning patterns in our assemblage of reptiles: (i) within
the genera Agama, Hemidactylus and Trachylepis there were high abundance differences
among species by both dry and wet season; (ii) the tryonichid turtles Cyclanorbis senegalensis
and Trionyx triunguis, occurring syntopically in the Nagbeto dam, were found in alternate
seasons in a clearly statistically significant way. Thus, although more research is needed,
we suppose that both elusiveness and synecology may explain the observed reptile patterns
at the study area.
4.3. Conservation Considerations
With the exception of a few turtles and crocodiles, all the other species of both classes
encountered on the study area are not considered priority taxa for conservation. Indeed,
only Kinixys nogueyi (VU), Cyclanorbis senegalensis (VU), Trionyx triunguis (VU), Osteolaemus
tetraspis (VU) and Crocodylus suchus (VU) are listed on the IUCN (2022) Red List. How-
ever, since (i) live specimens of some of the reptile species are exploited in international
trade (especially pythons, monitor lizards and freshwater turtles) and (ii) monitor lizards,
turtles and crocodiles are also hunted for local consumption, their populations should be
monitored regularly in order to prevent any unnoticed decline.
Author Contributions:
Conceptualization, G.H.S., G.K.K. and L.L.; methodology, G.H.S.; software,
L.L.; validation, L.L. and D.D.; formal analysis, L.L. and D.D.; investigation, J.K.D. and G.H.S.;
resources, G.K.K.; data curation, J.K.D. and D.D.; writing—original draft preparation, G.H.S. and
L.L.; writing—review and editing, all authors. All authors have read and agreed to the published
version of the manuscript.
Funding: This research was funded by Biotope and DEP Sarl.
Institutional Review Board Statement:
The study was conducted in accordance with the Declaration
of Helsinki, and approved by the Institutional Review Board (or Ethics Committee) of both the
University of Loméand IDECC.
Data Availability Statement:
All the data collected in the study are provided in the published paper.
Acknowledgments:
We sincerely thank Biotope and DEP Sarl for providing funding through contract
for the herpetofauna assessment in the framework of the for the Biodiversity component of the
environmental and social impact study of the Tététou dam project. We are indebted with three
anonymous referees for their helpful comments on the submitted draft.
Conflicts of Interest: The authors declare no conflict of interest.
Diversity 2022,14, 964 14 of 15
References
1.
Demenou, B.B.; Doucet, J.L.; Hardy, O.J. History of the fragmentation of the African rain forest in the Dahomey Gap: Insight from
the demographic history of Terminalia ystem. Heredity 2018,120, 547–561. [CrossRef] [PubMed]
2.
Luiselli, L.; Akani, G.C.; Ajong, S.N.; George, A.; Di Vittorio, M.; Eniang, E.A.; Dendi, D.; Hema, E.M.; Petrozzi, F.; Fa, J.E.
Predicting the structure of turtle assemblages along a megatransect in West Africa. Biol. J. Linn. Soc.
2020
,130, 296–309. [CrossRef]
3.
Gbewaa, S.B.; Oppong, S.K.; Horne, B.D.; Tehoda, P.; Petrozzi, F.; Dendi, D.; Akani, G.C.; Vittorio, M.D.; Ajong, S.N.; Pacini, N.;
et al. Community characteristics of sympatric freshwater turtles from savannah waterbodies in Ghana. Wetlands
2021
,41, 61.
[CrossRef]
4.
Luiselli, L.; Dendi, D.; Petrozzi, F.; Segniagbeto, G.H. Lizard community structure and spatial resource use along a forest-
savannah-urban habitat gradient in the Dahomey Gap (West Africa). Urban Ecosyst. 2022,25, 1015–1026. [CrossRef]
5.
Segniagbeto, H. Herpétofaune du Togo: Taxinomie, Biogéographie; Thèse de Doctorat, University of Lomé: Lomé, Togo; MNHN: Paris,
France, 2009; p. 456.
6.
Segniagbeto, G.H.; Trape, J.-F.; Afiademanyo, K.; Roedel, M.-O.; Ohler, A.; Dubois, A.; David, P.; Meirte, D.; Glitho, A.; Petrozzi,
F.; et al. Checklist of the lizards of Togo, (West Africa), with comments on systematics, distribution, ecology, and conservation.
Zoosystema 2015,37, 381–402. [CrossRef]
7.
Segniagbeto, G.H.; Bour, R.; Ohler, A.; Dubois, A.; Roedel, M.-O.; Trape, J.-F.; Fretey, J.; Petrozzi, F.; Aïdam, A.; Luiselli, L. Turtles
and tortoises of Togo: Historical data, distribution, ecology and conservation. Chel. Cons. Biol. 2014,13, 152–165. [CrossRef]
8.
Segniagbeto, G.H.; Trape, J.-F.; David, P.; Ohler, A.-M.; Dubois, A.; Glitho, I.A. The snake fauna of Togo: Systematics, distribution,
and biogeography, with remarks on selected taxonomic problems. Zoosystema 2011,33, 325–360. [CrossRef]
9.
Segniagbeto, G.H.; Bowessidjaou, J.E.; Dubois, A.; Ohler, A. Les Amphibiens du Togo: État actuel des connaissances. Alytes
2007
,
24, 72–90.
10. IUCN. The Red List of Threatened Species. 2022. Available online: www.iucnredlist.org (accessed on 29 September 2022).
11.
Nelson, D.M.; Verschuren, D.; Urban, M.A.; Hu, F.S. Long-term variability and rainfall control of savanna fire regimes in equatorial
East Africa. Glob. Chang. Biol. 2012,18, 3160–3170. [CrossRef]
12.
Ogutu, J.O.; Piepho, H.P.; Dublin, H.T.; Bhola, N.; Reid, R.S. Rainfall influences on ungulate population abundance in the
Mara-Serengeti ecosystem. J. Anim. Ecol. 2008,77, 814–829. [CrossRef]
13. Owusu, K. Rainfall changes in the savannah zone of northern Ghana 1961–2010. Weather 2018,73, 46–50. [CrossRef]
14.
Luiselli, L.; Angelici, F.M.; Akani, G.C. Food habits of Python sebae in suburban and natural habitats. Afr. J. Ecol.
2001
,39, 116–118.
15.
Crump, M.L.; Scott, N.J. Visual encounter survey. In Measuring and Monitoring Biological Diversity, Standard Methods for Amphibians;
Heyer, W.R., Donnelly, M.A., McDiarmid, R.W., Donnelly, M., Heyek, L.C., Foster, M.S., Eds.; Smithsonian Institution Press:
Washington, DC, USA, 1994; pp. 84–91.
16.
Chippaux, J.-P. Les Serpents D’afrique Occidentale et Centrale; Collection Faune et Flore Tropicales; IRD Éditions: Paris, France, 2006;
p. 311.
17. Trape, J.-F.; Mané, Y. Guide Des Serpents D’afrique Occidentale (Savane et Désert); IRD Éditions: Paris, France, 2006; p. 226.
18.
Trape, J.-F.; Trape, S.; Chirio, L. Lézards, Crocodiles et Tortues D’afrique Occidentale et Du Sahara; IRD Editions: Marseille, France,
2012; p. 503.
19.
Channing, A.; Rödel, M.O. Field Guide to the Frogs and Other Amphibians of Africa; Struik Nature: Cape Town, South Africa, 2019;
p. 408.
20.
Frost, D. Amphibian Species of the World: An Online Reference, Version 6.1; American Museum of Natural History: New York, NY,
USA, 2021; Available online: https://amphibiansoftheworld.amnh.org/index.php (accessed on 1 October 2022). [CrossRef]
21. Magurran, A.E. Ecological Diversity and Its Measurement; Princeton University Press: Princeton, NJ, USA, 1988.
22. Hammer, O. PAST—Paleontological Statistics, version 2.17; Reference Manual 1999–2012; PAST: Oslo, Norway, 2012.
23. Krebs, C.J. Ecological Methodology; Harper & Row: New York, NY, USA, 1989.
24. Tóthmérész, B. Comparison of different methods for diversity ordering. J. Veg. Sci. 1995,6, 283–290. [CrossRef]
25.
Oksanen, J.; Guillaume Blanchet, F.; Kindt, R.; Legendre, P.; Minchin, P.R.; O’Hara, R.B.; Simpson, G.L.; Solymos, P.; Stevens,
M.H.H.; Wagner, H. Vegan: Community Ecology Package. 2010. Available online: http://vegan.r-forge.r-project.org/ (accessed
on 13 August 2022).
26.
Rödel, M.-O. Herpetofauna of West Africa. In Amphibians of the West African Savana; Chimaira: Frankfurt am Main, France, 2000;
Volume 1, p. 335.
27. Tornier, G. Die Crocodile, Schildkröten und Eidechsen in Togo. Arch. Naturgeschichte 1901,1901, 65–88.
28.
Luiselli, L. Resource partitioning and interspecific competition in snakes: The search for general geographical and guild patterns.
Oikos 2006,114, 193–211. [CrossRef]
29.
Luiselli, L. Do lizard communities partition the trophic niche? A worldwide meta-analysis using null models. Oikos
2008
,117,
321–330. [CrossRef]
30.
Akani, G.C.; Luiselli, L. Ecological studies on a population of the water snake Grayia smythii in a rainforest swamp of the Niger
Delta, Nigeria. Contrib. Zool. 2001,70, 139–146. [CrossRef]
31.
Luiselli, L.; Angelici, F.M. Ecological relationships in two Afrotropical cobra species (Naja melanoleuca and Naja nigricollis). Can. J.
Zool. 2000,78, 191–198. [CrossRef]
Diversity 2022,14, 964 15 of 15
32.
Luiselli, L.; Angelici, F.M.; Akani, G.C. Comparative feeding strategies and dietary plasticity of the sympatric cobras Naja
melanoleuca and Naja nigricollis in three diverging Afrotropical habitats. Can. J. Zool. 2002,80, 55–63. [CrossRef]
33.
Maritz, B.; Alexander, G.J.; Maritz, R.A. The underappreciated extent of cannibalism and ophiophagy in African cobras. Ecology
2019,100, 1–4. [CrossRef]
34.
Luiselli, L.; Akani, G.C.; Capizzi, D. Food resource partitioning of a community of snakes in a swamp rainforest of south-eastern
Nigeria. J. Zool. Lond. 1998,246, 125–133. [CrossRef]
