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The amphibians and reptiles of Nouabale-Ndoki National Park, Republic of Congo (Brazzaville)

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We present an annotated list of 20 amphibian and 4 reptile species collected along the southern edge of Nouabale-Ndoki National Park in the Republic of Congo, which comprises lowland forests that are part of the Congo River drainage basin. This study has resulted in the first definitive records of the frogs Aubria masako, Amietophrynus regularis, Cryptothylax greshoffii, Hyperolius balfouri, H. brachiofa- sciatus, Leptopelis brevirostris, and L. calcaratus meridionalis from the Republic of Congo (Brazzaville). Comparing four sites subjected to different degrees of human disturbance, we note differences in her - petofaunal composition among these sites, which we attribute to difference in tolerance of human acti - vity, opportunistic colonisation by non-native species, and, in some cases, a preference for proximity to human habitations. We compare the results of our study to other herpetofaunal surveys of Central and West Africa in order to gain insight into which faunae are most similar to that of Nouabale-Ndoki Na - tional Park.
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
Rheinbach, 20 August 2007 ISSN 0036-3375149-164
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SALAMANDRA
http://www.salamandra-journal.com

e amphibians and reptiles of Nouabale-Ndoki National
Park, Republic of Congo (Brazzaville)

Abstract. 


Aubria masako
Amietophrynus regularisCryptothylax greshoffiiHyperolius balfouriH. brachiofa-
sciatus
Leptopelis brevirostrisL. calcaratus meridionalis







Résumé. 



Aubria masakoAmietophrynus regularisCryptothylax greshof-
fii
Hyperolius balfouri,H. brachiofasciatus Leptopelis brevirostris,  L. calcaratus meridionalis







Introduction
   







  

    
 










     

     

       

      
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





       
     

    
   
     

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     
   
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






     
      
  



    




     


Materials and methods







      
     
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












   


Chamaeleo
VaranusKi-
nixysPython sebae





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152



Crocodylus niloticusC. cataphractus
Osteolaemus tetraspisVaranus niloticus
 Python sebae   




Results



Arthroleptis
poecilonotus


     Arthroleptis
poecilonotus




   

Amietophrynus
camerunensis

     
       

      


    
      
    
     




AmietophrynusA.
togoensis    A. cristiglans



      
Amietophrynus    
BufoB. ca
-
merunensis
B. funereusB. gracilipesB. ma-
culatusB. regularis
Bufo
     B. funereus
B. gracilipes 

B. gracilipes

B. funereus

    


     



Amietophrynus
funereus  


      
     



Amietophrynus
gracilipes 
    


    
      


   


Amietophrynus maculatus 
    
   

153


    
Arthroleptis poecilonotus
Amietophrynus camerunensis
Amietophrynus funereus
Amietophrynus gracilipes
Amietophrynus maculatus
Amietophrynus regularis
Afrixalus quadrivittatus
Cryptothylax greshoffii
Hyperolius balfouri
Hyperolius brachiofasciatus
Hyperolius cinnamomeoventris
Leptopelis
aubryi
Leptopelis brevirostris
Leptopelis calcaratus meridionalis
Leptopelis notatus
Phrynobatrachus hylaios
Amnirana albolabris
Aubria masako
Hoplobatrachus occipitalis
Ptychadena perreti
Python sebae
Aparallactus modestus
Grayia smithii
Lamprophis olivaceous
Philothamnus carinatus
elotornis kirtlandii
Boulengerina annulata
Naja melanoleuca
Feylinia currori
Trachylepis maculilabris
Hemidactylus mabouia
Kinixys erosa
Osteolaemus tetraspis
Crocodylus cataphractus



154





Arthroleptis poecilonotus
Amietophrynus camerunensis

Amietophrynus funereus
Amietophrynus gracilipes
Amietophrynus maculatus
Amietophrynus regularis
Afrixalus quadrivittatus
Cryptothylax greshoffii
Hyperolius balfouri
Hyperolius brachiofasciatus
Hyperolius cinnamomeoventris
Leptopelis aubryi
Leptopelis brevirostris
Leptopelis calcaratus meridionalis
Leptopelis notatus
Phrynobatrachus hylaios
Amnirana albolabris
Aubria masako
Hoplobatrachus occipitalis
Ptychadena perreti
Python sebae
Aparallactus modestus
Grayia smithii
Lamprophis olivaceous
Philothamnus carinatus
elotornis kirtlandii
Boulengerina annulata
Naja melanoleuca
Feylinia currori
Trachylepis maculilabris
Hemidactylus mabouia
Kinixys erosa
Osteolaemus tetraspis
Crocodylus cataphractus




155


    



A. regularis
A. maculatus


Amietophrynus regularis
    



  
   Amietophrynus re-
gularis 

. 
   
A. regularis  A. camerunensis

A. regu
-
laris



    
 


Afrixalus quadrivittatus
 
   
     
        
     
   
      Afri-
xalus fulvovittatus     


A. quadrivittatus

 A. fulvovittatus   
A. quadrivittatus

Cryptothylax greshoffii  



  
      





Hyperolius balfouri   
   

   









     


  




    

    
      


     



Hyperolius
brachiofasciatus  . 
     


 H. brachiofasciatus   
156




     

  H. brachiofasciatus  


     


      

 

Hyperolius  cinnamomeoventris 


       
   
Hyperolius
H. cinna-
momeoventris




  Hyperlious schoutedeni  




Leptopelis
aubryi 




Leptopelis brevirostris
     

Leptopelis brevirostris





Leptopelis calcaratus meridionalis 

      
       

L.
c. meridionalis

Leptopelis notatus
   




Phrynobatrachus
hylaios
    
  
      
     




     
    

       


Amnirana albolabris  



 
    

      
   

Aubria masako


      
       
A. masa-
ko
157



Aubria subsigillata





A.
subsigillata    
     
A. masako.

A. masako
Aubria masakoA. subsigillata

 
 
A. masako

A. masako


Hoplobatrachus occipitalis

   
 

Hoplobatrachus
occipitalis
   Amietophrynus regularis 
     

Ptychadena
perreti
  

      
      

   




Python sebae    






Aparallactus modestus modestus




A. m.
modestus
     
 A. m. ubangensis





A. m. modestus
      




A. modestus


Grayia smithii

    
       

 
   
Grayia smithii
Grayia     Grayia 
     
      
    
      
Boulengerina annulata

G. smithiiB. annulata




158


Aparallactus modestus mo-
destus Grayia smithii Lamprophis olivaceousPhilothamnus carinatus
Boulengerina annulataFeylinia currori
Lamprophis olivaceus 

      
Lamprophis
L. oliva-
ceus
 L. virgatus   
Lamprophis
     



Philothamnus carinatus




Philothamnus

     Philothamnus
carinatus


  
P. ca
-
159

rinatus

elotornis kirtlandii  
   
      


      
 

       

Aparallactus modestus
Philothamnus carinatus   

elotornis
T. kirtlandii

     



Boulengerina annulata annulata

 




Grayia smithii
Naja melanoleuca
  
    





Feylinia currori
   




   

     Feyli
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nia currori   
      

    

Trachylepis maculilabris   
   




Hemidactylus mabouia

    

      
       



Kinixys erosa 





Osteolaemus tetraspis



Crocodylus cataphractus 
     Osteolae
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mus tetraspis



Discussion




160



      

 

      
     

      
  
       
     






      
  


   
  




      

   
      


      







      



    
      

     
    
   
  

 

     

    


    
     
    
   

 Amietophrynus gracilipes Ho-
plobatrachus occipitalis Amnirana albolab-
risPhrynobatrachus perretiArthroleptis
poecilonotus
Hyperolius cinnamo-
meoventris  Leptopelis calcaratus  





    
 
 Amietophrynus ca-
merunensis . funereus A regularis Afri-
xalus quadrivittatus, Cryptothylax gresshof
-
fii Hyperolius balfouri H. brachiofasciatus
Leptopelis brevirostrisL. notatus, Aubria
masako     
Afrixalus quadrivittatus     
Afrixalus fulvovittatus
    
A. quadrivitta-
tus





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
Amietophrynus
camerunensis
      
  A. regularis  
      
elotornis kirtlandii   
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     
 Lamprophis olivaceus    
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P. carinatus
      
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    
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Osteolaemus tetraspisPython sebae
Feylinia currori  
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

   Hoplo-
batrachus occipitalis   Amnirana
albolabris   Amietophrynus regu-
laris Arthroleptis poecilono-
tus
Amietophrynus gracilipes
Hyperolius cinnanomeoventrisA. fu-
nereusCryptothylax greshoffiiH. bal
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fouri Phrynobatrachus hylaiosH. bra-
chiofasciatusAubria masakoLep-
topelis calcaratus meridionalis
L. calcaratus
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
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     
     


Naja melanoleucaPython sebae
elotornis kirtlandii Grayia smithii Tra-
chylepis maculilabris
Kinixys erosa
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
Aubria masakoAmie-
tophrynus regularis Cryptothylax greshoffii
Hyperolius balfouriH. brachiofasciatus
Leptopelis brevirostris    

L. calcaratus meridi
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onalis
Aparallactus modestus modes-
tus

A. m. modestusA. m. ubangensis
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2
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
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

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 35
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      
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8
       
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 
  
94
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         

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

 
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297


28
Ptychadena


20


Hemidactylus   
Acknowledgements
     



    

    
      

     
  



References

He
-
midactylus
55

       Cryp
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tothylax greshoffii  

37



39
     

163
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
H. muriceus
52
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

4
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
 
  



2

    
  


   Feylinia currori 
35


      
Rhinotyphlops






4
      
   
      

4
       


2 



63
   Leptopelis

     
202










  
     




    


4
    
Aubria
3


Aubria
    
Aubria subsigillata
8

     
  
29







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2
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... This species is relatively widespread occurring in wetlands throughout much of Central, eastern, and western Africa, though it is apparently absent from much of the Congo Basin (IUCN 2009; for exception, see Jackson and Blackburn 2007;). (Fig. 6b) is widespread throughout the coastal region of Central Africa extending in-land to parts of the Congo Basin ( Jackson and Blackburn 2007;). ...
... This species is relatively widespread occurring in wetlands throughout much of Central, eastern, and western Africa, though it is apparently absent from much of the Congo Basin (IUCN 2009; for exception, see Jackson and Blackburn 2007;). (Fig. 6b) is widespread throughout the coastal region of Central Africa extending in-land to parts of the Congo Basin ( Jackson and Blackburn 2007;). All specimens occurred in association with swampy habitat in the wetlands. ...
... All specimens occurred in association with swampy habitat in the wetlands. These specimens agree with the morphological diagnosis provided for the poorly known P. hylaios by Perret (1959) and are similar to those reported from elsewhere in the Republic of Congo (e.g., Jackson and Blackburn 2007). 4723, 4725, 4732-3, 4762, 4776, 4788. ...
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We report here the findings of a faunal survey of amphibians and reptiles included in an environmental impact assessment carried out in a heavily anthropogenically degraded area near the city of Pointe-Noire, Republic of Congo. Specifically, we use these results as an opportunity to investigate the effects of habitat destruction and fragmentation on herpetofauna, an increasingly widespread yet rarely studied phenomenon in sub-Saharan Africa, in one of the most poorly surveyed countries in the world. Among the 37 identified species (12 amphibians and 25 reptiles), we report here for the first time in the Republic of Congo, three species: the frog Hemisus perreti, the skink Afroablepharus tancredi, and the tortoise Kinixys homeana. Résumé.—Nous rapportons dans cet article les résultats d'un inventaire sure les populations d'amphibiens et de reptiles réalisé dans le cadre d'une évaluation de l'impact environnemental sur les populations d'amphibiens et de reptiles dans une région fortement dégradée du fait de l'homme, celle de Pointe Noire en République du Congo. Nous nous sommes en particulier penchés sur les effets de la destruction et du morcellement des habitats sur l'herpétofaune, un phénomène de plus en plus répandu mais jusqu'à maintenant rarement étudié en Afrique sub-saharienne, dans l'une des contrées les moins étudiées de la planète. Parmi les 37 espèces recensées (12 amphibiens et 25 reptiles), nous signalons les premières captures en République du Congo de trois espèces: la grenouille Hemisus perreti, le scinque Afroblepharus tancredi et la tortue Kinixys homeana.
... La République Démocratique Congo (RD Congo) renferme la plus grande richesse spécifique des Amphibiens qui exploitent une large variation de milieux écologiques (17). À part la revue de la littérature postcoloniale sur l'herpétofaune des forêts d'Afrique tropicale et subtropicale par (30), Méta-analyse exploratoire des effets de perturbations anthropiques sur la div... les Amphibiens du bassin du Congo demeurent un groupe parmi les moins étudiés (25). Pourtant, ils constituent des éléments symptomatiques de l'effondrement et des indicateurs de l'intégrité des écosystèmes (48) dont ils évaluent le degré de stress (31). ...
... L'audition des chants, basée sur un temps d'écoute dont la durée est variable selon les espèces, a permis de capturer les espèces vocalement actives pendant la nuit(45). Les méthodes et techniques de captures des Amphibiens varient selon les auteurs(2,3,25,26,46,50). Selon (3), les rendements sont influencés par l'expérience du chercheur et l'effort engagé dans la capture. ...
Article
Ce travail présente les résultats d’une méta-analyse de quatre études menées sur les Amphibiens à Kasugho, Butembo, Mambasa et Kisangani en République Démocratique du Congo. L’objectif principal était de vérifier le lien entre le taux d’anthropisation des habitats et la fréquence des espèces observées afin d’identifier d’éventuelles espèces indicatrices des perturbations anthropiques. L’observation directe a généré 815 Amphibiens capturés dans les habitats anthropisés (étang piscicole, jachère) et non anthropisés (marécage, forêt secondaire, forêt primaire). Sur les 37 espèces identifiées, 2 (Amietophrynus kisoloensis, Hoplobatrachus occipitalis) vivent uniquement dans les habitats anthropisés et 11 (Afrixalus quadrivittatus, Amietophrynus gracilipes, Arthroleptis variabilis, Cardioglossa gracilis, C. leucomystax, Hyperolius viridiflavus, Leptopelis aubryioides, L. ocellatus, Phrynobatrachus auritus, Ptychadena anchietae, P. chrysogaster) préfèrent uniquement les habitats non anthropisés. La plus forte similarité entre les habitats anthropisés et non anthropisés a été observée à Mambasa (étang piscicole, marécage, jachère, forêt secondaire, forêt primaire) et la plus faible entre les habitats à Butembo (marécage, jachère). Un test de Chi-carré souligne un lien entre le statut d’habitat et les abondances d’Amphibiens. Une corrélation linéaire significative confirme qu’il n’y a pas de relation directe entre les fréquences dans les deux statuts d’habitat. La présente étude confirme le potentiel des Amphibiens comme indicateurs de perturbations anthropiques des écosystèmes.
... The arthroleptid treefrog Leptopelis brevirostris (Werner, 1898) was originally described from Victoria, Cameroon, and has since been reported from lowland and submontane (<1 500 m above sea level) forests extending from southern Nigeria through Cameroon, Equatorial Guinea, Gabon, and to northern Republic of the Congo (Amiet and Schiøtz 1974;Amiet 1975;de la Riva 1994;Hofer et al. 1999;Schiøtz 1999;Lasso et al. 2002;Jackson and Blackburn 2007;Frétey et al. 2011;Amiet 2012). This Central African treefrog has a characteristically short and vertically truncated snout, a tooth-like process at the centre of the mandible, and a relatively small tympanum (Amiet 2012). ...
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The Central African treefrog Leptopelis brevirostris has a characteristically short and vertically truncated snout, a tooth-like process at the centre of the mandible, and unlike most species of Leptopelis, eats terrestrial gastropods. Two morphologically similar species (L. crystallinoron and L. brevipes) have been described in sympatry with L. brevirostris, each on the basis of a single female specimen and then provisionally synonymised with L. brevirostris by subsequent authors. Here we re-examine the holotypes of the three species and collect both genetic (mtDNA and 25 nuDNA loci) and morphological data across the range of L. brevirostris and its sister species L. notatus to test the hypothesis that L. brevirostris is comprised of more than one species. We found that the diagnostic characters for L. crystallinoron (lacking a visible tympanum and having larger vomerine teeth in contact) and L. brevipes (distinctive dorsal colouration) are also present in L. brevirostris and L. notatus. Furthermore, these characters vary among individuals that share the same mitochondrial haplotype and that occur within a single locality, including the type locality of L. crystallinoron. Although all samples from the type locality of L. crystallinoron form a distinct mitochondrial lineage relative to L. brevipes and L. brevirostris, our analysis of 25 nuclear loci does not support this relationship and instead suggests that this mitochondrial divergence reflects phylogeographic structure across the range of L. brevirostris, including samples from the type localities of L. crystallinoron and L. brevipes. By contrast, the mitochondrial divergence between L. notatus and L. brevirostris is strongly supported in the nuDNA dataset. Consequently, we recognise both L. brevipes and L. crystallinoron as synonyms of L. brevirostris. Given the extensive variation in the colour pattern, the tympanic membrane, and the size and shape of the vomerine teeth among L. brevirostris collected from one locality, variation in these traits should be interpreted with caution in taxonomic research on Leptopelis.
... assessed the species as Data Deficient in 1996, but re-assessment by the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group in 2013 provisionally assessed the survival status of the species as Endangered. The species has been recorded from at least the following protected areas: Parc National Iles Ehotile, Parc National d'Assagny, Parc National de Banco, and Parc National Tai in Ivory Coast; Kakum National Park in Ghana; Okomu National Park, Taylor Creek Forest Reserve, Edumanon Forest Reserve (Akani et al. 2014a), Upper Orashi Forest Reserve (Akani et al. 2014b), Stubbs Creek Forest Reserve, Taylor Creek Forest Reserve, Nun River Forest Reserve, and Cross River National Park in Nigeria; Dja River Faunal Reserve (LeBreton 1999 ), Korup National Park, Banyang- Mbo Sanctuary, and Nta-Ali Reserve in Cameroon (Lawson 1993); Gamba complex of protected areas in Gabon (Pauwels et al. 2006); and Nouabale-Ndoki National Park in Congo– ROC (Jackson and Blackburn 2007). Conservation Measures Proposed. ...
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The Forest Hinge-back Tortoise, Kinixys erosa (Family Testudinidae), is a forest tortoise with considerable range over the continuous Guinea–Congo rainforest region in West and Central Africa. It is a medium-sized to large tortoise, with a carapace length reaching ca. 400 mm, and males larger than females. Tortoises of the genus Kinixys can close themselves entirely within their shells through a unique posterior carapacial hinge. Kinixys erosa inhabits the lowland evergreen forest, marshy areas, and forest galleries growing along rivers and streams, where it is locally threatened by clearance of forest for cultivation and hunting pressure. It has an omnivorous diet, with mushrooms being predominant. Population sizes are strongly depressed in areas where these tortoises are actively hunted by human populations. The main threats for this species include subsistence hunting by local people in desperately poor economic conditions, agricultural and industrial expansion with deforestation, and trade for the pet industry. There is a strong need for more field research on K. erosa ecology, abundance, and status. There are no known conservation actions for this species; however, there is a need to establish protected areas that include viable populations of these tortoises through their natural range.
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Recent molecular phylogenies of African green snakes suggested the geographically widespread species Philothamnus carinatus includes at least two distinct lineages. We utilised an integrative taxonomic approach with morphological and genetic data to reconcile the taxonomic status of these cryptic lineages, including the recently described taxon P. brunneus from West Africa. We sequenced three mitochondrial (16S, cyt b and ND4) and two nuclear (c-mos and RAG1) genes from several Central African populations of P. carinatus and combined our data with other closely related species to infer a maximum likelihood phylogenetic tree with IQ-TREE. Our results are consistent with previous studies that showed P. cf. carinatus populations from Democratic Republic of the Congo (DRC) represent a cryptic lineage that is distinct from P. carinatus sensu stricto in Cameroon, Central African Republic, Equatorial Guinea (including Bioko Island), Gabon, eastern Nigeria, Republic of the Congo, and extreme western DRC. In our preferred tree, P. brunneus (limited to 16S molecular data) was recovered as a relatively long branch in a moderately supported clade with P. carinatus sensu stricto, whereas P. cf. carinatus populations from northern Angola, most of DRC, and East Africa (Burundi, Kenya, Rwanda, Tanzania and Uganda) were described as a new species, Philothamnus chifunderai n.sp. A possible hybrid population between south-eastern Cameroon and north-western DRC is consistent with an increasing body of evidence suggesting the Ubangi River might represent a hybrid zone area.
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The reed frog genus Hyperolius (Afrobatrachia, Hyperoliidae) is a speciose genus containing over 140 species of mostly small to medium-sized frogs distributed in sub-Saharan Africa. Its high level of colour polymorphism, together with in anurans relatively rare sexual dichromatism, make systematic studies more difficult. As a result, the knowledge of the diversity and taxonomy of this genus is still limited. Hyperolius robustus known only from a handful of localities in rain forests of the central Congo Basin is one of the least known species. Here, we have used molecular methods for the first time to study the phylogenetic position of this taxon, accompanied by an analysis of phenotype based on external (morphometric) and internal (osteological) morphological characters. Our phylogenetic results undoubtedly placed H. robustus out of Hyperolius into a common clade with sympatric Cryptothylax and West African Morerella. To prevent the uncovered paraphyly, we place H. robustus into a new genus, Congolius. The review of all available data suggests that the new genus is endemic to the central Congolian lowland rain forests. The analysis of phenotype underlined morphological similarity of the new genus to some Hyperolius species. This uniformity of body shape (including cranial shape) indicates that the two genera have either retained ancestral morphology or evolved through convergent evolution under similar ecological pressures in the African rain forests.
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The Cameroon Volcanic Line, a mountain chain located between West and Central Africa, is a region of numerous endemic diversifications, including of puddle frogs ( Phrynobatrachus ). This study reviews the phylogeny and taxonomy of puddle frogs of the “Cameroon radiation,” which is a clade containing mainly montane but also at least three lowland species. Molecular data revealed a novel evolutionary lineage from high altitudes in the northern part of the mountains. Puddle frogs from the new, minute-sized (SVL < 20 mm) lineage are identified using molecular, morphological and acoustic data and described as two new species, Phrynobatrachus arcanus sp. nov. (Gotel Mountains, Cameroon–Nigeria) and P. mbabo sp. nov. (Tchabal Mbabo, Cameroon). The tadpole of the first species is also described. Phylogenetic analyses placed the new lineage to the proximity of the recently described lowland small-sized taxa ( P. horsti , P. ruthbeateae ). Based on the inferred phylogeny, we propose five species groups within the Cameroon radiation: P. arcanus , P. chukuchuku , P. ruthbeateae , P. steindachneri , and P. werneri . The taxonomically enigmatic P. hylaios is proposed to be a member of the P. ruthbeateae species group. The basal radiation evolved during the late Miocene with subsequent diversifications occurring during the Pliocene, while closely related terminal taxa originated during the Pleistocene. We recommend that the newly described species are categorized as Critically Endangered due to their limited ranges and because recent surveys did not identify any individuals at the type localities. This further supports the need for conservation interventions in the mountains of Cameroon and Nigeria.
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