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Climate is globally changing. In Europe, studies have highlighted an increasing trend in both the frequency and magnitude of droughts. Abrupt changes in the frequency, location, or intensity of extreme heatwaves and droughts can have direct and severe effects on wild populations. Amphibians are the planet's most threatened group of vertebrates, with over 40% of known species considered in decline. To date, researchers have mainly focused on the influence of repeated droughts on species occurrence and community composition; however, evidence of the direct impact of climatic factors on the demographic parameters of amphibians is currently not well documented. Further investigation of this issue is therefore of critical importance in order to optimize local and global wildlife conservation policies in the context of a changing climate. This study used capture–recapture data to investigate the impact of severe drought on the survival and fecundity of a threatened amphibian, the yellow-bellied toad (Bombina variegata, L.), as well as to predict how potential changes in the frequency of droughts might influence the population growth rate. By developing multievent capture-recapture models, we showed that severe drought has a negative impact on fecundity and postmetamorphic survival at different ontogenetic stages. Then, using stochastic matrix population models, we predicted that changes in drought frequency negatively influence the population growth rate, which is a warning sign for population persistence. Direct conservation actions are then proposed to mitigate the detrimental effects of drought on population dynamics.
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v v Article e012461v
IntroductIon
     -
       -

     

       
        
     -
      
      -
       
       -

     


23412
1UMR 5023 LEHNA, Laboratoire d’Ecologie des Hydrosystèmes Naturels et Anthropisés,
CNRS, Université Lyon 1, 69100 Villeurbanne, France
2CEFE UMR 5175, CNRS – Université de Montpellier – Université Paul-Valéry Montpellier – EPHE, Laboratoire
Biogéographie et Ecologie des Vertébrés, 1919 Route de Mende, 34293 Montpellier Cedex 5, France
3Oce National des Forêts, Agence de Verdun, 55100, Verdun, France
4Alcedo Faune Flore, Quartier Le Fez, 07110, Sanilhac, France
Citation:


Abstract.
-


    
      -



Bombina varie-
gata-


  
-

Key words:Bombina variegata
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
v v Article e012462v www.esajournals.org
CAYUELA ET AL.
-

     
       

      -
       



     


      

 
-

-

 -
  
   
Bufo bufo
    Triturus cristatus   
  
 T. cristatus
Ambysto-
ma tigrinum

Rana sevosaAmbystoma
opacum
Gyrinophilus porphy-
riticus

     
     
  
     
      
     
       

 

      


    Bombina varie-
gata 
      
      

       
        
    

-

       

    -
     B variegata  

        -
 

     -
 

     
      -
       

      -
-

    
      -
      
      -
     
-


Methods
Study area and field sampling
      
of B variegata     -
    -
       
       
      

   
      
       
    
      
       
v v Article e012463v www.esajournals.org
CAYUELA ET AL.
      -
     
     
      -
      
         

       
       

      
      
      
  
 
-
  

       
    

-
       

 
-
        
    
-
     

    
       
       
      

       
       
    
     


    -
-

Multievent capture–recapture model
       
       
       
     
         
     
      
     
     -
     
        
     -
    
      
       
       
      
        
          
      
       
       -
       
      

 -
      -
     
    
       -
      
       
       
       
  

 
     
       Bombina
variegata


v v Article e012464v www.esajournals.org
CAYUELA ET AL.
-


     
   αα 

α
ββββ

 -
    

 
     
     
      -


 φ φ
  φφ  φφ 
       
      

     
  -
-
      
     
  -
    
       
    -


-

1𝛼
JM
0𝛼
JM 0 0 0 0 0 000
01𝛼JF 0𝛼JF
0 0 0 0 000
00𝛽JM 01𝛽JM
0 0 0 000
0 00𝛽JF 01𝛽JF
0 0 000
0 0 00 𝛽SM 01𝛽SM
0 000
0 0 00 0 𝛽SF 01𝛽SF
000
0 0 0 0 0 0 1 0 000
0 0 0 0 0 0 0 1 000
0 0 0 0 0 0 0 0 100
0 0 0 0 0 0 0 0 010
0 0 0 0 0 0 0 0 001
10 0 0 0 0 0 0 0 0 0
01 0 0 0 0 0 0 0 0 0
00𝜙JM 000 0 0 0 0 1𝜙JM
00 0 𝜙JF 0000 0 0 1𝜙JF
00 0 0 𝜙SM 000 0 01𝜙SM
00 0 0 0 𝜙SF 00 0 01𝜙SF
00 0 0 0 0 𝜙BM 0 0 01𝜙BM
00 0 0 0 0 0 𝜙BF 0 01𝜙BF
00 0 0 0 0 0 0 𝜙NBM 01𝜙NBM
00 0 0 0 0 0 0 0 𝜙NBF 1𝜙NBF
00 0 0 0 0 0 0 0 0 1
(2)
(1)
v v Article e012465v www.esajournals.org
CAYUELA ET AL.

   γγ 
γγ 

sensu
    -
-


(4)
      
-

Biological scenarios using the E- SURGE program
    
      
     
     -
   
    
 -
      
 α ϕ   γ p(-
        

      
    -
  

 
     -
       
      -
       
-
       

      
     

-


     -
     -

     
t
   t       

     
  
  -


Simulation matrix model
      

  
100000 0 0 0 0 0
010000 0 0 0 0 0
001000 0 0 0 0 0
000100 0 0 0 0 0
000010 0 0 0 0 0
000001 0 0 0 0 0
000000 𝛾BM 01𝛾BM
00
000000 0 𝛾BF 01𝛾BF 0
0000001𝛾NBM 0𝛾NBM
00
000000 0 1𝛾NBF 0𝛾NBF 0
000000 0 0 0 0 1
1 00 00
1 00 00
1pJM pJM
000
1pJF pJF
000
1pSM 0pSM
00
1pSF 0pSF
00
1pBM 00pBM 0
1pBF 000pBF
1 00 00
1 00 00
1 00 00
(3)
v v Article e012466v www.esajournals.org
CAYUELA ET AL.
    
   

(5)
     1 
2
      
-

     t  
female at t   
      -
  

    
       
-
      -
        -
    

         
     k 
      
     
tkt0k
       


result
        
      
      
(00F
BP
S1
00
0
S2S3)

 
α 
α 
β 
β 
β 
β 
φ 
φ 
φ 
φ 
φ 
φ 
φ 
φ 

γ tt
γ tt
γ 

γ 

p 

p 

p 

p 

p 

p 

v v Article e012467v www.esajournals.org
CAYUELA ET AL.
      -
       

       
       
        
        
        
      
  
     α
φγ p  


    
        -
     
      
       
       

       -
      
  
 
       -
     
  
Bombina variegata
rk-

      

r    kDev 
1  YEAR  24  
2  YEAR  22  
3  YEAR  21  
4  YEAR    
5 DRY  YEAR  18  
6 DRY  YEAR  20  
7  YEAR  17  
8  YEAR    
   YEAR YEAR 21  
10   YEAR YEAR   
11   YEAR YEAR 18  
12   YEAR YEAR 16  
13 DRY  YEAR YEAR 15  
14 DRY  YEAR YEAR 17  
15   YEAR YEAR 14  
16   YEAR YEAR 16  
17   YEAR  21  
18   YEAR    
   YEAR  16  
20   YEAR  18  
21 DRY  YEAR  15  
22 DRY  YEAR  17  
23   YEAR  14  
24   YEAR  16  
25   YEAR  17  
26   YEAR  15  
27   YEAR  14  
28   YEAR  12  
 DRY  YEAR  11  
30 DRY  YEAR  13  
31   YEAR  10  
32   YEAR  12  
v v Article e012468v www.esajournals.org
CAYUELA ET AL.
 
      

     
       

       

dIscussIon

       
     B. variegata
     

      
    
Fecundity is impacted by drought events
      
     
      
     

       
   B variegata  
      
Bombina variegata
         
             
   





v v Article e01246v www.esajournals.org
CAYUELA ET AL.

  
        

 
    
    
      
  
       -

      
      -
       
       -
       
       
        
      -
      
         

Survival probability is impacted by age and drought
       -
      
      
      
        
       
         
     
  

       -
        -
 
       
 B variegata     

     
     
      
    -
    
     

     
      
     

       
      
 B variegata     -
     
      
      
     
      
     
      

Population growth rate is impacted by
drought frequency
     
     
      

       
      
       
     
      -
 
        
         
          
      
        B variegata
     
      
        
     
     -
  
      
     
     -
     
Conservation recommendations
      

for B. variegata    -
      
     
       -
     

    -
      
v v Article e0124610v www.esajournals.org
CAYUELA ET AL.
      -
      
Bombina variegata

-


      
    
 -
     -
     


-

       
     
      
    
  
       
       
 
      -
       


-
-
 

      -

 
     
      -

       
        
     
      -

 

 
     -
   

-
      -
  
      
     
      
     
      -
     

-
      
      
-
       

     
B. variegata
AcknowledgMents
       
   
       
       
      
  
      
 
lIterAture cIted

   

-
  
(Rana sylvatica
       
Bombina
variegata
       
     
       
     

-
     -

         
        
      Bombina
variegata



v v Article e0124611v www.esajournals.org
CAYUELA ET AL.
-

        
  
-
      

         



   
      -
   in   
   
    

-

    Ambystoma tigri-
num
-
-



-

-
  
  -

 -
       
    in     
-
       -
  
-
      -

      
    


-
 -
  

          
      -
     


      -
      


  -
 

        
   
   

          
    
  -




   
-

     Bombina Pelo-
phylaxRana
-
   


        
  Bombina variegata   
       


         
      



      
    

  -
        -
    Bombina variegata -
    


      
    

     


     
    
  

v v Article e0124612v www.esajournals.org
CAYUELA ET AL.
       
     
Bombina variegata et Bufo calamita

         
-
    
 -
-

     -

-

        -
Bombina variegata
      

    -

 
      Bombi-
na variegata    


-

        -

    

           
     
Rana sevosa
-

          
      -
      



     
-





           
     -
    

         
       
-

          -



        


-

  -


 
   
-
    




     -

  -
-

 
       -
      

        


   
     
  -
    

... The embryo and larval stage of biphasic amphibians are confined to aquatic environments (or very moist terrestrial habitats), with natural processes such as competition and predation causing mortality rates of up to 90% [26,27]. Anthropogenic threats within aquatic environments that may exacerbate the problem of embryo and larval survival include water pollution [28,29], changes to natural hydrology [30], pathogens [31,32], and invasive predators [33,34]. As larvae metamorphose and emerge from the water as froglets to disperse into the terrestrial environment, they are naturally prone to desiccation and predation [35,36], with the challenge of survival and successful reproduction as frogs compounded by fires [37], drought [30], habitat loss [38], and disease [39]. ...
... Anthropogenic threats within aquatic environments that may exacerbate the problem of embryo and larval survival include water pollution [28,29], changes to natural hydrology [30], pathogens [31,32], and invasive predators [33,34]. As larvae metamorphose and emerge from the water as froglets to disperse into the terrestrial environment, they are naturally prone to desiccation and predation [35,36], with the challenge of survival and successful reproduction as frogs compounded by fires [37], drought [30], habitat loss [38], and disease [39]. The combinations of these factors exert pressure on more than one life stage, thus exacerbating the potential for extinction and complicating conservation management. ...
... While this study identified that post-relocation survival and program success can depend on in situ threat management (i.e., predation, interspecific competition or disease), Cayuela et al. [213] did not actively control for threats across the release site. The predominant threat B. variegata face is habitat loss caused by agriculture and urban development [214]; however, drought and transport infrastructure are also causing population impacts [30,179]. The estimated population growth rate (λ) of the relocated B. variegata population was greater (2.71) than the control (1.21) and source populations (0.85), which demonstrates the success of this program in creating a self-sustaining population. ...
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Simple Summary Programs to conserve biphasic amphibians may fail if threats at different life stages are not addressed. Anthropogenic threats, such as altered hydroperiods and water pollution, exacerbate the already high natural rates of mortality at the aquatic egg and larval stage, while the terrestrial life stage is threatened by disease and habitat destruction. Threats at both of these life stages influence population viability. However, our examination of the literature suggests that studies rarely address threats to both life stages, and conservation actions rarely attempt to manage threats across the life cycle. The conservation of biphasic amphibians may thus be substantially improved by applying multiple conservation actions that deal with specific anthropogenic threats across all life stages. Abstract The unprecedented rate of global amphibian decline is attributed to The Anthropocene, with human actions triggering the Sixth Mass Extinction Event. Amphibians have suffered some of the most extreme declines, and their lack of response to conservation actions may reflect challenges faced by taxa that exhibit biphasic life histories. There is an urgent need to ensure that conservation measures are cost-effective and yield positive outcomes. Many conservation actions have failed to meet their intended goals of bolstering populations to ensure the persistence of species into the future. We suggest that past conservation efforts have not considered how different threats influence multiple life stages of amphibians, potentially leading to suboptimal outcomes for their conservation. Our review highlights the multitude of threats amphibians face at each life stage and the conservation actions used to mitigate these threats. We also draw attention to the paucity of studies that have employed multiple actions across more than one life stage. Conservation programs for biphasic amphibians, and the research that guides them, lack a multi-pronged approach to deal with multiple threats across the lifecycle. Conservation management programs must recognise the changing threat landscape for biphasic amphibians to reduce their notoriety as the most threatened vertebrate taxa globally.
... Similarly, droughts usually precede wildfire events and can reduce the availability of suitable breeding habitat and refuges which can lead to reductions in amphibian populations and communities before the passing of a wildfire Cayuela et al., 2016;Wassens et al., 2013). ...
... This was clearly shown for a coastal population of the green and golden bell frog (Litoria aurea) in the southern portion of the study area, which shrunk 10-fold during the 2019-2020 drought before the wildfires occurred . Drought can affect amphibians through mortality of tadpoles due to desiccation of drying water bodies (Beranek et al., 2020;, desiccation of adults and temperatures surpassing physiological thresholds Cayuela et al., 2016). These observations underscore the importance of long-term monitoring programmes to account for the cumulative impact of several weather events, especially as we enter a time where more extreme weather anomalies may occur in close succession or even simultaneously . ...
... and northern model r = −.228; Table S2), which is valuable given that it is common for drought and fire variables to be tightly linked (McEvoy et al., 2019), and (2) amphibians are highly dependent on moisture in their environment, allowing us to capture one of the main effects of drought on species in this group(Cayuela et al., 2016). ...
Article
Full-text available
Aim Changes to the extent and severity of wildfires driven by anthropogenic climate change are predicted to have compounding negative consequences for ecological communities. While there is evidence that severe weather events like drought impact amphibian communities, the effects of wildfire on such communities are not well understood. The impact of wildfire on amphibian communities and species is likely to vary, owing to the diversity of their life‐history traits. However, no previous research has identified commonalities among the amphibians at most risk from wildfire, limiting conservation initiatives in the aftermath of severe wildfire. We aimed to investigate the impacts of the unprecedented 2019–2020 black summer bushfires on Australian forest amphibian communities. Location Eastern coast of New South Wales, Australia. Methods We conducted visual encounter surveys and passive acoustic monitoring across 411 sites within two regions, one in northeast and one in southeast New South Wales. We used fire severity and extent mapping in two multispecies occupancy models to assess the impacts of fire on 35 forest amphibian species. Results We demonstrate a negative influence of severe fire extent on metacommunity occupancy and species richness in the south with weaker effects in the north—reflective of the less severe fires that occurred in this region. Both threatened and common species were impacted by severe wildfire extent. Occupancy of burrowing species and rain forest specialists had mostly negative relationships with severe wildfire extent, while arboreal amphibians had neutral relationships. Main Conclusion Metacommunity monitoring and adaptive conservation strategies are needed to account for common species after severe climatic events. Ecological, morphological and life‐history variation drives the susceptibility of amphibians to wildfires. We document the first evidence of climate change‐driven wildfires impacting temperate forest amphibian communities across a broad geographic area, which raises serious concern for the persistence of amphibians under an increasingly fire‐prone climate.
... Conversely, individuals being stuck in a patch could cause uneven survival rates among patches when drought extremes occur unpredictably. In such settings, local extinctions were more likely to occur when some patches were turned into ecological traps due to environmental change (Hale & Swearer, 2016) Drought is a climatic extreme, which has serious consequences for the persistence of metapopulations, seen here as an increasing drought severity significantly reducing the time that metapopulation persisted and increasing the rate of metapopulation decline, a phenomenon, which is consistent with the prediction that severer drought would cause higher speed of extinction (Cady et al., 2019;Cayuela et al., 2016). Increasing the severity of drought is more likely to cause a strong effect of desiccation, causing a high rate of mortality when reaching species' limits to drought. ...
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Corridors with good-quality habitats maintain the spatial dynamics of metapopulations by promoting dispersal between habitat patches, potentially buffering populations, and communities against continued global change. However, this function is threatened by habitats becoming increasingly fragmented, and habitat matrices becoming increasingly inhospitable, potentially reducing the resilience and persistence of populations. Yet, we lack a clear understanding of how reduced corridor quality interacts with rates of environmental change to destabilize populations. Using laboratory microcosms containing metapopulations of the Collembola Folsomia candida, we investigate the impact of corridor quality on metapopulation persistence under a range of simulated droughts, a key stressor for this species. We manipulated both drought severity and the number of patches affected by drought across landscapes connected by either good- or poor-quality corridors. We measured the time of metapopulation extinction, the maximum rate of metapopulation decline, and the variability of abundance among patches as criteria to evaluate the persistence ability of metapopulations. We show that while drought severity negatively influenced the time of metapopulation extinction and the increase in drought patches caused metapopulation decline, these results were mitigated by good-quality corridors, which increased metapopulation persistence time and decreased both how fast metapopulations declined and the interpatch variability in abundances. Our results suggest that enhancing corridor quality can increase the persistence of metapopulations, increasing the time available for conservation actions to take effect, and/or for species to adapt or move in the face of continued stress. Given that fragmentation increases the isolation of habitats, improving the quality of habitat corridors may provide a useful strategy to enhance the resistance of spatially structured populations.
... Previous studies have reported deleterious effects of hot summers on juvenile newt abundance, due mostly to desiccation of breeding sites. Desiccation of breeding sites drastically reduced larval amphibian survival, which had a direct impact on the abundance of post-metamorphic juveniles (Cayuela et al. 2016;Weinbach et al. 2018). In our study, we added water to mesocosms daily, so the aquatic habitats did not dry out even in the warm climate, which could explain the absence of any effect of a warm climate on juvenile abundance. ...
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... such, forecast increases in temperature, evaporation and rainfall variability (Steffen, 2009) and reduced moisture availability from cloud-stripping (Laidlaw et al., 2011(Laidlaw et al., , 2022) represent a major threat for these high-elevation species, with no capacity for upslope migration and western Europe (Cayuela et al., 2016). Ultimately, in the face of unmitigated climate change, montane and/or mesic-adapted amphibians with small geographic ranges face an uncertain future. ...
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... Likewise, a reduction in the immune capacity can involve higher disease susceptibility (Warne et al. 2011, Kohli et al. 2019; Chapters 4 and 5 in this volume) and might be contributing to the decline of amphibian populations facing droughts (McMenamin et al. 2008; reviewed by GriffisKyle 2016). Furthermore, costs in response to desiccation can persist beyond larval stages, and they can even negatively impact fecundity (Cayuela et al. 2016). Other environmental conditions that involve developmental acceleration in amphibian larvae can also imbalance the redox machinery and the immune system of amphibians such as in response to high salinity, warm temperatures, toxic substances, or as consequence of compensatory growth responses to detrimental conditions at early life (Mann et al. 2009, Burraco and GomezMestre 2016, Burraco et al. 2018, 2020a, MurilloRincón et al. 2017, Hidalgo et al. 2020. ...
... Drought is a climatic extreme which has serious consequences for the persistence of metapopulations, seen here as an increasing drought severity significantly reducing the time that population persisted and increasing the rate of population decline, a phenomenon which is consistent with the prediction that severer drought would cause higher speed of extinction (Cady et al. 2019, Cayuela et al. 2016. Increasing the severity of drought is more likely to cause a strong effect of desiccation, causing a high rate of mortality when reaching species' limits to drought. ...
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Connectivity maintains the spatial dynamics of metapopulations by promoting dispersal between habitat patches, potentially buffering populations and communities against continued global change. However, this function is threatened by habitats becoming increasingly fragmented, and habitat matrices becoming increasingly inhospitable, potentially reducing the resilience and persistence of populations. Yet, we lack a clear understanding of how reduced connectivity interacts with rates of environmental change to destabilise populations. Using laboratory microcosms containing metapopulations of the Collembola Folsomia candida , we investigate the impact of habitat connectivity on metapopulation persistence under a range of simulated droughts, a key stressor for this species. We manipulated both drought severity and the number of patches affected by drought across landscapes connected by either good or poor-quality corridors. We measured the time of population extinction, the maximum rate of population decline, and the variability of abundance among patches as criteria to evaluate the persistence ability of metapopulations. We show that whilst drought severity and number of drought-affected patches negatively influenced population persistence, these results were mitigated by increased habitat connectivity, which increased population persistence time and decreased both how fast populations declined and the variability in abundance among patches. Our results suggest that enhancing spatial connectivity can increase the persistence of metapopulations, increasing the time available for conservation actions to take effect, and/or for species to adapt or move in the face of continued stress. Given that fragmentation increases the isolation of habitats, improving habitat connectivity by using good quality corridors may provide a useful strategy to enhance the resistance of spatially structured populations.
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This research paper examines the influence of internal factors (female body weight, body condition) and external ecological factors on the reproductive parameters of females, as well as on the reproductive ecology of adult individuals of anuran amphibians. Among the most significant reproductive characteristics of females are the number of eggs in a clutch, the proportion of reproductive products to female body weight (contribution to reproduction), and the average weight of eggs. The body weight of the female and the ecological (meteorological) conditions of her activity during the year preceding spawning, as well as the hibernation conditions, have the greatest impact on the quantitative expression of these parameters. The proportion of reproductive products to female body weight in anuran amphibians usually ranges from 13 to 30%. Climate warming can directly affect the reproductive parameters of females, the survival of metamorphs, and the phenology of the spawning period.
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In Western Europe, habitat loss and landscape fragmentation has led to significant population decline in various animal groups, including amphibians. The extinction of the last natural populations of the yellow-bellied toad in Belgium, Luxembourg and several regions of southern and western France suggests a widespread decline. By using site-occupancy models and adding covariates corresponding to the human-influenced features of the landscape, we tried to identify the relative effects of different land-use types on the species’ distribution pattern in a man-made environment (the Alsatian Rhine floodplain in France). We recorded presence-absence data in 150 forest sample plots (300 × 300 m) and then modeled species distribution while taking into account detection errors in the field. Land-use was recorded on two spatial scales: within the forest sample plots and in a 1500 m radius buffer area around the forest plots. In the forest plots, toad occurrence was negatively correlated with loss of forest cover to agricultural land. In contrast, occurrence is positively correlated with the density of human-made rutted dirt paths and tracks, which provide semi-natural breeding sites. In the 1500 m radius buffer zones around forest plots, toad occurrence was negatively correlated with the density of urbanization and road networks. These results can be used to plan conservation strategies for amphibians in human-dominated landscapes.
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The fine structure of nuptial pad surface of the anuran amphibians Bom-bina variegata, Pelophylax epeiroticus, Pelophylax ridibundus and Rana dalmatina, was examined by scanning electron microscopy. Nuptial pads are cutaneous second-ary sexual characters of males that appear during the breeding season and disappear afterwards following an annual cycle. In males of P. epeiroticus, P. ridibundus and R. dalmatina, nuptial pads were observed on the ventrolateral aspect of the first digit (the thumb) as darkish and remarkably keratinized papillae. In males of B. variega-ta nuptial pads were almost black and very visible on the thumb, the second and the third digit of the front legs. They also extended on the ventral surface of the forearms. Under scanning electron microscope numerous small papillae were observed rising above pad's surface. In P. epeiroticus, P. ridibundus and R. dalmatina, these papillae were almost rounded at the base while at the dome shaped top they had many micro-processes organised in groups, thus assuming the shape of a "flower" which differed slightly among these three ranid species. In B. variegata the protuberances were coni-cal with heavily keratinized hooks without microprocesses. Our results show that sur-face morphology of nuptial pads is unique for each species and could be considered as a species-specific character.
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