ArticlePDF Available

Observations on the Reproductive Behavior of a Neotropical Glassfrog, Hyalinobatrachium fleischmanni (Anura: Centrolenidae)

Authors:

Abstract and Figures

This study investigated geographic variation in a suite of reproductive behavioral traits in Hyalinobatrachium fleischmanni across several sites in Mexico and Ecuador. We made observations on the frequency of egg-mass brooding behavior and compared brooding encounter rates between wet and dry forest types. Brooding encounter rates were significantly higher in the drier region, suggesting a potential relationship between paternal care and climatic conditions. We also compared calling and oviposition sites between geographic regions and tested for associations with the distributional range of the frog-eating bat, Trachops cirrhosus. In regions where H. fleischmanni and T. cirrhosus co-occur, both calling males and egg masses were more frequently found on ‘less exposed’ lower surfaces of leaves, where risk of attack from aerial predators may be reduced. We also provide novel information on brooding behavior and clutch guarding, and discuss the implications of our results in the framework of existing information on the reproductive biology of this species.
Content may be subject to copyright.



Jesse Delia1,2,7, Diego F. Cisneros-HereDia3,4, JonatHan WHitney2,5, anD rene Murrieta-galinDo6








abstraCt.              

                
       
      
     
   


KeyWorDs.          


  
    

   
      
       
    
     
     
     

 
   
      

   
     
      
   

      



        
     
     

       




       
     
     
      


       


 
   
     
       

    
     
     


     
       
 
     
      
      
       
   


   
 
       

    

       

      







      
     
     
       
   
Figure 1.           
 
                 
    






  
        
      
   



    
       

        




     
  
      
     



     
    

      
       
      
    

    
         
      

      
   
     



      
 
   
  



 

       

         
table 1.                

   


 
  
 
  
 
  
 
  
 
  


 
  
 
  
 
  

 
  
 
  
 
  
  
   
       
      
         






      



   



    


  
  
 


  

 




      
       




       


        
    
      








        
     

         
    
   

 


        
       

       
   
       
          





     

        

  
         
        
  
    




  
       



       


  







        
        
      
 


      


     
   




Figure 2.   
       


   

 


Figure 3. 




     
 
           

table 2.     

  


 
   
  
   
  
  
   
   
       
       
  

      
       
        
       
      
    
     


      


     

     
  
      
      

    




     









 


      

  



        


   
      

Figure 4.






        



     
      
   

  

     


         
      


   


     
      
 




     

      

     




      

       
       
Figure 5.
    


  
     
     

  


Figure 7.


              



  

Figure 6.


       

    




      
       
  

        
    
        


      

    
        
       





     





  
   
       
       




      


       

      
        
  
   
     
  
  

    

         

     
       
         
 
      


        

   
     
   
      
     
       
      


   








     

      
       
   
     



         
  

       
        

       
       
      

  
       



         
    
    
     


    
      
       

    
     

     

     
   

  

   

       
     
      
       
       
     
    

        


      
        





     
   

     

  
       
       
       
      
     

      
      
  

       

  
    
     
       






         
          

     
       
           


     


     


         


        
         
       


       
 




  
      
      




bolivar-g. W., t. grant, anD l. a. osorio.  
     

breeDlove, D. e. 
       

CalDWell, J. P. 


CastrovieJo-FisHer, s., J. M. PaDial, J. C. CHaParro, r. aguayo,
anD i. De la riva. 
       


Cisneros-Here Dia, D. C. anD r. W. MCDiarMiD. 
      
  
        

ClarK, M.      
    

       

DraKe, D. l. anD a. W. ranvestel.  
     

eMMons, l. H.     
      

goin, C.      
     

greer, b. J. anD K. D. Wells. 
      

guayasaMin, J. M. anD C. barrio-aMoros.  
      

guayasaMin, J. M., s. CastrovieJo-FisHer, J. ayarzagüena,
l. trueb, anD C. vila.   
      
     

Hayes, M. P. 
    
      

Heyer, W. r., M. a. Donnelly, r. W. MCDiarMiD, l-a. C. HayeK,
anD M. s. Foster (eDs).    
     

HiJMans, r. J., s. e. CaMeron, J. l. Parra, P. g. Jones, anD
a. Jarvis.      
       

HolDriDge, l. r.        

JaCobson, s. K.       
      

JaCobson, s. K.     
       

iuCn        
    

Janzen, D. H.   

KubiCKi, b. 
      

liPs, K. r., J. r. MenDelson, iii, a. Munoz-alonso, l. CanseCo-
Marquez, l., anD D. g. MulCaHy.  


MCDiarMiD, r. W. 
   
     

MCDiarMiD, r. W. 


MCDiarMiD, r. W. anD K. aDler.    
        

MeDellín, r. a., H. t. arita, anD o. sánCHez. 
        
     

PounDs, J. a., M. P. FogDen, J. M. savage, anD g. C. gorMan.


savage, J. M. 


starrett, P. H. anD J. M. savage. 
  
       

stuart, l. C.       

tuttle, M. D. anD M. J. ryan.     
       

tuttle, M. D. anD M. J. ryan.     



villa, J. 


villa, J.      
        

villa, J.  

     

voCKenHuber, e. a., W. HöDl, anD u. KarPFen. 
  
      
      

  
voCKenHuber, e. a., W, HöDl, anD a. aMézquita.  
      
      

Wells, K. D. 

Wells, K. D. anD J. sCHWartz. 






... Glass frogs (Centrolenidae) are unique in this aspect since most of the species produce whitish eggs; yet, arboreal clutches are the main reproduction mode (Guayasamin et al., 2009). It has been suggested that these arboreal eggs are mostly deposited in the underside of leaves to avoid UV radiation; however, in Hyalinobatrachium fleischmanni this is an adaptation against predation (Delia et al., 2010). Hence other selective pressures, different to UV protection, could be influencing the presence, absence and the amount of egg pigmentation in amphibians. ...
... Parental guarding is widespread across Centrolenidae, and some species with dark pigmented eggs like E. prosoblepon have reduced parental care, compared to species with whitish eggs (Delia et al., 2017;Jacobson, 1985). In locations where H. fleischmanni overlaps with a batrachophagous bat (Trachops cirrhosus), nesting behavior and oviposition is enclosed, in the downside of leaves, and in locations outside the distribution of the bat, oviposition occurs in exposed locations (Delia et al., 2010). The study of nesting behavior in the polymorphic populations of E. prosoblepon could provide evidence to support this hypothesis. ...
Article
Full-text available
The adaptive role of amphibian oocyte melanic pigmentation and its molecular control are still elusive. Here we present evidence of a polymorphism in egg pigmentation in the emerald glass frog Espadarana prosoblepon. In Ecuadorian natural populations of this species, females can lay dark brown or pale eggs that develop into normal pigmented tadpoles and adults. This trait is a sex-limited phenotype that is inherited like a recessive allele that we called pale eggs like (pel). The pel phenotype is exclusive of oocyte cortical melanic pigmentation, which is reduced in comparison to wild type (wt) dark pigmented oocytes. Consequently, pel early embryos are paler in appearance, with reduced melanic pigmentation distributed to early blastomeres and embryonic ectoderm. However, these embryos form normal melanocyte derived pigmentation. Finally, we discuss the origin of this polymorphism and propose the use of E. prosoblepon as a model to study the adaptive role of egg pigmentation.
... We never observed territorial fighting in H. cappellei; however, this behavior has been documented in other glass frog species with parental care (Hyalinobatrachium colymbiphyllum ;Savage 2002;H. fleischmanni;Delia et al. 2010;H. valerioi;McDiarmid and Adler 1974;Cochranella granulosa;Kubicki 2007; Centrolene daidalea; Rojas-Runjaic and Cabello 2011). ...
Article
Female mate choice is often based on male traits, including signals or behaviors, and/or the quality of a male’s territory. In species with obligate paternal care, where care directly affects offspring survival, females may also base their mate choices on the quality of a sire’s care. Here, we quantified male reproductive success in a natural population of the glass frog Hyalinobatrachium cappellei, a species with male parental care, to determine the influence of territory quality, male traits, and paternal care behaviors on female mate choice. We found that attending males have a higher chance of gaining new clutches than nonattending males. Our results indicate that females do not select males based only on body condition, calling persistence, or territory traits. Instead, our findings support the hypothesis that females choose males based on care status. Indeed, males already attending a clutch were 70% more likely to obtain another clutch, and the time to acquire an additional clutch was significantly shorter. We also found that males adjust their parental care effort in response to genetic relatedness by caring only for their own offspring; however, remaining close to unrelated clutches serves as a strategy to attract females and increase chances of successful mating. Thus, males that establish territories that already contain clutches benefit from the signal eggs provide to females.
Article
Full-text available
Background The Tropical Andes is the world’s most biodiverse hotspot. This region contains >1,000 amphibian species, more than half of which are endemic. Herein we describe two new glassfrog species (Centrolenidae: Hyalinobatrachium ) that we discovered within relatively unexplored and isolated localities of the Ecuadorian Andes. Methods We employed morphological, acoustic, and molecular methods to test the hypothesis that Hyalinobatrachium mashpi sp. nov and H. nouns sp. nov. are species new to science. Following standard methods, we generated mitochondrial sequences (16S) of 37 individuals in the genus Hyalinobatrachium . We inferred the phylogenetic relationships of the two new species in comparison to all other glassfrogs using Maximum Likelihood. In addition to describing the call of H. mashpi sp. nov., we performed a discriminant analysis of principal components (DAPC) with the advertisement call characteristics of several congeners. Results Based on an integrative taxonomy approach, we describe two new species. Morphological traits and the inferred phylogeny unambiguously place the new taxa in the genus Hyalinobatrachium . Both species are distinguished from other glassfrogs mainly by their dorsal coloration ( i.e ., dorsum lime green with small light yellow spots, head usually with interorbital bar) and transparent pericardium ( i.e ., the heart is visible through the ventral skin). The new species exhibit a high morphological similarity ( i.e ., cryptic) and occur within relatively close geographical proximity (closest aerial distance = 18.9 km); however, their uncorrected p distance for the mitochondrial gene 16S is 4.6–4.7%, a value that greatly exceeds the genetic distance between closely related species of centrolenid frogs. The DAPC revealed that the advertisement call of H. mashpi sp. nov. is acoustically distinct. Discussion Our findings are congruent with several previous studies that report a high degree of endemism in the Toisán mountain range, which appears to be isolated from the main Andean cordillera for some amphibian groups. We recommend that both H. mashpi sp. nov. and H. nouns sp. nov. be listed as Endangered, following IUCN criteria. These new species provide another example of cryptic diversity in the Andes—further evidence that the region fosters much more biodiversity than we have the resources to catalog. Threatened by mining and other exploitative industries, these glassfrogs and many other yet-to-be-discovered Andean species highlight the dire need for effective conservation measures—especially in northwestern Ecuador.
Article
Full-text available
Signal detection is a fundamental requirement for any communicative interaction. Acoustic signals, however, experience amplitude losses during their transmission through the environment, reducing their detection range. Displaying from sites that increase the amplitude of the sound produced, such as cavities or some reflective surfaces, can improve the detectability of signals by distant receivers. We measured the effect of leaf calling sites on the calls of an arboreal (Hyalinobatrachium fleischmanni) and a leaf-litter specialist (Silverstoneia flotator) frog species. We collected the leaves where males of both species were observed calling, and conducted play-back experiments to measure their effect on the amplitude of frog calls. Overall, the leaves used by H. fleischmanni and S. flotator were of similar dimensions, and amplified the calls of each species by about 5.0 and 2.5 dB, respectively. The degree of call amplification was unrelated to leaf dimensions or the position of the frogs on the leaves, but explained by the different frequency content of the calls of each species. We suggest that amplification of frogs calls by leaves could represent either a benefit or impose costs for arboreal and terrestrial species, which may depend on the spatial location of intended and unintended receivers.
Article
Full-text available
Ten genotypes of maize collected from National Center for Genetic Resources and Biotechnology (NACGRAB) were induced with X-ray for morphological and molecular assessment. The experimental design was complete randomized design with four replicates. Morphological and molecular statistical analyses of treated genotypes were conducted using SAS and Power Maker Packages, respectively while dendrogram was generated using Jaccards similarity coefficient using Unweighted Paired Group Method and Arithmetic Averages (UPGMA). The study revealed significant difference which is an indication of genetic variation of characters in treated maize. Genotype DTSR-Wco performed best in plant height (62.35 cm), leaf length (62.35 cm), number of leaves (3.15), leaf width (7.55 cm) and dry leaf biomass (0.24 g). X-ray at 90 Kv/mass, 95 Kv/mass and 100 Kv/mass decreased plant heights to 54.25cm, 53.87cm and 54.10cm respectively compared to Control. Heritability estimate was greater than 70% for all characters evaluated. Genotype TZM 1551 at 0 Kv/mass yielded the highest concentration of DNA at 2841.60 ng/ul and the highest genomic DNA concentration was obtained at 95 Kv/mass for TZM 132 with 1.91%. Primer BMC 1755 was most polymorphic with 58.77% in treated maize genotypes. The plant height was strongly correlated with leaf length (r=0.9), leaf width (r=0.76) and number of leaves (r=0.77). Principal component analysis showed close relationship between plant height (-0.03) and leaf length (0.05) compared with leaf width (-0.67) and number of leaves (0.69). Dry shoot biomass (0.05) was closely related to dry root biomass (-0.03) and dry leaf biomass (-0.04).
Article
Full-text available
The Neotropical amphibian family Centrolenidae currently includes 156 named species of nocturnal anurans commonly known as glassfrogs. With 79 species, Colombia is the country with the highest diversity of centrolenids. However, the number of species known to occur in the country remains uncertain because research often results in names being resurrected or placed in synonymy, the description of new taxa, and range extensions of species, including new country records. Based on field trips and assess of additional specimens, herein we report new distribution data for centrolenids species in Colombia. These data include six new distribution records for: (Cochranella granulosa, Nymphargus balionotus, N. chami, N. grandisonae, Hyalinobatrachium mondolfii, and H. pellucidum). Records of C. granulosa and H. pellucidum are the first records of these species from Colombia. Thus, our study increases to 81 the numbers of glassfrogs for this country. Because most Hyalinobatrachium have a conservative morphology, making species identification problematic when only based on external traits, we sequenced a fragment of the mitochondrial gene 16S to confirm species identities within a phylogenetic context. We discuss the taxonomic implications of our results for the recognition of species and populations that are morphologically similar to H. talamancae.
Article
Full-text available
Hyalinobatrachium fleischmanni is one of the widest ranging glassfrog species, occurring in the lowlands from Mexico through Central America to Ecuador. Despite its conservative morphology, previous studies suggested that the species is comprised of multiple lineages. Here we test the hypothesis of cryptic species within H. fleischmanni by means of morphology, morphometrics, bioacoustics, and molecular analysis. Molecular delimitation based on mitochondrial and nuclear genes detected 17 candidate species within H. fleischmanni but combined with other sources of evidence, we support the recognition of at least three different species within the name H. fleischmanni. The identity of H. fleischmanni sensu stricto is supported for populations from Costa Rica to eastern Honduras while the name Hyalinobatrachium tatayoi corresponds to the southern lineages in Costa Rica and South America. Those two species differ in the note duration of the advertisement call and in the absence of nuptial pads in the hand webbing of H. fleischmanni males. Populations from Mexico and Guatemala represent a third species to which we assign the available name H. viridissimum comb. nov. Hyalinobatrachium viridissimum differs from H. fleischmanni and H. tatayoi in mitochondrial DNA divergence, variation in peak frequency, and note duration of the advertisement call. A divergent lineage from western and central Honduras is tentatively assigned to H. viridissimum. Based on these results, we provide updated information for each species. http://www.zoobank.org/urn:lsid:zoobank.org:pub:96D65174-4F8B-4E4B-8C85-967767311255
Article
Full-text available
Parental care increases offspring survival, but may impose costs by decreasing adult survival or mating opportunities. Because individuals have limited resources, time allocation and risk decisions are expected to vary according to the care status and threat faced by parents. Herein, we evaluated the sources of mortality of clutches of the glassfrog Hyalinobatrachium cappellei and the importance of paternal care for offspring survival. We also compared time allocation patterns and antipredator behavior between attending and non-attending males. Using naturalistic observations and field experiments with different dummy predators, we hypothesized that (1) offspring survival would be positively correlated with paternal care; (2) attending males would spend most of the time caring for the embryos, while non-attending males would spend more time foraging and calling; (3) attending males would prioritize their own survival when facing a high risk of predation, even with negative impacts on offspring survival. Main sources of embryo mortality included predation and dehydration, and offspring survivorship was almost totally dependent on paternal care. Although non-attending males spent more time calling and foraging, attending males also called and were able to attract females and increase their mating success. However, contrary to our prediction, we found that attending males were more risk-tolerant, increasing not only offspring survival but also their mortality risk. Our findings highlight the importance of the predation risk level on parents’ decisions and that the reproductive status may play a significant role in determining antipredator behavior and mating success in glassfrog males. Significance statement In species with parental care, parents face a trade-off between investment in current offspring survival and chances of future reproduction. Hence, it is expected that natural selection will favor parents that attend offspring without incurring in higher risk of predation. We investigated time allocation patterns and behavioral responses to different levels of threat in a glassfrog with paternal care. Using field observations and predation experiments, we found that attending and non-attending males of Hyalinobatrachium cappellei behaved differently depending on their care status and level of threat. Males were more likely to tolerate high risks only when they were caring for clutches. We also found that the commitment of males to continue caring resulted in higher offspring survival. Parental care behavior increased not only larvae hatching success, but also matting success of attending males, suggesting that paternal care might be under sexual selection.
Article
Full-text available
Glassfrogs (family: Centrolenidae) represent a fantastic radiation (~150 described species) of Neotropical anurans that originated in South America and dispersed into Central America. In this study, we review the systematics of Ecuadorian glassfrogs, providing species accounts of all 60 species, including three new species described herein. For all Ecuadorian species, we provide new information on the evolution, morphology, biology, conservation, and distribution. We present a new molecular phylogeny for Centrolenidae and address cryptic diversity within the family. We employ a candidate species system and designate 24 putative new species that require further study to determine their species status. We find that, in some cases, currently recognized species lack justification; specifically, we place Centrolene gemmata and Centrolene scirtetes under the synonymy of Centrolene lynchi; C. guanacarum and C. bacata under the synonymy of Centrolene sanchezi; Cochranella phryxa under the synonymy of Cochranella resplendens; and Hyalinobatrachium ruedai under the synonymy of Hyalinobatrachium munozorum. We also find that diversification patterns are mostly congruent with allopatric speciation, facilitated by barriers to gene flow (e.g., valleys, mountains, linearity of the Andes), and that niche conservatism is a dominant feature in the family. Conservation threats are diverse, but habitat destruction and climate change are of particular concern. The most imperiled glassfrogs in Ecuador are Centrolene buckleyi, C. charapita, C. geckoidea, C. medemi, C. pipilata, Cochranella mache, Nymphargus balionotus, N. manduriacu, N. megacheirus, and N. sucre, all of which are considered Critically Endangered. Lastly, we identify priority areas for glassfrog conservation in Ecuador.
Article
Full-text available
We describe the fighting behaviour in Centrolene andinum. Males fight upside down, grasping one another venter-to-venter. This behaviour agrees with the prediction that all species in the genera Centrolene and Cochranella share a derived fighting behaviour, in contrast with the plesiomorphic, amplexus-like state of Hyalinobatrachium.
Article
During some nights, male Centrolenella fleischmanni called continuously from vegetation overhanging streams and maintained amplexus and deposited eggs that were attended by males. Males generally attended eggs late in the evening, when few additional females were available, thus minimizing lost mating opportunities. Male C. prosoblepon called sporadically, moved actively, initiated amplexus, and showed no paternal care of clutches. Female C. prosoblepon attended eggs immediately after deposition. Egg attendance did not enhance larval survivorship significantly in either species. For both species, male reproductive success was correlated with length of residency at the site, but snout-vent length and call pitch or duration were not correlated with male success in obtaining mates. Larval survivorship was enhanced by choice of wet microhabitats for oviposition by C. prosoblepon. -from Author
Article
A case of symbiosis between the centrolenid frog Centrolenella fleischmanni and the drosophilid fly Drosophila sp. nov. is documented. The fly lays her eggs near the surface of the frog's egg mass. Upon hatching, the larvae feed upon the frog embryos, killing many or all of them. Pupation occurs within the egg mass before the embryos hatch. Flies emerge about 10-13 days after the maggots hatch, and after the tadpoles have left the egg mass. For the "frogflies" the relationship appears to be obligatory, but not so for the frogs, which derive no obvious benefit from the association.
Article
Biological Central America includes political Central America, the lowlands of southern México, and northwestern Colombia (Chocó). Ninety per cent of the region lies north of the Nicaraguan Depression, and only 25% of the area rises above the 600-m contour. Owing to the Pacific position of the continental divide most of the lowlands lie on the Caribbean versant, and the major drainage basins are so located. Pliocene uplift, erosion, and Tertiary and Quaternary volcanism are responsible for the high relief of the highlands, which are discontinuous above about 1,500-2,000 m. Temperature is largely a function of altitude, and annual range is slight. The Caribbean versant receives 2-3 times as much rainfall as do the Pacific lowlands and the highlands. The low sun period is the dry season, and the rainfall displays a double maximum with peaks during the early and late portions of the high sun period. Rainfall varies from less than 500 mm annually to more than 7,000 mm. As a generalization rainforest clothes the lowlands of the Caribbean versant and dry forests the Pacific. The northern highlands support a cover of oak-pine up to about 3,000 m above which are pine-fir forests and meadows. In the south, wet forests are characteristic of the highlands with patches of páramo above 3,100 m. Protected valleys support savannas and scrub forests. In the north Nuclear Central America has remained positive since the Cretaceous. To the south between southern Nicaragua and Colombia open, island-studded seaways persisted, with the possible exception of the Paleocene interval, up to the Pliocene.