Saturday, March 19, 2022

[Herpetology • 2022] Hyalinobatrachium mashpi & H. nouns • Two New Glassfrogs (Anura: Centrolenidae: Hyalinobatrachium) from Ecuador, with Comments on the Endangered Biodiversity of the Andes

 

Hyalinobatrachium mashpi & H. nouns  
Guayasamin​​, Brunner​, Valencia-Aguilar, Franco-Mena, Ringler, Armijos, Morochz, Bustamante, Maynard & Culebras, 2022


Abstract 
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.
 

Dorsal patterns of glassfrogs in life.
(A) Hyalinobatrachium mashpi sp. nov., CJ11642 (holotype). (B) H. nouns sp. nov., ZSFQ0537. (C) H. aureoguttatum, SC 435.
(D) H. talamancae, Costa Rica. (E) H. vireovittatum, Costa Rica. (F) H. valerioi, Costa Rica.
   Photos by Jaime Culebras (A, D, E, F), Jose Vieira (B) and Luis Coloma (C).

Dorsal and ventral photos of glassfrogs in life.
(A) Male of Hyalinobatrachium mashpi sp. nov., CJ11642 (holotype). (B) Gravid female of H. mashpi sp. nov., Mashpi Reserve, Ecuador.
(C) Male of H. nouns sp. nov., ZSFQ0537. (D) Male of H. nouns sp. nov., MZUTI3299 (holotype).
(E) Male of H. aureoguttatum, Ecuador. (F) Gravid female of H. aureoguttatum, Ecuador.
Photos by Jaime Culebras (A, B, D, E, F) and Ross Maynard (C).


Hyalinobatrachium mashpi new species 

Suggested English name: Mashpi Glassfrog
Suggested Spanish name: Rana de Cristal de Mashpi
 
Generic placement. The new species is placed in the genus Hyalinobatrachium Ruiz-Carranza & Lynch (1991), as modified by Guayasamin et al. (2009), on the basis of morphological and molecular data. The molecular phylogeny (Fig. 2) places the new species within the genus Hyalinobatrachium with high confidence. Phenotypically, the main diagnostic traits of Hyalinobatrachium are: (1) completely transparent ventral parietal peritoneum; (2) digestive tract and bulbous liver are covered by iridophores; (3) absent humeral spines; (4) white bones in life; (5) males call from the undersides of leaves; (6) females place the eggs on the undersides of leaves; (7) males provide extended parental care; and (8) tympanum with an orientation that places it almost on a horizontal plane (instead of a more lateral plane as observed in other glassfrog genera). All the aforementioned characteristics are present in Hyalinobatrachium mashpi sp. nov. We note that we have observed males on the same leaves as egg clutches for continuous days, but additional studies are necessary to confirm that these observations actually represent extended paternal care.

Diagnosis. Hyalinobatrachium mashpi sp. nov. is distinguished from other species in the genus mainly by its dorsal coloration (i.e., head with light yellow spots that may form an interorbital bar; dorsum lime green with small light yellow spots) and by its transparent pericardium (i.e., red heart visible in ventral view). Hyalinobatrachium mashpi sp. nov. is most similar to H. aureoguttatum, H. talamancae, H. valerioi, H. vireovittatum, and the new species described below. Differences among these species are indicated in Table 1 and Figs. 3–5. The new species is morphologically cryptic with Hyalinobatrachium nouns sp. nov. (described below); however, the two new species exhibit a considerable genetic distance (16S; 4.6–4.7%), which is particularly remarkable given that they are found at relatively close geographic proximity (straight distance = 18.9 km), but separated by the Intag-Guayllabamba river valley.

Parental care in Hyalinobatrachium mashpi sp. nov.
 (A) Male calling at San Vicente River, Mashpi Reserve, Pichincha Province, Ecuador. (B) Male at tributary of the Mashpi River, Tayra Reserve, Pichincha Province, Ecuador.
Photos by Carlos Morochz (A) and Jaime Culebras (B).

Habitat of Hyalinobatrachium mashpi sp. nov. Pichincha Province, Ecuador
(A) Tributary of the Mashpi River, Tayra Reserve. (B) Mashpi Reserve.
 (C) Tayra Reserve. (D) Habitat loss in the vicinity of Tayra Reserve. 
Photos by Jaime Culebras.

Etymology. The specific epithet mashpi is used as a noun in apposition and refers to the Mashpi area in northwestern Ecuador. There are several conservation efforts to preserve the last patches of forest remaining in Mashpi (e.g., Mashpi Lodge Reserve, Tayra Reserve, Amagusa Reserve, Mancomunidad del Chocó Andino, Chocó Andino Biosphere Reserve). Mashpi is a Yumbo word that means ‘friend of water’, an apt description of this glassfrog, which depends on healthy streams for its reproduction.

 

Hyalinobatrachium nouns new species
 
Suggested English name: Nouns’ Glassfrog
Suggested Spanish name: Rana de Cristal de Nouns
 
Generic placement. Based of morphological and molecular data, the new species is placed in the genus Hyalinobatrachium sensu Ruiz-Carranza & Lynch, as modified by Guayasamin et al. (2009). The molecular phylogeny (Fig. 2) places the new species within the genus Hyalinobatrachium with high confidence. Phenotypically, Hyalinobatrachium nouns sp. nov. shares the following diagnostic traits of the genus Hyalinobatrachium: (1) completely transparent ventral parietal peritoneum; (2) digestive tract and bulbous liver are covered by iridophores; (3) absent humeral spines; (4) white bones in life; (5) males call from the undersides of leaves, (6) females place the eggs on the undersides of leaves; (7) males provide extended parental care; and (8) tympanum with an orientation that places it almost on a horizontal plane (instead of a more lateral plane as observed in other glassfrog genera). All the aforementioned characteristics are present in Hyalinobatrachium nouns sp. nov. We note that we have observed males on the same leaves as egg clutches for consecutive days, suggesting the possibility of parental care, but additional studies are necessary to confirm that these observations actually represent extended paternal care as observed in other Hyalinobatrachium species (see Delia, Bravo-Valencia & Warkentin, 2017).

Diagnosis. Hyalinobatrachium nouns sp. nov. is distinguished from other species in the genus mainly by its dorsal coloration (i.e., head with light yellow spots that may form an interorbital bar; dorsum lime green with small light yellow spots) and by its transparent pericardium. Hyalinobatrachium nouns sp. nov. is most similar to H. aureoguttatum, H. mashpi sp. nov., H. talamancae, H. valerioi, and H. vireovittatum. Differences among these species are indicated in Table 1 and Figs. 2–4. The new species is morphologically cryptic with Hyalinobatrachium mashpi sp. nov. (described above), but they exhibit a considerable genetic distance (16S; 4.6–4.7%), which is remarkable given that they are found at relatively close geographic proximity (straight distance = 18.9 km), but separated by the Intag-Guayllabamba river valley.

Etymology. The specific epithet honors Nouns DAO, a global decentralized autonomous organization (“DAO”) composed of owners of Nouns characters, which are digital art creations that live on the blockchain. The mission of Nouns DAO is to promote and build the Nouns brand throughout the physical and digital world. One of the ways Nouns DAO accomplishes this is by building public works and funding philanthropic projects that support the wonder of nature.

Habitat of Hyalinobatrachium nouns sp. nov.  Imbabura Province, Ecuador
(A) Tributary of the Manduriacu River, Río Manduriacu Reserve. (B) Tributary of the Manduriacu River, Río Manduriacu Reserve.
(C) Río Manduriacu Reserve. (D) Habitat loss in the vicinity of Los Cedros Reserve. 
Photos by Jaime Culebras.


 Juan M. Guayasamin​​, Rebecca M. Brunner​, Anyelet Valencia-Aguilar, Daniela Franco-Mena, Eva Ringler, Anderson Medina Armijos, Carlos Morochz, Lucas Bustamante, Ross J. Maynard and Jaime Culebras. 2022.  Two New Glassfrogs (Centrolenidae: Hyalinobatrachium) from Ecuador, with Comments on the Endangered Biodiversity of the Andes. PeerJ. 10:e13109. DOI:  10.7717/peerj.13109