Fig 5 - uploaded by Sebastián Barrionuevo
Content may be subject to copyright.
Hyoid apparatus and the m. sternohyoideus and its insertion area in the hyoid plate of Telmatobius rubigo (upper and lower left) and T. oxycephalus (upper and lower right). In T. rubigo , it is evident the broader insertion area of M. sternohyoideus . Note the mineralized hyoid plate and the invasion of the ossification of the posteromedial processes into the more wide and robust plate of T. rubigo . In con-
Source publication
The most common feeding mechanism among aquatic vertebrates as fishes, turtles, and salamanders is inertial suction. However, among the more than 6,400 species of anurans, suction feeding occurs only in pipids. Pipidae is a small basal lineage relative to Neobatrachia, an enormous clade that contains about 96% of extant anurans. The Andean neobatra...
Contexts in source publication
Context 1
... arise from the lateral and posterior margins of the plate-the anterolateral, the posterolateral, and the post- eromedial processes. In most anurans, just posteromedial processes ossify. The hyoid plate of Telmatobius rubigo is broad, with the anteromedial margin of the hyoglossal sinus lying at about the level of the anteromedial proc- esses ( Fig. 5). Ossification of the posteromedial processes reaches the level of the base of the posterolateral proc- esses. In addition, the central and anterolateral regions of the plate are heavily mineralized. The hyoid plate in T. oxycephalus is narrower than in T. rubigo and the medial margin of the hyoglossal sinus lies well posterior to the ...
Context 2
... toward the mouth relative to a stationary reference point. For the morphological analysis, museum specimens of Telmatobius rubigo and T. oxycephalus were studied. To examine musculature and provide contrast between muscles and cartilaginous elements of hyoid, cartilage was stained with Alcian Blue as described by Wassersug (1976) but interrupting the process at his point. In this way, bone was not stained and soft tissues were not cleared. To examine osteology, the protocol of Wassersug (1976) was finished, that is, specimens were cleared and double-stained with Alizarin Red S (for bone) and Alcian Blue (for cartilage). Specimens are housed in Fundaci on Miguel Lillo Herpetological Collection (FML) and the National Herpetological Collection of Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” (MACN). Telmatobius oxycephalus FML 03836-I (adult female, cleared and stained -CS-), 3836-II, and 3836-III (adult males, CS); FML 2867-I, 2867-II (adult males, CS), 2867-III, and 2867-IV (adult females, CS); FML SB 016, 555, MACN 39082 (adult females, stained -S-), FML 019 (adult male, CS), 556 (adult male, S). Telmatobius rubigo FML 20829 (adult male, CS); MACN 41671 (adult male, S), 41673 (adult female, S), 41661, 41668 (adult females), 41679, 41682 (adult males). The underwater feeding pattern in Telmatobius rubigo includes movements of the body (approach and/ or lunge), jaws (opening and closing), and buccal floor (retraction-depression and protraction-elevation). The prey-capture sequence begins when the frog approaches the prey (Fig. 2, SVideo 1: no1jo2kc, Video 2: and Video 3: A lunge, powered by extension of the hind limbs, often is initiated before the mouth is opened. The mouth is opened when the frog is close to the prey; the gape angle does not exceed 45 . This small gape is limited to the anterior part of the mouth, whereas the lateral sides of the mouth remain closed or barely opened. The lower jaw bending and the depression of the buccal floor are evident. Immediately after mouth opening, the prey moved toward the frog (in an earth-bound frame of reference) and the forelimbs are not involved in the ingestion (inertial suction feeding, Fig. 3). In fact, Telmatobius rubigo was never observed using forelimbs for prey capture; during feeding, the forelimbs remain on the sub- strate. Although T. rubigo did not use its forelimbs to catch prey, it has been observed that it is capable of some manual dexterity when the prey is not completely engulfed. In that case T. rubigo can use the dorsal side of its hands to accommodate the prey. Once the prey is engulfed, the mouth closes as the buccal floor is raised and water is expelled from the anterior part of the mouth. This is evidenced by air bubbles that appear as water is expelled. The underwater feeding pattern in Telmatobius oxycephalus includes movements of the body (approach and/or lunge), jaws (opening and closing), and forelimbs (extension and scooping). The prey-capture sequence begins when the frog approaches the prey (Fig. 4, Video 4: http:// bcove.me/a6npaavu). The mouth is opened when the frog is close to the prey, and the gape angle is around 90 8 . This striking wide gape is radically different from that of T. rubigo . Lower jaw bending is not evident. As the mouth opens, the frog extends its forelimbs forward to scoop the prey into the mouth with the dorsal side of its hands. During the feeding cycle, depression of the buccal floor was less evident than in T. rubigo . The forelimbs obstruct the direct observation of the profile of the frog during feeding. However, in one of the trials, the prey was pressed against the tank wall and the frog could not extend its forelimbs; in this sequence, the absence of buccal floor depression was evident. After engulfing the prey, the frog closes its mouth; the mouth can be open again to manipulate the prey by pushing it with the forelimbs. In land, T. oxycephalus was observed to use its round and short tongue (Video 5: As its tongue cannot extend too farther, the frog needs to lunge over the prey to get closer to catch the prey with the tongue. The major differences found between Telmatobius rubigo and T. oxycephalus in relation to the hyoid apparatus and related muscles, tongue, lower jaw, and labial configuration are summarized in Table 1. Hyoid apparatus and related muscles. The hyoid of adult anurans typically consist in a broad cartilaginous plate that bears 4 pairs of processes. The anterior hyalia are slender cartilaginous processes that, in most anurans, connect the hyoid with the otic capsules. Usually, there are three other pairs of processes that arise from the lateral and posterior margins of the plate— the anterolateral, the posterolateral, and the posteromedial processes. In most anurans, just posteromedial processes ossify. The hyoid plate of Telmatobius rubigo is broad, with the anteromedial margin of the hyoglossal sinus lying at about the level of the anteromedial processes (Fig. 5). Ossification of the posteromedial processes reaches the level of the base of the posterolateral processes. In addition, the central and anterolateral regions of the plate are heavily mineralized. The hyoid plate in T. oxycephalus is narrower than in T. rubigo and the medial margin of the hyoglossal sinus lies well posterior to the level of the anteromedial processes. The hyoid plate is completely cartilaginous and the ossification of the posteromedial processes is not reaching the base of the posterolateral processes. As in other anurans, in Telmatobius there are hyoid protractors (the m. geniohyoideus) and hyoid retractors (the m. sternohyoideus), as well as hyoid levators (the m. petrohyoideus) and depressors (the m. omohyoideus). The m. sternohyoideus originates from the sternum (but some fibers are in continuity with m. rectus abdominis) and inserts in the ventral surface of the hyoid plate. The hyoid muscles of T. rubigo and T. oxycephalus differ primarily in relation to the morphology and insertion of the m. sternohyoideus. In T. rubigo , the m. sternohyoideus is massive, and it is formed by two slips: a deep slip and a superficial slip. The deep or dorsal slip inserts along the posterior border of the hyoid plate near the bases of the posterolateral and posteromedial processes. The superficial or ventral slip inserts on the anterior part of the hyoid plate at the base of hyale and the anterolateral process, almost reaching the medial line of the hyoid plate. In T. rubigo , the area of the hyoid plate where the m. sternohyoideus inserts is heavily mineralized. In T. oxycephalus , the m. sternohyoideus is single and less massive than in T. rubigo . This muscle inserts along the lateral margin of the hyoid plate, near the base of the hyale and the base of the anterolateral, posterolateral and posteromedial processes. The area of insertion is smaller than in T. rubigo , and the hyoid plate is not mineralized. rubigo has a small and flat tongue (Fig. 6A,C) that is attached to the buccal floor approximately to 90% of its extension, with only the posterior margin free. In contrast, the tongue of T. oxycephalus is better developed, thicker and it is also attached to the buccal floor (Fig. 6B,D) but approximately to 70% of its total length, and the posterior and posterolateral margins are free. The tongue of anurans is composed of two muscles (Figs. 7 and 8)—the m. genioglossus (protracting the tongue) and the m. hyoglossus (retracting the tongue). The paired m. hyoglossus originates from the posteromedial process of hyoid and the anterior fibers enter the tongue. In T. rubigo , the m. hyoglossus is not massive, and the contralateral muscles are not completely fused to each other; the anterior fibers of the m. hyoglossus insert superficially in the tongue and divides in segments that interdigitated with the m. genioglossus. The ventralmost fibers of m. hyoglossus insert to the anterior part of the tongue (Fig. 8). In T. oxycepha- lus , the paired hyoglossus muscles are massive and fused to one another (Fig. 8); the anterior fibers enter the tongue and their anterior segments are not evident as in T. rubigo . In both species, only the interdigitating element of the m. genioglossus is present. This muscle originates from the mandibular symphysis and radiate posterolaterally to enter the tongue. The interdigitation of the posterior fibers of the m. genioglossus is more superficial and evident in T. rubigo , than in T. oxycephalus , where the posterior fibers enter the larger tongue. The ventral element of the m. genioglossus is absent in both species. Jaw and submandibular muscles. The jaw muscles consist, basically, of one set of muscles to open the mouth (depressor) and several sets of muscles to close it (levators). In Telmatobius rubigo , the m. depressor mandibulae is composed of anterior and posterior parts (Fig. 9). The anterior slip originates from the annulus tympanicus, otic ramus of squamosal and the epimysium of the lateral edge of m. levator mandibulae posterior longus. This slip is bulky and inserts on the articular process of the lower jaw. The posterior slip originates from the dorsal fascia; it is thick and triangular, and almost entirely covers the m. dorsalis scapulae and the m. latissimus dorsi. The most posterior fibers originate at the level of m. obliquus externus. Like the anterior slip, the posterior inserts on the articular process of lower jaw. In T. oxycephalus , the anterior part of the m. depressor mandibulae is less bulky than in T. rubigo . It originates mostly from the epimysium of the lateral edge of m. levator mandibulae posterior longus, although some fibers originate in tympanic annulus and in the otic ramus of squamosal (Fig. 9). The posterior slip does not extend as far posteriorly as in T. rubigo; it covers only the anterior half of the m. dorsalis scapulae (Fig. 9). The difference in the origins of the posterior slip of depressor mandibulae between the two ...
Similar publications
Anuran amphibians are a key group when assessing diversity patterns in Amazonia. Of the many different habitat types in this region exploited by anurans, floating meadows have received little attention. These are semi-anchored, thick plant mats on the surface of water bodies. We characterize the diversity of anuran communities encountered in this h...
Two sympatric species of aquatic frogs (Pipa pipa and Pipa snethlageae) are reported for the first time for the
Bita and Orinoco rivers in the moriche palm swamp streams of the floodplain, in the department of Vichada,
Colombia. Updated maps are provided with the extension of the range of these two species, comments on their taxonomy and some aspec...
A developmental series of nearly 250 tadpoles of Shomronella jordanica from the Early Cretaceous (Hautetivian) of the Shomron (Samaria) region of central Israel, a small collection (12) of Thoraciliacus rostriceps tadpoles from the Early Cretaceous (Aptian) of Makhtesh Ramon, Israel, and 13 tadpoles from the Late Cretaceous (Campanian/Maastrichtian...
Within the already peculiar Bauplan of anurans, pipid frogs have evolved an array of bizarre features that are commonly linked to their highly aquatic lifestyle. Among the latter, there are several distinctive sacro-caudo-pelvic features shared by extant pipids, which have been regarded as evolutionary novelties taking part of a specialized fore-af...
Citations
... Among tetrapods, few animal lineages have developed suction as a form of underwater feeding, a characteristic that evolved in association with secondary events of recolonization of water (Wainwright et al. 2015 ;Barrionuevo 2016 ;Molnar et al. 2022 ). Among animals that have acquired this behavior are several lin-eages of frogs, salamanders, (although in some amphibian lineages suction feeding is a plesiomorphic trait), and turtles (Deban and Wake 2000 ;Nishikawa 2000 ;Deban 2003 ;Barrionuevo 2016 ;Lautenschlager et al. 2018 ); and some birds and mammals (e.g., flamingos and whales; Wainwright et al. 2015 ). ...
... Among tetrapods, few animal lineages have developed suction as a form of underwater feeding, a characteristic that evolved in association with secondary events of recolonization of water (Wainwright et al. 2015 ;Barrionuevo 2016 ;Molnar et al. 2022 ). Among animals that have acquired this behavior are several lin-eages of frogs, salamanders, (although in some amphibian lineages suction feeding is a plesiomorphic trait), and turtles (Deban and Wake 2000 ;Nishikawa 2000 ;Deban 2003 ;Barrionuevo 2016 ;Lautenschlager et al. 2018 ); and some birds and mammals (e.g., flamingos and whales; Wainwright et al. 2015 ). In amphibians, this ability appeared recurrently in over a dozen lineages that, while not sharing a direct common ancestor (Barrionuevo 2016 ), display correlated convergent morphological features, such as a highly ossified hyoid apparatus and loss or reduction of the tongue (Nishikawa 2000 ;Deban 2003 ). ...
... Among animals that have acquired this behavior are several lin-eages of frogs, salamanders, (although in some amphibian lineages suction feeding is a plesiomorphic trait), and turtles (Deban and Wake 2000 ;Nishikawa 2000 ;Deban 2003 ;Barrionuevo 2016 ;Lautenschlager et al. 2018 ); and some birds and mammals (e.g., flamingos and whales; Wainwright et al. 2015 ). In amphibians, this ability appeared recurrently in over a dozen lineages that, while not sharing a direct common ancestor (Barrionuevo 2016 ), display correlated convergent morphological features, such as a highly ossified hyoid apparatus and loss or reduction of the tongue (Nishikawa 2000 ;Deban 2003 ). ...
Synopsis
The hyoid apparatus of tetrapods is highly diverse in its morphology. It plays an important role in feeding, breathing, sound production, and various other behaviors. Among turtles, the diversity of the hyoid apparatus has been recurrently linked to their habitat. The ossification of the hyoid corpus is often the main trait used in correlations with “niche” occupancy, an ossified corpus being associated with aquatic environments and a cartilaginous corpus with terrestrial life. Most studies conducted so far have focused on species belonging to Testudinoidea, the clade that occupies the biggest diversity of habitats (i.e., terrestrial, semi-terrestrial, and aquatic animals), while other turtle lineages have been largely understudied. We assessed the adult anatomy of the hyoid apparatus of 92 turtle species from all “families”, together with ossification sequences from embryological series of 11 species, some described for the first time here. Using nearly 40 different discrete anatomical characters, we discuss the evolutionary patterns and the biological significance of morphological transformations in the turtle hyoid elements. Morphological changes are strongly associated to feeding modes, with several instances of convergent evolution within and outside the Testudines clade, and are not as strongly connected to habitat as previously thought. Some of the hyoid character states we describe are diagnostic of specific turtle clades, thus providing phylogenetically relevant information.
... All prey items were presented clean. Filming was done in terrestrial settings, with exception for Lepidobatrachus species, which were filmed both on land and underwater due to their postmetamorphic ecology (Barrionuevo, 2016;Nishikawa, 2000;O'Reilly et al., 2002). Feeding trials were recorded with a highspeed video camera (FASTEC IMAGING,Model: TS5;Fastec Imaging Corp.) at 400-1000 frames per second, and scaling factors were provided using background grids. ...
... While the majority of anurans primarily feed on land, some forage in water (see Barrionuevo, 2016;O'Reilly et al., 2002). These species employ various mechanisms for prey capture, including forearm scooping, ram feeding, jaw prehension, or suction (Barrionuevo, 2016). ...
... While the majority of anurans primarily feed on land, some forage in water (see Barrionuevo, 2016;O'Reilly et al., 2002). These species employ various mechanisms for prey capture, including forearm scooping, ram feeding, jaw prehension, or suction (Barrionuevo, 2016). Intriguingly, the use of forelimbs, particularly scooping, for capturing and transporting prey to the mouth in water appears to represent an ancestral behavior, with tongue protrusion, jaw bending, and head flexion evolving for terrestrial feeding (Nishikawa, 2000). ...
Horned frogs, members of the Ceratophryidae family, encompass a group of anurans varying in size and behavior, yet unified by morphological and behavioral traits enabling them to adopt a megalophagous diet (i.e., large prey feeding). Although the group has been the focus of numerous studies, our understanding of its feeding behavior remains limited. In this study, we characterize the feeding mechanism in five species representing the three extant genera of ceratophryid anurans, both in terrestrial and aquatic environments. We also explore the ability of Chacophrys pierottii to adjust feeding behavior based on prey type. Our findings show that all species are capable of wide mouth opening, displaying an asymmetric feeding cycle. While tongue usage is the primary method for capturing prey on land, ceratophryids may use their forelimbs to manipulate prey into their mouths, exhibiting different behavioral patterns. C. pierottii shows modulation of its feeding kinematics and is also capable of some modulation of its feeding in response to prey properties.
... Whereas tongue projection mechanisms have been extensively studied, the adhesive mechanism of the tongue has received less attention. Recently, several studies have reported on the adhesive properties given by the interaction of tongue surface microstructure and the secreted mucus (Kleinteich and Gorb, 2014, 2015, 2016Noel et al., 2017;Noel and Hu, 2018). The dorsal surface of the tongue in anurans is characterized by fungiform and filiform papillae, which are covered with mucus secreted by specific cells (Iwasaki, 2002;Nalavade and Varute, 1971;Waller, 1849;Zylberberg, 1977). ...
... Although pipid frogs are recognized for their suction feeding behavior (Carreño and Nishikawa, 2010;Dean, 2003), this mode of feeding was previously unknown in Neobatrachia (O'Reilly et al., 2002), the clade that includes 96% of all extant species of toads and frogs. The revelation came with the description of suction feeding in the neobatrachian frogs of the genus Telmatobius (Barrionuevo, 2016). This Andean genus comprises semiaquatic species generally distributed in mid elevation areas and species that have acquired a secondarily aquatic mode of life in the higher elevation habitats of the Andes. ...
... The strictly aquatic T. rubigo perform suction feeding, where the tongue plays no direct role. In contrast, the semiaquatic T. oxycephalus relies on its hands to capture aquatic prey due to its inability to perform suction and, in land, captures terrestrial prey using its tongue, as most anurans (Barrionuevo, 2016). ...
The evolution of the tongue in tetrapods is associated with feeding in the terrestrial environment. This study analyzes the tongue morphology of two closely related frog species, Telmatobius oxycephalus and T. rubigo, which exhibit contrasting feeding mechanisms. Telmatobius oxycephalus, a semi-aquatic species, relies on its tongue to capture terrestrial prey whereas T. rubigo, a secondarily aquatic species, uses suction feeding not involving the tongue. Through anatomical, histological and scanning electron microscopy analyses, we revealed remarkable differences in tongue morphology between these species. Telmatobius oxycephalus exhibits a well-developed tongue whose dorsal epithelium has numerous and slender filiform papillae. The epithelial cells of the papillae are protruded and have a complex array of microridges. In contrast, T. rubigo possesses a reduced tongue with flat and less numerous filiform papillae. The epithelial cells are completely flat and lack microridges. These findings highlight the remarkable adaptability of lingual morphology in Telmatobius to respond to the contrasting ecological niches and prey capture mechanisms. This study sheds light on the relationship between tongue shape and the different functional demands, contributing to our understanding of the evolution of prey capture mechanisms in amphibians.
... Anurans exhibit a variety of diets, wich are strongly influencied by microhabitats (Moen 2019;Paluh et al. 2020), prey availability, body size, ontogeny, foraging strategies, and even by ancestral-descendant relationship (Pacheco et al. 2017;Bayrakcı & Çiçek 2022). For example, some high mountain aquatic species of the Andes, due to their lifestyle, are considered aquatic specialists (e.g., some species of Telmatobius Wiegmann, 1834; [Barrionuevo 2016;Araos et al. 2022]). On the other hand, species in the forest environment tend to be generalists and/or opportunists (Vidal-García & Keogh 2017;Paluh et al. 2020). ...
ABSTRACT
Computed microtomography is an important tool for understanding the natural history of species using
biological collections. Here we report the first dietary data of Alsodes cantillanensis Charrier, Correa,
Castro & Méndez, 2015. Using this technique, we found remains of Diplopoda and Coleoptera in the
digestive tract of a male from the type locality, providing valuable information on the ecology of the
species. These findings may be useful for designing conservation strategies for this endangered species.
Keywords: Alsodes, biological collection, computed microtomography, diet, ecology.
RESUMEN
La microtomografía computarizada es una herramienta importante para comprender la historia natural
de las especies utilizando colecciones biológicas. Aquí reportamos los primeros datos de dieta de Alsodes
cantillanensis Charrier, Correa, Castro & Méndez, 2015. Usando esta técnica, encontramos restos de
Diplopoda y Coleoptera en el tracto digestivo de un macho de la localidad tipo, proporcionando valiosa
información sobre la ecología de la especie. Estos hallazgos pueden ser útiles para diseñar estrategias
de conservación para esta especie en peligro de extinción.
Palabras clave: Alsodes, colección biológica, dieta, ecología, microtomografía computarizada.
... Another indirect effect of water acidification and metal pollution is through the trophic chains, affecting the species composition of aquatic invertebrate communities(Tripole, Vallania & Corigliano, 2008;Alvial et al., 2013), on which the frogs' diet depends (Akmentins & Gast on, 2020; Gast on, Salica & Akmentins, 2022). Since T. rubigo feeds by suspension or inertial suction(Barrionuevo, 2016), lives in alkaline fresh waters, and reproduces during both seasons (Gast on, 2022), the AMD would be a considerable threat to the survival of their populations, with pollutants entering the body through ingestion or skin absorption. A more detailed study is essential to assess the state of conservation of T. rubigo populations closest to Pan de Azúcar, and other mines granted or to be granted. ...
The aquatic Andean frogs of genus Telmatobius are one of the most threatened amphibian taxa, with many species having suffered drastic declines and even possible extinction. The Laguna de los Pozuelos' rusted frog Telmatobius rubigo is a fully aquatic species that inhabits lotic systems in the Argentinean vertex of the Lithium Triangle of South America.
This study estimated the environmental suitability of an area and geographical distribution of T. rubigo through an ecological niche model. This study also aimed to assess the possible extent of impacts related to mining operations on this threatened species.
The ecological niche model of T. rubigo was obtained using specific freshwater habitat variables and the MaxEnt algorithm. The possible extent of impacts related to mining operations was evaluated by overlaying the mining tenure and the estimated distribution of T. rubigo resulting from the model.
According to the ecological niche models, T. rubigo could occupy 2,001 km ² in four Argentine basins and three hydrographical units of southern Bolivia and is unlikely to occur in northern Chile. Five environmental variables had the highest contribution to the best selected model: shrub coverture, soil pH, soil organic carbon, and two variables related to the upstream air temperature. The suitable area for T. rubigo overlaps with mining operations by 61.8%.
We advise the local communities, governmental environmental agencies, mining companies, and environmental assessors to consider the presence of threatened Telmatobius species in areas subject to mining to protect them and their environment. We encourage incorporating the aquatic Andean frogs as key species into management, environmental monitoring, and remediation plans.
... All other non-pipid suction feeding frogs such as Telmatobius rubigo (Barrionuevo, 2016), possibly Lankanectes corrugatus (Pethiyagoda et al., 2014), Lepidobatrachus laevis and L. llanensis (Fabrezi & Lobo, 2009) and Calyptocephalella gayi (Wiesinger, 2017;Kunisch et al., 2021) have, at least, a broadened hyoid apparatus with heavier musculature when compared to more generalized frogs. On the other hand, enlarged hyoids are also encountered in the Discoglossidae and Bombinatoridae (see Trewavas, 1933), but their aquatic feeding habits have not yet been studied in detail. ...
... Apart from studies of the pipids, there are just two investigations about aquatic feeding frogs within the Neobatrachia: Lankanectes corrugatus (Pethiyagoda et al., 2014) and Telmatobius rubigo (Barrionuevo, 2016). Data on a third species, Calyptocephalella gayi, are not yet published. ...
... A further variation shown by the aquatic species is a wide gape, opening up to 90°, but no obvious mandibular bending. Barrionuevo (2016) compared the hyoid apparatus and tongue morphology of these species and revealed a greater level of ossification of the hyoid plate in the aquatic T. rubigo, and broader insertion areas of the sternohyoid muscle, which serves as a hyoid retractor. The tongue of the predominantly terrestrial species was broader and thicker and showed some surface structures. ...
Modern amphibians are referred to as Lissamphibia and comprise the three extant groups: Anura (frogs and toads), Caudata (salamanders and newts) and Gymnophiona (caecilians). From a phylogenetic point of view, lissamphibians are considered the sister taxon of extant amniotes (sauropsids and mammals). Lissamphibians have a long evolutionary history, reaching back into the Late Paleozoic and most probably originated within a temnospondyl clade. One of the most conspicuous features of lissamphibians is their aquatic larval stage. Many lissamphibians have, however, secondarily reduced the free-living larval stage and are direct developers. Direct development is a secondary feature and might be seen as an adaptation to terrestrial life. Given that the aquatic larval stage is the ancestral condition for lissamphibians, adaptations to aquatic feeding might also be seen to be the ancestral condition, at least for lissamphibian larvae. After metamorphosis, some lissamphibians become terrestrial, others adopt a semiterrestrial/semiaquatic lifestyle, while others remain fully aquatic. Accordingly, although in many lissamphibian cases the secondary nature of aquatic adaptations might be obvious, a strict distinction between secondary and primary adaptations is less clear in others. Examples of secondarily aquatic lissamphibians are aquatic frogs and toads, as well as some desmognathid salamanders that have definitely reinvaded aquatic trophic habitats during their evolutionary history. In contrast, some salamandrid and ambystomatid salamanders continuously switch between aquatic and terrestrial lifestyles after metamorphosis and it is not obvious whether their (semi)aquatic lifestyle is retained from their larval condition (i.e. primary) or has evolved de novo. In fact, many adaptations to aquatic feeding in lissamphibians might represent a combination of both primary and secondary features, defying a strict dichotomy. In this chapter we summarize aquatic feeding strategies in all three extant groups of lissamphibians and highlight homologous and convergent features where appropriate.
... Por otro lado, los contenidos estomacales de T. atacamensis presentaron frecuentemente restos minerales y vegetales. Si bien la información respecto a los hábitos alimenticios del género es escasa, Barrionuevo (2016) describe los mecanismos de alimentación de T. oxycephalus y T. rubigo, dos especies que representan los modos de vida predominantes en el género, siendo esta última muy similar a T. atacamensis. En su trabajo reportó que T. rubigo tiene un mecanismo de alimentación similar a los Pípidos, de succión inercial. ...
... En su trabajo reportó que T. rubigo tiene un mecanismo de alimentación similar a los Pípidos, de succión inercial. Ya que ambas especies habitan la región puneña y son de hábitos exclusivamente acuáticos (Barrionuevo 2016) podría explicarse la presencia de estos elementos por un consumo accidental en el momento de captura y por la búsqueda de alimento en el fondo de los ríos. La presencia de elementos no nutritivos, como restos vegetales y arena en los estómagos también fue reportado en la dieta de T. rubigo (Akmentins y Gastón 2020). ...
Telmatobius atacamensis, anuro microendémico de la Puna salteña, tiene hábitos exclusivamente acuáticos. Está categorizado como especie en peligro crítico a nivel global y como amenazada a nivel nacional. El conocimiento de la ecología trófica es útil para mejorar manejo y conservación de una especie y, debido a que esta información es escasa, el objetivo fue describir y analizar su dieta. Mediante la técnica de lavado estomacal se obtuvieron 37 contenidos de individuos recolectados en los ríos San Antonio y Los Patos durante un ciclo anual (2018), una vez al mes. Se registraron 724 presas, pertenecientes a diez órdenes; dípteros, coleópteros y hemípteros fueron los más importantes. No hubo correlación significativa entre el tamaño depredador-presa. Tampoco hubo diferencias significativas entre hembras, machos y juveniles y el número y volumen de presas consumidas. El índice de diversidad de la dieta fue de 1,05 y la amplitud del nicho trófico estandarizado fue de 0,09. La superposición de nicho entre las categorías fue de Ojk = 0,80. De acuerdo con el índice de similitud de Jaccard, las dietas de hembras y juveniles fueron más semejantes (71 %). Presentaron una predominancia al consumo de invertebrados de hábitos bentónicos y, si bien se encontraron presas de hábitos terrestres, podría deberse a un consumo accidental. Este consumo desproporcionado de fauna bentónica estaría directamente relacionado con los hábitos de vida de la especie. Por otro lado, la composición de la dieta no varía significativamente entre las categorías consideradas, sin registrar diferencias en la cantidad y volumen de presas.
... Although the articulation was already described by Pregill (1981, as mention any related foramen. No muscles-neither adductor mandibulae, depressor mandibulae nor hyoid musculature-are expected to go through this opening (e.g., Limeses, 1965;Starrett, 1968;Carroll & Holmes, 1980;Barrionuevo, 2016;Roček et al., 2016;Kunisch et al., 2021). ...
In the present paper, we report new anuran remains recovered from strata referred to the Adamantina Formation (Upper Cretaceous) cropping out near Catanduva city, São Paulo, Brazil. The remains represent two individuals, one of which bears a set of peculiar characteristics, both cranial and postcranial, that allows us to assign them to the already known genus Baurubatrachus. To date, the genus was only represented by the holotype of Baurubatrachus pricei, recovered from the Upper Cretaceous Serra da Galga Formation (which is younger than the Adamantina Formation), near Peirópolis (Minas Gerais, Brazil), 200 km north of Catanduva City. The lesser ossification as well as the slender configuration of the scapula and ilia of the new remains, relative to B. pricei, points to the identification of a new species, Baurubatrachus santosdoroi sp. nov. The detailed study of the peculiar anatomy of these specimens provides new osteological features for the genus, such as the presence of a subtympanic foramen, as well as new character states for other traits to be considered in future systematic studies.
El presente trabajo reporta nuevos restos de anuros hallados en estratos referidos a la Formación Adamantina (Cretácico Superior) aflorantes en las proximidades de la ciudad de Catanduva, San Pablo, Brasil. Los restos representan dos individuos, uno de ellos portador de una cantidad de características particulares, cranianas y postcranianas que permite asignarlo al género ya conocido Baurubatrachus. Hasta la fecha, el género estaba únicamente representado por el holotipo de Baurubatrachus pricei, recuperado de la Formación Serra da Galga del Cretácico Superior (que es más joven que la Formación Adamantina), cerca de la ciudad de Peirópolis (Minas Gerais, Brasil), 200 km al norte de la ciudad de Catanduva. La menor osificación, así como la condición más esbelta de las cinturas pectoral y pélvica de estos restos respecto de B. pricei, indica la presencia de una especie diferente, Baurubatrachus santosdoroi sp. nov. El estudio detallado de la anatomía particular de estos especímenes permitió identificar nuevos caracteres como la presencia de un foramen subtimpánico y, a su vez, nuevos estados de carácter para otras características, las cuales son plausibles de ser utilizadas en futuros estudios sistemáticos.
... The Rusted Frog Telmatobius rubigo Barrionuevo & Baldo 2009 is a fully aquatic frog endemic to the endorheic basin of the Laguna de Los Pozuelos in the Central Andean Puna ecoregion of Jujuy province in Argentina (Barrionuevo & Baldo, 2009), at 3,500 -4,300 m a.s.l. This frog has a unique feeding mechanism among Neobatrachia, using inertial suction to capture their prey (Barrionuevo, 2016), mainly aquatic coleopterans, insects, and crustaceans (Akmentins & Gastón, 2020). It appears that the larval period in T. rubigo lasts more than a year, given the simultaneous occurrence of different larval stages in the same site and the low temperatures of the high mountain permanent streams inhabited by the species (Barrionuevo, 2018). ...
The genus Telmatobius (Anura: Telmatobiidae) includes 63 species of aquatic and semiaquatic frogs associated with high Andean ecosystems and distributed from Ecuador to Chile and Argentina. Telmatobius frogs were used by the Inca culture as symbols to propitiate rainfall and fertility, possibly due to frogs’ conspicuous reproductive biology. Despite this, there is little information about the reproduction of these Andean water frogs. The present study showed that the rusted frog Telmatobius rubigo has axillary amplexus and breeds during the wet and dry seasons. The species seems to conform to reproductive mode 16, in that it lays eggs on the bottom of fast-moving fresh water and has free-living tadpoles that feed on nutrients in their environment without parental support. The difference in clutch sizes reported for the species suggests consecutive laying events of small egg masses (~ 30 eggs) that could eventually result in an egg mass of ~ 400 eggs. If spawning occurs at the same place, then embryos at different development stages would be found in a clutch consistent with the data presented here for T. rubigo. Further studies are needed to unveil other reproductive aspects of T. rubigo, such as parental care behaviour that has been suggested by the association of males with the clutches. The effect that increasingly frequent extreme climatic events have on the biology of the threatened frog T. rubigo needs to be thoroughly studied. Knowing how reproductive behaviour can be affected by climate change and other human-related threats is crucial for developing conservation strategies for the species.
... Adult aquatic feeding frogs generally use modifications of terrestrial mechanisms, such as lunging at their prey and ingestion by jaw prehension. Only a few species of pipids and Telmatobius have re-evolved suction feeding (Barrionuevo, 2016;Carreño & Nishikawa, 2010;Cundall et al., 2017;O'Reilly et al., 2002). The only extant species of the genus Calyptocephalella, C. gayi, shows a fully aquatic lifestyle-although being able to feed in terrestrial environment-and also seems to use suction feeding (Wiesinger, 2017). ...
... While the hyoid apparatus has a limited function in lingual prehension in anurans (Gans & Gorniak, 1982), it is indispensable for suction feeding (see Lauder, 1985;Lauder & Shaffer, 1993). Concerning hyoid and tongue dimensions, aquatic and terrestrial species show an inverse relationship in tetrapods with aquatic ones generally possessing large hyoids and less developed tongues, while the opposite is the case for terrestrial ones (Barrionuevo, 2016;Bramble & Wake, 1985;Lemell et al., 2000Lemell et al., , 2002. This probably also applies to C. gayi and L. pentadactylus, as the former does indeed have a broader hyoid and a smaller tongue. ...
... The MDM of the aquatic C. gayi has a more fanlike shape with a broader area of origin at the scapula, resulting in longer posterior fibres. This pattern was also described in aquatic and semiaquatic species of Telmatobius (Barrionuevo, 2016). In contrast, the MDM of L. pentadactylus is rather compact and oriented in a more vertical direction. ...
Micro-computed tomography (microCT) of small animals has led to a more detailed and more accurate three-dimensional (3D) view on different anatomical structures in the last years. Here, we present the cranial anatomy of two frog species providing descriptions of bone structures and soft tissues of the feeding apparatus with comments to possible relations to habitat and feeding ecology. Calyptocephalella gayi, known for its aquatic lifestyle, is not restricted to aquatic feeding but also feeds terrestrially using lingual prehension. This called for a detailed investigation of the morphology of its feeding apparatus and a comparison to a fully terrestrial species that is known to feed by lingual prehension such as Leptodactylus pentadactylus. These two frog species are of similar size, feed on similar diet but within different main habitats. MicroCT scans of both species were conducted in order to reconstruct the complete anatomical condition of the whole feeding apparatus for the first time. Differences in this regard are evident in the tongue musculature, which in L. pentadactylus is more massively built and with a broader interdigitating area of the two main muscles, the protractor musculus genioglossus and the retractor musculus hyoglossus. In contrast, the hyoid retractor (m. sternohyoideus) is more massive in the aquatic species C. gayi. Moreover, due to the different skull morphology, the origins of two of the five musculi adductores vary between the species. This study brings new insights into the relation of the anatomy of the feeding apparatus to the preferred feeding method via 3D imaging techniques. Contrary to the terrestrially feeding L. pentadactylus, the skeletal and muscular adaptations of the aquatic species C. gayi provide a clear picture of necessities prescribed by the habitat. Nevertheless, by keeping a certain amount of flexibility of the design of its feeding apparatus, C. gayi is able to employ various methods of feeding.
