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The Sri Lankan torrent toads (Bufonidae: Adenominae: Adenomus): Species boundaries assessed using multiple criteria
Abstract and Figures
The bufonid genus Adenomus, an endemic of the montane and lowland rainforests of central and south-western Sri Lanka, has been considered to comprise of three species, viz. A. kelaartii, A. dasi and A. kandianus, the last of which has been recently highlighted as " the world's rarest toad " . We conducted a survey across the known range of Adenomus and used multiple criteria to delineate species boundaries within the genus. These include: a molecular phylogeny based on a 16S ribosomal RNA gene fragment; an examination of the external morphology of adults and larvae, and the skeletal morphol-ogy of adults; a bioacoustic analysis; and ecological niche modelling. We show that Adenomus is monophyletic and that it comprises only two species: A. kelaartii and A. kandianus, with A. dasi being a junior synonym of the latter. For the two valid species of Adenomus, we provide detailed osteological descriptions; clarify the distribution patterns; and provide genetic data to facilitate their scientific conservation management.
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... For higher-level taxonomy, we followed Frost et al. (2006) and in species taxonomy the following literature were used: Frost et al. (2006), Manamendra-Arachchi and Pethiyagoda (2006), Fernando et al. (2007), Joshy et al. (2009), Li et al. (2013), Biju et al. (2014), Khajeh et al. (2014), Meegaskumbura et al. (2015), Oliver et al. (2015), Peloso et al. (2016), Wijayathilaka et al. (2016), Garg et al. (2018), Sanchez et al. (2018), Batuwita et al. (2019b), and Chandramouli et al. (2019). The conservation statuses of species were taken from the following published sources: Fernando et al. (2007); IUCN (1999;2007;; Manamendra-Arachchi and Pethiyagoda (2006); Wickramasinghe et al. (2013b;; and Batuwita et al. (2019b). ...
... Subsequently, Van Bocxlaer et al. (2009) showed that Bufo atukoralei, B. kotagamai and B. scaber are in fact members of Duttaphrynus. Apart from the above mentioned species, two other species from the family Bufonidae exist and they belong to an endemic genus Adenomus, sc., A. kelaartii and A. kandianus (Wickramasinghe et al., 2012b;Meegaskumbura et al., 2015). Until Wickramasinghe et al. (2012b) rediscovered the latter species, it was considered as an extinct species (Manamendra-Arachchi and . ...
... Until Wickramasinghe et al. (2012b) rediscovered the latter species, it was considered as an extinct species (Manamendra-Arachchi and . Moreover, Meegaskumbura et al. (2015) showed that previously described Adenomus dasi Manamendra-Arachchi and Pethiyagoda, 1998 is a new junior synonym of A. kandianus. Also, recent studies revealed that Duttaphrynus atukoralei is conspecific with D. scaber and the population that inhabits the Lowland Wet Zone ( Pethiyagoda, 2006) and has recently been assigned to M. syhadrensis (Annandale, 1919), but now it is known as M. agricola (Sanchez et al., 2018;Chandramouli et al., 2019). ...
The amphibian fauna of Sri Lanka comprises 120 species, including 107 (~90.0%) endemic species. They belong to five families: Bufonidae, Dicroglossidae, Ichthyophiidae, Microhylidae, and Rhacophoridae. Based on distribution, we recognized five zoogeographic zones for them, Central Hills, Dry Zone, Knuckles Range, Lowland Wet Zone, and Rakwana Hills. Fifty three species were reported from the Central Hills (48 endemics [90.6%] and 42 [79.2%] threatened species). 47 species were recorded from the Lowland Wet Zone, including 36 (76.6%) endemics and 28 (59.6%) threatened species. The Knuckles Range had 25 species, of which, 19 (76.0%) were endemics and 15 (60.0%) are threatened species. 19 species were reported from Dry Zone including seven endemics (36.8%) and four threatened species (21.1%). Out of 29 species, which inhabited in the Rakwana Hills, 26 were endemics (~89.7%) including 24 (82.8%) threatened species. Species diversity along the elevational gradient was also observed with the highest species richness in the mid-elevational localities. Family Ichthyophiidae can be considered as the least studied family. Recent rediscoveries and studies have helped to reduce the number of extinct species from 21 to 18. It is speculated that some of the other extinct species have to be rediscovered or probably were misidentified as other species. About 90% of Sri Lankan amphibians occur in the regions with the highest human populations where there are established agricultural lands. Loss of habitats, competition due to anthropogenic species and invasive species, pollution (cause for malformations, parasites, and other diseases), and climate change appear to be major threats.
... Since 2012, 13 new species of amphibians have been added to the species list by Wickramasinghe et al. (2013), Biju et al. (2014), Meegaskumbura et al. (2015), Wickramasinghe et al. (2015), Wijayathilaka et al. (2016), Jayawardena et al. (2017), Garg et al. (2018), and Senevirathne et al. (2018). All of these are endemic to Sri Lanka. ...
... As a result of some taxonomic revisions to this group by Biju et al. (2014), Meegaskumbura et al. (2015), Wijayathilaka et al. (2016), Jayawardena et al. (2017, and Garg et al. (2018), five species of amphibians were removed from the recent list of amphibians. These are Adenomus dasi, Duttaphrynus atukoralei, Hylarana aurantiaca, Microhyla rubra, and Ramanella variegata. ...
Sri Lanka’s location, historic and geologic isolation from the continental landmass, topography and climate act to shape its biogeography and biodiversity, including conferring a remarkably high level of endemism, given its close proximity to the mainland.
The island hosts several ‘point endemic1 species and even monotypic endemic genera. However this irreplaceable biodiversity is now under severe threat because of extensive anthropogenic landuse changes that began over two centuries ago, under colonial rule, and continues to this present date. Due to high levels of endemism, extensive loss
and degradation of natural ecosystem, Sri Lanka has been identified as one of the 36 global biodiversity hotspots.
... Sequences were assembled in 4peaks v.1.7.1. Subsequently, the sequences of the new population were compared against a dataset consisting of Adenomus kanidanus and A. kelaartii obtained from Meegaskumbura et al. (2015). Sequences were aligned using ClustalW as implemented in MEGA 5.0 (Tamura et al. 2011). ...
... Often, females occupy a different habitat from that of males to prevent premature amplexus, to reduce stress and to avoid competition for food. This suggests that, larger-bodied females (Meegaskumbura et al. 2015) probably wander far from the breeding streams, foraging to build up energy reserves to produce their substantial clutches of eggs and to undergo the strenuous torrent diving activity, while the smallerbodied males live in forested riparian habitats, awaiting a chance to mate. ...
Endemic to Sri Lanka, genus Adenomus contains two torrent-associated toad species whose ecology and natural history in the wild is virtually unknown. Adenomus kelaartii is relatively common, with a wide geographic distribution. Its sister species, A. kandianus , however, is restricted to two isolated populations in fast-disappearing montane and sub-montane forests. Formally declared extinct after not being recorded for over a century, following several years of surveying, a few A. kandianus were found in 2012 and referred to as "the world's rarest toad." However, tadpoles of A. kandianus bearing unique ventral suckers were soon discovered, but the rarity of the adult and the profusion of tadpoles were never explained. Here, using ecological methods, niche modeling and DNA-barcoding, we aim to understand the ecology, natural history and distribution of this rare toad. Following a two-year study of occurrence, habits and habitat associations of adults and larvae, we show this to be a secretive species with a patchy distribution. During non-mating periods female toads ( N = 23) were found in primary forests habitat up to 650 m away from the breeding streams, and predominantly males in the riparian zone (12 males, 2 females). Following heavy rain they form large ( N = 388) but patchy mating congregations in torrential streams (six sites; range 0−95 mating pairs; mean = 25, SD = 38.16, CV = 152%). Amplexed pairs swim synchronously, enabling them to traverse fast currents. Egg-laying sites remain unknown, but ability to dive, vocalize underwater, and characteristics of the eggs, suggests that they lay eggs in dark recesses of the stream. Quadrat sampling of tadpoles show microhabitat partitioning (in depth, flow-rate and substrate conditions) within the stream: the greatest diversity of larval developmental stages (25-42) in slow-flowing (depth, 0.75−1.5 m) rocky areas; more robust stages (31−39) bearing sucker discs utilise rocky-rapids (depth, 0.25−0.75 m); metamorphic stages (43-45) use stream margins (depth, <0.25 m); slow flowing silt covered areas of the stream were unoccupied, irrespective of the depth. DNA barcoding of the 16S rRNA gene fragment from the two known localities confirms the identity of the Pedro population also as A. kandianus . The uncorrected pairwise genetic distance of 0.1−0.7% suggests historical gene flow between the two populations. Distribution modeling (using MaxEnt), with forest-cover layers added, predicts a very small remaining area of suitable habitats (an area of occupancy of 16 km ² and an extent of occurrence of 128 km ² ) isolated by habitats that are not conducive to these toads. While the healthy population recorded at one site gives hope for the survival of the species, long-term conservation of this climatically and ecologically restricted species hinges largely on the preservation of cloud and riparian forests and the unpolluted high-flow torrents.
... Suctorial and gastromyzophorous larvae evolved independently at least 10 times in Bufonidae (Fig. 16). Gastromyzophorous tadpoles have been reported in all known Atelopus larvae, in three species of the Rhinella veraguensis group (R. chrysophora, R. quechua, and R. veraguensis), in Sabahphrynus maculatus, in Adenomus kandianus, and in Bufo aspinius [33,60,[145][146][147], whereas suctorial tadpoles have evolved in Adhaerobufo gen. nov., Ansonia, Blaira, Phrynoidis, Bufo pageoti, Bufo torrenticola, Bufo tuberospinus, and Werneria ( [66,[148][149][150][151]; the present study). ...
Tadpoles serve as crucial evidence for testing systematic and taxonomic hypotheses. Suctorial tadpoles collected in Guyana were initially assigned to Rhaebo nasicus through molecular phylogeny. Subsequent analysis of larval and adult morphological traits revealed synapomorphies within the clade encompassing R. nasicus and R. ceratophrys, prompting the recognition of a new genus described herein as Adhaerobufo. The new genus is distinguished from other bufonids by specific phenotypic traits including an enlarged, suctorial oral disc with distinct papillae arrangements, and the presence of certain muscles and narial vacuities at the larval stage. However, only a few adult external characteristics (e.g., enlarged eyelids, infraocular cream spot), seem to be reliably discriminative from related genera. This study underscores the significance of larval morphology in anuran systematics and offers new insights into the evolution of suctorial and gastromyzophorous larvae within bufonids.
... Gastromyzophorous tadpoles have been reported in Amolops, Huia, Meristogenys, Sumaterana, Wijayarana, and Rana sauteri-(e.g. Kuramoto et al. 1984;Arifin et al. 2021); in three species of the Rhinella veraguensis group (R. chrysophora, R. quechua, and R. veraguensis), in Sabahphrynus maculatus, in Adenomus kandianus, and in Bufo aspinius (Rao and Yang 1994;Matsui et al. 2007;Aguayo et al. 2009;Meegaskumbura et al. 2015); finally, the hylid Phyllodytes gyrinaethes is also gastromyzophorous (Peixoto et al. 2003;Vera Candioti et al. 2017). ...
The Neotropical genus Atelopus is the most diverse genus of bufonids comprising 99 species. Tadpoles of these frogs are
readily distinguished based on the presence of a belly sucker, used by them to stay attached to rocks in fast-flowing streams.
Despite their intriguing biology, information about their anatomy is scarce and many morphological systems are unknown.
We describe the buccopharyngeal cavity of five Atelopus species. The Atelopus buccopharyngeal cavity is characterized by
(1) presence of a pendulum-like papillae in the prenarial arena, (2) presence of a glandular zone in the prenarial arena, (3)
narial vacuities, (4) conical median ridge, (5) absence of buccal roof arena papillae, (6) absence of buccal roof pustulations,
(7) single pair of infralabial papillae, (8) absence of lingual papillae, and (9) absence of pustulations in the buccal floor. We
propose that characters 1, 2, and 3 are new synapomorphies for the genus. We also propose that the presence of a single pair
of infralabial papillae is a synapomorphy for bufonid. Finally, we discuss the convergent evolution of gastromyzophorous
and suctorial tadpoles withing anurans.
... More than 65% of known genera of bufonids have information on larval morphology, showing high phenotypic and ecological diversity (e.g., Duellman and Lynch 1969;Lamotte and Xavier 1972;Müller et al. 2005;Haas et al. 2009;Meegaskumbura et al. 2015;Viertel and Channing 2017;Müller 2019;Romero-Carvajal et al. 2023), with many larval characters presenting interesting evolutionary history and phylogenetic significance (Channing 1978;Haas 2003;Frost et al. 2006;Hirschfeld et al. 2012). Very few larval external features of Frostius pernambucensis support the notion that the species is part of the family Bufonidae, such as the eyes placed dorsally, the medial vent tube, and the sinistral spiracle (located in general below the medial line). ...
Frostius pernambucensis is a phytotelm-breeding frog with endotrophic larvae. Although the larvae were formally described, no aspect of its internal morphology is known. In this paper, we re-describe the tadpole based on a large sample, describe its internal anatomy (buccopharyngeal cavity and musculo-skeletal system), provide data on natural history, and discuss the evolution of endotrophy and phytotelma colonization. The tadpoles of F. pernambucensis are highly modified, with depressed bodies, reduced mouthparts, and long tails. Many character-states described for these tadpoles can be related to its endotrophic development. Consequence of this highly modified phenotype, we propose several novel putative synapomorphies for the genus: (1) labial tooth row formula 1/1; (2) absence of pustulation in the buccal roof and (3) floor; (4) absence of median ridge; (5) absence of lateral ridge papillae; (6) absence of secretory ridges and pores; (7) absence of filter plates; (7) m. subarcualis rectus II–IV originating on ceratobranchial III; (8) m. subarcualis rectus II–IV inserting on ceratobranchial I; (8) ventral slip of the m. subarcualis rectus I inserting on the ceratobranchial III; (9) suprarostral corpora fused to the cornua trabeculae; (10) commissura quadratoorbitalis absent; (11) cerabranchial II attached to the planum hypobranchiale; and (12) ceratobranchial III attached to the planum hypobranchiale. Finally, we also propose that the presence of a single pair of infralabial papilla could represent a synapomorphy of bufonids. The colonization of phytotelma seem to have created a selective pression on the development of F. pernambucenis, favoring the evolution of endotrophy.
... In conclusion, the multivariate analyses suggested that parotoids and the inner metatarsal tubercles are the most important morphological characteristics for distinguishing different entities. The differences in the inner metatarsal tubercle have also been used in previous studies for discriminating different Pelophylax species (Plötner et al. 2012;Domeneghetti et al. 2013), while the shape and dimension of the parotoids were used for comparing another bufonid species (Khan 2001;Maneyro et al. 2004;Das et al. 2013;Meegaskumbura et al. 2015). The above reports also confirm the usefulness of the findings of the present study. ...
The geographic range of a species is crucial for obtaining information on the exact distribution of the species. The geographic data are important for delimiting distinct species or exploring the degree of differentiation among different populations of a species. The local details of species boundaries facilitate the study of the importance of phylogeographic background, secondary contacts, and hybrid zones, along with the relations between the species and its extrinsic environmental factors. In the present study, the range boundaries of Bufo bufo and Bufo verrucosissimus in the north-eastern region of Türkiye were delineated using an integrative taxonomic approach that utilized a combination of molecular and morphological data. According to the mtDNA results of the present study, B. bufo inhabits a single distribution from İyidere town to Çayeli town in Rize, while B. verrucosissimus is distributed from Şavşat town of Artvin to Ardeşen town in Rize. In addition, the two species coexist in Pazar, Hemşin, and Çamlıhemşin towns in Rize. The demographic analyses indicated a distinct population expansion for the B. verrucosissimus species after the Last Glacial Maximum, while the same did not occur for B. bufo. The univariate and multivariate statistical analyses conducted for the morphological data of the two species corroborated the presence of a putative contact zone between B. bufo and B. verrucosissimus. In summary, the present study resolved the non-distinct geographic boundaries between B. bufo and B. verrucosissimus species and also revealed the easternmost distribution of B. bufo in Türkiye. In addition, important evidence on the putative contact zone between the two species was indicated using an integrative taxonomic approach.
... Liver tissues were used for genetic analysis. Partial sequences (to 3882 nucleotides) for the 16s rRNA gene were generated using the primers (forward primer [L02510]-CGCCTGTTTATCAAAAACAT; reverse primer [H03063]-CTCCGGTTTGAACTCAGATC ;Palumbi 1996) and compared with congeners using published 16s rRNA sequence data (Ao et al. 2003;Bocxlaer et al. 2009;Meegaskumbura et al. 2015;Portik and Papenfuss 2015; Table 2). Sequences were aligned with Mega 7 using the muscle algorithm with default parameter settings (Kumar et al. 2016). ...
First record and molecular phylogenetic f Duttaphrynus chandai from Mizoram.
Despite increased attention by molecular taxonomists, the herpetofauna of Southeast Asia still hides many undescribed species among far-ranging taxa. In this study, we reexamine the mitochondrial diversity of painted frogs of the microhylid genus Kaloula, based on ~2,455 bp of published and new 12S and 16S rRNA sequences, and describe two new species from the tropical forests of southern Vietnam and central Laos based on integrative evidence. These species, which belong to the K. baleata complex, feature species-level mitochondrial divergence (> 4.4% at 16S rRNA) and are both morphologically well-differentiated from each other and from the recently described K. indochinensis, to which they were previously confounded. Comparative examinations also indicate distinct male advertisement calls and unique coloration features. Based on genetic barcoding, we preliminarily revise the species distribution ranges in the K. baleata complex, which support a general pattern of biogeographic partitioning that has been widely retrieved among the In-dochinese amphibians studied so far. Molecular diversity within K. baleata further suggests genetic structure across Sundaland, namely three shallow mitochondrial haplogroups worthy of fine-scale phylogeographic and taxonomic investigations. Furthermore, our study highlights the propensity of amphibian species "hidden in plain sight," even among recently studied taxa, thus calling for caution when specifying type specimens-the type series of K. indochinensis, described in 2013, includes specimens of the one of the new species. Our study emphasizes the continued need for thorough herpetological surveys even in supposedly well-known parts of Indochina and sets the ground for future research in Kaloula painted frogs, notably to test evolutionary and taxonomic hypotheses with genomic loci.
The Koyna Toad, Beduka koynayensis, was described some 50 years ago as Bufo koynayensis. Due to taxonomic changes in the generic position now the species is considered under the recently established genus Beduka. Although the terrestrial toad species are morphologically cryptic and difficult to identify them based on morphological characters alone the members of Beduka are exceptions due to clear body colour patterns and habitat specificity. Even though the species is well studied in terms of reproductive biology, call pattern and life history traits there is a lacuna in the understandings of its range of distribution, morphological and genetic variations due to limited field samples available in the museums and the genetic data availability in the GenBank. Based on the fresh collections around the type locality, here we report morphological variations across the different populations within the species. With the 16S rRNA generated in the study discussions are made on the genetic variations across its range of distribution utilizing the unpublished sequences available in the GenBank
Climate change is one of the most-discussed issues in current global fora. The objective of this paper is to seek evidence for climate change in Sri Lanka by analyzing longterm (i.e. from 1869 to 2007) monthly data of air temperature and rainfall from seven selected locations (i.e. Anuradhapura, Kurunegala, Kandy, Ratnapura, Badulla, Nuwara Eliya and Colombo) representing the major climatic zones of the country. Decadal mean air temperatures of all selected locations, except Kandy, showed highly significant (p<0.001) linear increasing trends over the entire 140-year period considered. In all locations, including Kandy, almost continuous decadal warming has occurred during the last 6-10 decades. The rates of continuous warming in all locations except Ratnapura exceeded, by a substantial margin, the global mean (i.e. 0.074 °C decade⁻¹) during the period from 1906 to 2005. Analysis of frequency distributions of annual mean air temperatures showed that the above increases have occurred because of a shift in the entire distribution of temperatures over time rather than due to a few extremely warm years. Four out of the seven locations (i.e. Anuradhapura, Kandy, Badulla and Nuwara Eliya) examined showed statistically significant (p<0.05) linear declining trends of decadal mean annual rainfall (RFa) with time over the whole 140-year period. The highest rate of rainfall decline was shown in Nuwara Eliya at 52 mm decade-1. Within the respective trends over the 140-year period, a period of significant (p<0.05) decline of decadal mean RFa could be identified in all locations except Colombo. In particular, Kurunegala has shown a rainfall decline of 121 mm decade-1 from the 1970s onwards. Kandy and Nuwara Eliya have also shown rainfall declines in the range of 64-67 mm decade⁻¹ since 1940s and 1920s respectively. In all locations, mean RFa during the period from 1990 to 2007 was lower than that during the 1950-1989 period. The reductions ranged from 28 mm yr⁻¹ at Ratnapura to 202 mm yr⁻¹at Kurunegala. Analysis of shifts in rainfall distributions show that rainfall reductions in the years of extremely lower and higher rainfall have contributed relatively more to the mean rainfall reductions in successive periods than rainfall reductions in the years of average rainfall. In all locations, RFa showed decreasing trends, of varying strengths, with increasing mean annual temperature, Ta, with Nuwara Eliya showing the highest rate of rainfall decline (371 mm °C⁻¹). Analysis of monthly and annual rainfall data from 1950 to 1989 showed that the El Niño phenomenon reduced RFa during the following year in all locations, mainly because of rainfall reductions in June-July (South-West Monsoon) and January-February. From 1990 onwards, these post-El Niño RFa reductions have increased in all locations except Colombo and Ratnapura, where post-El Niño RFa has been higher than in normal years. Notably, in all locations, post-El Niño reductions of June-July rainfall have been absent since 1990, where RFa reductions have occurred because of reductions in January- February and October-December (North-East Monsoon) rainfall.
We describe the tadpoles of Ansonia hanitschi Inger, 1960 and Polypedates colletti (Boulenger, 1890) from East Malaysia, Borneo. The morphological description is supplemented by photos of living specimens and SEM images of external and internal features. Identification was based on morphological and genetic characters (16S rRNA). The tadpole of A. hanitschi is among the largest tadpoles described for the genus Ansonia from Borneo. This suctorial-rheophilous tadpole has been collected from fast-flowing rocky streams, in association with foaming currents. The tadpole of P. colletti is redescribed due to uncertainties about its identity and lack of photographic evidence in previous descriptions. It is an inhabitant of stagnant waters, living in and on flooded leaf litter accumulations. © 2008 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT).
Adenomus kandianus Günther (1872) was previously known only from two specimens both deposited in the British Museum, the holotype BMNH1947.2.20.63, and the syntype of A. kelaarti BMNH1947.2.20.62. The only record of A. kandianus since the initial description in 1872 was by Ferguson in 1876, who mentions two specimens resembling Bufo kandianus in his collection, making A. kandianus the world's rarest toad. The species had not been reported since, and was considered extinct. Here we report on its rediscovery.
The area under the receiver operating characteristic (ROC) curve, known as the AUC, is currently considered to be the standard method to assess the accuracy of predictive distribution models. It avoids the supposed subjectivity in the threshold selection process, when continuous probability derived scores are converted to a binary presence–absence variable, by summarizing overall model performance over all possible thresholds. In this manuscript we review some of the features of this measure and bring into question its reliability as a comparative measure of accuracy between model results. We do not recommend using AUC for five reasons: (1) it ignores the predicted probability values and the goodness-of-fit of the model; (2) it summarises the test performance over regions of the ROC space in which one would rarely operate; (3) it weights omission and commission errors equally; (4) it does not give information about the spatial distribution of model errors; and, most importantly, (5) the total extent to which models are carried out highly influences the rate of well-predicted absences and the AUC scores.
