Charles W. Myers

Further classification of skin alkaloids from neotropical poison frogs (Dendrobatidae), with a general survey of toxic/noxious substances in the Amphibia

Cutaneous granular glands are a shared character of adult amphibians, including caecilians, and are thought to be the source of most biologically active compounds in amphibian skin. Data are available from one or more species in over 100 of nearly 400 genera comprising the three living orders of Amphibia. Many species contain unidentified substances judged to be noxious based on predator aversion or human taste. Additionally, there is a great diversity of known compounds, some highly toxic as well as noxious, which can be tabulated under four broad categories: biogenic amines, peptides, bufodienolides (bufogenins) and alkaloids. The last category includes alkaloids derived from biogenic amines, water-soluble alkaloids (tetrodotoxins) and lipophilic alkaloids. Most compounds are known only from skin of adult amphibians, but the toxic and noxious properties of eggs and larvae of certain salamanders and toads can be attributed to tetrodotoxins and bufodienolides, which occur also in adult tissues other than skin. Predator aversion and various antipredator behaviors and aposematic colorations clearly prove the defensive value of these diverse metabolites, whether or not they are elaborated primarily (e.g. alkaloids) or secondarily (e.g. some peptides and biogenic amines) for this function. Lipophilic alkaloids include the samandarine alkaloids, known definitely only from an Old World genus of salamanders, and the more than 200 dendrobatid alkaloids. Nearly all the latter are unique to neotropical poison frogs of the genera Dendrobates and Phyllobates (Dendrobatidae), except for seemingly homoplastic occurrences of a few such alkaloids in small brightly colored anurans of several other families. Owing to recent discoveries and new structural information, the dendrobatid alkaloids are here partitioned among the following major and minor classes: batrachotoxins, histrionicotoxins, indolizidines, pumiliotoxin-A class and its allopumiliotoxin and homopumiliotoxin subclasses, decahydroquinolines, gephyrotoxins, 2,6-disubstituted piperidines, 2,5-disubstituted pyrrolidines, pyridyl-piperidines, indole alkaloids, azatricyclododecenes and amidine alkaloids. Except for the steroidal batrachotoxins, and the minor classes of pyrrolidine alkaloids, indole alkaloids and amidine alkaloids, all the above contain a piperidine ring. A large number of piperidine-based alkaloids occur mainly as trace compounds in Dendrobates and remain unclassified; the only water-soluble toxin so far discovered in a dendrobatid (Colostethus) is structurally unknown, but conceivably an alkaloid.

Classification of skin alkaloids from neotropical poison-dart frogs (dendrobatidae)

Abstract Dendrobatid frogs have evolved an imposing number of unique alkaloids, apparently as a chemical defense against predation. Toxic skin extracts from a majority (18) of the approximately two dozen species of Dendrobates (sensu lato) were analyzed by thin-layer chromatography, gas chromatography and mass spectrometry. Ninety alkaloids were detected and characterized, with structures being presented for many. The species of Dendrobates elaborate at least 5 classes of biosynthetically related alkaloids, namely the pumiliotoxin-C class (decahydroquinolines), the hydroxypumiliotoxin-C class, the histrionicotoxin class (1-azaspiro [5.5]undecanes), the gephyrotoxin class (perhydropyrrolopiperidines and perhydropyrroloquinolines) and the pumiliotoxin-A class (of as yet unknown structure). A sixth class, the batrachotoxins, is a series of highly toxic, steroidal alkaloids that are produced only by species of Phyllobates (sensu stricto). A wide range of biological activity of the dendrobatid alkaloids is indicated by injection of unresolved alkaloid fractions into white mice: extracts from different species of Dendrobates produce reactions as diverse as Straub tail, penile erection, prostration, convulsions and salivation.

Morphology of the granular secretory glands in skin of poison-dart frogs (Dendrobatidae).

The granular glands of nine species of dendrobatid frogs were examined using light and electron microscopy. The glands are surrounded by a discontinuous layer of smooth muscle cells. Within the glands proper the secretory cells form a true syncytium. Multiple flattened nuclei lie at the periphery of the gland. The peripheral cytoplasm also contains mitochondria, rough surfaced endoplasmic reticulum, the Golgi apparatus, and an abundance of smooth endoplasmic reticulum. Centrally, most of the gland is filled with membrane-bound granules surrounded by amorphous cytoplasm. Few other organelles are found in this region. Early in the secretory cycle, the central part of the gland is filled with flocculent material which appears to be progressively partitioned off by membranes to form the droplet anlage. As granules form, the structure of the contents becomes progressively more vesicular. Dense vesicles, which bud off from the Golgi apparatus, fuse with the granular membrane during the development of granules, and might contain enzymes involved in toxin synthesis. The granules at this point resemble multivesicular bodies. Their structure is similar in all species of dendrobatid frogs even though the different frogs secrete substances of different chemical structure and toxicity.

Rare Snakes—Five New Species from Eastern Panama: Reviews of Northern Atractus and Southern Geophis (Colubridae: Dipsadinae)

Abstract The South American genus Atractus barely enters political North America on the eastern half of the Isthmus of Panama, where it is extraordinarily rare. Collected over a period of 39 years, the five Panamanian specimens of Atractus known to the author represent five species! Four new species are described: A. darienensis, A. hostilitractus, A. imperfectus, and A. depressiocellus. The fifth species is A. clarki Dunn and Bailey, for which a second specimen is reported from the Colombia Chocó. The noncapitate hemipenis of A. clarki may be primitive in being calyculate and deeply bilobed. The morphologically convergent Geophis is primarily a Middle American genus—Mexico to western Panama, with two or three outlying species in the western Andes of Colombia (G. betaniensis, G. nigroalbus, and probably G. hoffmanni). The genus is unrecorded from eastern Panama, and a few old records for central Panama seem to have been based on erroneous specimen data. Nonetheless, the genus does occur in east-central Panama, based on two specimens of G. hoffmanni (W. Peters) and on a specimen each of Geophis bellus, new species, and G. brachycephalus (Cope)—the latter representing a disjunct population separated by about 340 km from those in the Boquete area of western Panama. Geophis bellus is a tiny snake differing from sympatric G. brachycephalus and South American G. nigroalbus in characters of size, color, and hemipenis. Geophis brachycephalus may be a composite species in western Panama. Unicolored specimens from the Atlantic versant seem to differ from those in the polymorphic Boquete population in hemipenial and other characters, and they are set aside as a species inquirenda. The first specimen of Geophis hoffmanni is reported from Colombia, but it lacks precise data. Atractus depressiocellus, A. imperfectus, Geophis bellus, G. brachycephalus, and G. hoffmanni are at least broadly sympatric on the “Piedras-Pacora Ridge”—the continental divide—between the upper drainages of the Río Chagres and Río Pacora, some 30 km northeast of Panama City. This relatively low upland likely is a premontane forest refuge, where some very rare snakes may be making a last stand prior to extinction.

Herpetofauna of the Yutaje-Corocoro Massif, Venezuela: second report from the Robert G. Goelet American museum-Terramar Expedition to the northwestern tepuis

Abstract The Yutajé–Corocoro massif is a highly eroded sandstone table mountain, with internal drainage mainly to the central valley of the Río Corocoro, a stream in the headwater drainage of the Río Manapiare—some 100 km east of the middle Río Orinoco, at the northern edge of the State of Amazonas in southern Venezuela. The rocky soil supports a mosaic of diverse scrubland and forest, with small tepui meadows at the higher elevations. The herpetofauna is depauperate, as is typical of the Venezuelan tepuis. Eight species of amphibians and reptiles were collected during a 7-day period in the dry season (February). This sample includes two new frogs (Hyalinobatrachium eccentricum, n. sp., Centrolenidae; Colostethus undulatus, n. sp., Dendrobatidae) and a new genus and species of lizards (Adercosaurus vixadnexus, n. gen. & sp., Teiidae), all of which were found in humid montane mossy forest at 1700–1750 m elevation. Another new lizard (Tropidurus panstictus, n. sp., Tropiduridae) was discovered at lower elevations (180–1220 m), especially in dry scrub. The fauna also includes a widespread lowland frog (Pseudopaludicola llanera Lynch), two tepui frogs (Eleutherodactylus cantitans Myers and Donnelly; E. yaviensis Myers and Donnelly), a tepui lizard (Prionodactylus goeleti [Myers and Donnelly], new combination), a snake (Liophis?) that escaped capture, and another snake (Thamnodynastes corocoroensis Gorzula and Ayarzagüena) obtained by S. Gorzula in 1987. The two Eleutherodactylus and the Prionodactylus also occur on neighboring Cerro Yaví (the type locality), although one of the frogs (E. yaviensis) and the lizard show evidence of differentiation. Based on the original description, the snake Thamnodynastes corocoroensis appears to be distinct from a related species on Cerro Yaví. Two of the new species exhibit characters that are novel or not previously noted. The dendrobatid frog Colostethus undulatus, n. sp. has a glandular supracarpal pad atop the wrist, being best developed in males. This species, which also has the parasphenoid bone curiously concealed, seems to be unusual among tepui Colostethus in lacking the recently described median lingual process. The centrolenid frog Hyalinobatrachium eccentricum, n. sp. has a peculiar bicolored iris, with a dark median sector that conceals the pupil and which apparently dilates with the pupil. This character is retained in preservative and differentiates H. eccentricum from H. crurifasciatum Donnelly and Myers. Both species share a previously overlooked bubblelike structure in the web between the third and fourth fingers, herein termed bulla (possibly parasite induced?).

First occurrence of tetrodotoxin in a dendrobatid frog (Colostethus inguinalis), with further reports for the bufonid genus Atelopus

The water-soluble toxin present in skin of Colostethus inguinalis (Dendrobatidae) was identified as tetrodotoxin by fluorometric HPLC analysis. The amount of tetrodotoxin per frog skin was estimated by HPLC, mouse toxicity, and inhibition of [3H]saxitoxin binding to brain membranes as 0.1 to 1.2 micrograms. Small amounts of anhydrotetrodotoxin and 4-epietrodotoxin also were present. Tetrodotoxin-like activity was not detected by inhibition of [3H]saxitoxin binding in other species of Colostethus nor in other dendrobatids (Aromobates, Dendrobates, Phyllobates). Tetrodotoxin-like activity was present in extracts of skin of five species of Atelopus (Bufonidae). HPLC analysis identified tetrodotoxin as the major toxic component in Atelopus spumarius and A. varius, as a minor component in A. spurrelli, and as a trace component in A. ignescens and A. zeteki. The major tetrodotoxin-like compounds in the last three species were not identified. Tetrodotoxin-like activity was not detected by inhibition of [3H]saxitoxin binding in skin extracts from three other genera of bufonids.

The Summit Herpetofauna Of Auyantepui, Venezuela: Report From The Robert G. Goelet American Museum–Terramar Expedition

Abstract Auyantepui is an immense sandstone table mountain in the Venezuelan Guayana. This mesa did not appear on aviation maps and was unknown to the literate world prior to the late 1930s. It was explored from the air by Jimmy Angel, a bush pilot and colorful soldier of fortune for whom the worlds highest waterfall is named (Angel Falls at the northern end of Auyantepui). About the same time, in 1937, Captain Félix Cardona Puig and Gustavo Heny discovered an access crack in the sandstone, allowing ascent onto the southern end of the mesa. The first scientific exploration followed immediately—the 1937–1938 Phelps Venezuelan Expedition of the American Museum of Natural History made the first zoological and general botanical collections. Today, no tepui other than the “Lost World” of Cerro Roraima is better known to the general public. The summit of Auyantepui has a known fauna of 24 species of amphibians and reptiles, including species added by the Robert G. Goelet American Museum–Terramar Expedition in 1994. This expedition collected 16 species during a month of fieldwork in the dry season (February), in five camps at elevations of 1700–2100 m above sea level. All species known from the summit of Auyantepui are treated in this bulletin; illustrations where possible include tadpoles, bioacoustic spectrograms, and hemipenes. Four new species are described—two frogs (Hypsiboas angelicus, n. sp., Eleutherodactylus auricarens, n. sp.), a lizard (Arthrosaura montigena, n. sp.), and a snake (Atractus guerreroi, n. sp.). Arthrosaura montigena possesses a hemipenial character not previously described—an orifice (orificium) of unknown function, situated in the lobular crotch between the two lobes. Attention is called to a probably undescribed snake (Liophis “miliaris” sensu lato) from the nearby Gran Sabana. The herpetofauna of the Auyán summit comprises 12 families, 20 genera, and 24 species. This is compared with the known herpetofauna of the Chimantá massif, lying less than 50 km south-southeast of Auyantepui. Despite the proximity and similar dimensions, the summits of Auyantepui and Chimantá have in common only 11% of the combined number of species (4 of 36), 44% of the genera (11 of 25), and 62% of the families represented (8 of 13), showing that neighboring tepuis may have herpetofaunas very different from one another. Nonetheless, the adjacent mountains that constitute the more fragmented Chimantá massif are relatively close to one another and seem to have a unified herpetofauna.

An Enigmatic New Snake from Cloud Forest of the Península de Paria, Venezuela (Colubridae: Genus Taeniophallus?)

Abstract The snake Taeniophallus nebularis, new species, is known from a single specimen collected in montane cloud forest, 800 m above sea level, Península de Paria, northeastern Venezuela. It is a small “xenodontine” colubrid (adult male, 492 mm total length); dorsal scales in 19-19-17 rows, smooth, with paired apical pits anteriorly; brown dorsally and grayish laterally, with ill-defined pattern; white postocular stripe; and bright yellow midventrally between serrated black edges. The species is easily diagnosed, although assignment to Taeniophallus is problematic. However, a few suggestive characters are shared with T. brevirostris and T. nicagus. These species, presumably the closest geographic relatives of T. nebularis, occur in the Amazon basin and the Guianas, indicative of a biogeographic parallel with certain plants. Taeniophallus occipitalis, with extreme scale-row reduction and a distinctive color pattern possibly derived from a brevirostris-like precursor, is widely distributed south of the Amazon. Four additional species of Taeniophallus s.l. comprise the monophyletic affinis species group centered in southeastern Brazil. The genus Echinanthera (also centered in southeastern Brazil) is sometimes expanded to include all of Taeniophallus. Echinanthera s.s. is viewed as a demonstrably monophyletic group of six named species, whereas relationships of the subgroups of Taeniophallus s.l. among themselves and to Echinanthera remain uncertain. Evolutionary divergence in copulatory organs of the otherwise similar Taeniophallus nicagus and T. brevirostris is extraordinary, suggesting that uncritical weight cannot safely be assigned to hemipenial characters of presumptive relatives. The hemipenis of Taeniophallus nebularis differs from those of other taxa discussed in being conspicuously bilobed for nearly a third of its length. However, some degree of bilobation is symplesiomorphic for these snakes, as evidenced by presence or absence of weak bilobation in a few species and divided insertions of retractor muscles in all. The penial asulcate interspinal gap in T. nebularis also might be symplesiomorphic for Taeniophallus s.l. and Echinanthera s.s., but homologies and level of generality for this character are not yet clear.

Frogs of the Eleutherodactylus biporcatus Group (Leptodactylidae) of Central America and Northern South America, Including Rediscovered, Resurrected, and New Taxa

Abstract A revision of the broad-headed frogs of the biporcatus species group of Eleutherodactylus s.l. has a wholly unexpected nomenclatural consequence. Eleutherodactylus biporcatus (W. Peters, 1863) is not from “Veragua” (western Panama) as originally thought, but is the proper name for the Venezuelan frog heretofore known as E. maussi (Boettger, 1893). Three names are resurrected from synonymy for Central American species currently masquerading under the misapplied name biporcatus, and a fourth species is described as new: (1) The rediscovery of Eleutherodactylus gulosus (Cope, 1875) shows it to be a large montane frog occupying an apparently small range in the borderland of Costa Rica and Panama. (2) Eleutherodactylus rugosus (W. Peters, 1863) is a smaller species occurring on the Pacific versant of southwestern Costa Rica and western Panama; Lithodytes pelviculus Cope and L. florulentus Cope are synonyms of E. rugosus. (3) Eleutherodactylus megacephalus (Cope, 1875), an intermediate-sized frog ranging from Honduras to central Panama, is the more common species to which the name biporcatus has usually been applied. Available material from the western half of the Isthmus of Panama was too sparse to decide if another (unnamed) species is being included under the name megacephalus. (4) The name biporcatus also has been used for Eleutherodactylus opimus, new species, which occurs from central Panama to western Colombia. Based on the condition of the m. adductor mandibulae, the Venezuelan Eleutherodactylus biporcatus s.s. (E. maussi, auctorum) belongs to the Middle American clade of Eleutherodactylus (subgenus Craugaster). However, preliminary data on karyotypes, as well as morphological differences, cast doubt on the closeness of E. biporcatus to the other species studied. The monophyly of the “biporcatus group” therefore remains to be tested. RESUMEN La revisión de las ranas de cabeza ancha del grupo biporcatus de Eleutherodactylus tiene una consecuencia nomenclatural completamente inesperada. Eleutherodactylus biporcatus (W. Peters, 1863) no es de “Veragua” (Panamá occidental) como se creía previamente, sino que es el nombre propio de la rana venezolana conocida hasta ahora como E. maussi (Boettger, 1893). Se resucitan tres nombres de la sinonimia para especies centroamericanas previamente ocultos bajo el nombre incorrecto de biporcatus, y se describe una cuarta especie nueva: (1) El redescubrimiento de Eleutherodactylus gulosus (Cope, 1875) indica que es una rana grande, de montaña, que tiene una distribución geográfica pequeña en la frontera entre Costa Rica y Panamá. (2) Eleutherodactylus rugosus (W. Peters, 1863) es una especie más pequeña que ocurre en las tierras más bajas del Pacífico del suroccidente de Costa Rica y del occidente de Panamá; Lithodytes pelviculus Cope y L. florulentus Cope son sinónimos de E. rugosus. (3) Eleutherodactylus megacephalus (Cope, 1875), una rana de tamaño intermedio y distribuida desde Honduras hasta Panamá central, es la especie que más comunmente se ha llamado biporcatus. El material disponible de la mitad occidental del Istmo de Panamá no es adecuado para decidir si hay alguna otra especie (sin nombre) incluida bajo el nombre megacephalus. (4) El nombre biporcatus también se ha usado para Eleutherodactylus opimus, especie nueva, que ocurre desde Panamá central hasta Colombia occidental. Basándose en la condición del m. adductor mandibulae, Eleutherodactylus biporcatus s.s. (E. maussi auctorum) de Venezuela pertenece al clado mesoamericano de Eleutherodactylus (subgenero Craugaster). Sin embargo, información preliminar sobre cariotipos, así como diferencias morfológicas, hacer dudar del parentesco de E. biporcatus con las otras especies estudiadas. La monofilia del “grupo biporcatus” debe ser corroborada.

Morphological Extremes—Two New Snakes of the Genus Atractus from Northwestern South America (Colubridae: Dipsadinae)

Abstract Two new Andean snakes exhibit extreme morphology in a genus of South American dipsadine colubrids. One, Atractus attenuatus, new species, is a slender, exceptionally attenuated snake 420 mm in total length (adult male holotype), with 17 scale rows, a high ventral + subcaudal count (226), and an extremely vague pattern of numerous, closely spaced, indistinct dark crossbars on a brown ground color. Atractus attenuatus comes from 1000 m elevation in the northern end of the Cordillera Central (Sabanalarga, Antioquia, Colombia). A geographic neighbor, Atractus sanguineus Prado, is of similar morphology but differs in having distinct, widely spaced crossbars on a red ground color. At another extreme, Atractus gigas, new species, is a very robust snake that exceeds a meter in length (adult female holotype 1040 mm in total length), with a hint of pale transverse dorsal bars on a brown ground color. It is the largest known Atractus, differing in color pattern and details of scutellation from the several o...