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Osteology of Bufo sternosignatus Günther, 1858 (Anura:Bufonidae) with Comments on Phylogenetic ImplicationsAuthor(s): Claudia M. Vélez-RodríguezSource: Journal of Herpetology, 39(2):299-303. 2005.Published By: The Society for the Study of Amphibians and ReptilesDOI: http://dx.doi.org/10.1670/31-04WURL: http://www.bioone.org/doi/full/10.1670/31-04W

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Journal of Herpetology, Vol. 39, No. 2, pp. 299–303, 2005Copyright 2005 Society for the Study of Amphibians and Reptiles

Osteology of Bufo sternosignatus Gunther, 1858 (Anura: Bufonidae) withComments on Phylogenetic Implications

CLAUDIA M. VELEZ-RODRIGUEZ

Casilla 13, Sucursal Diego Portales, Santiago, Chile

ABSTRACT.—Osteological characters are used to infer the phylogenetic relationships of the Venezuelan toad,Bufo sternosignatus. The species does not have a ventrolateral process on the quadratojugal, a synapomorphyfor the especies of the B. typhonius clade and is associated to B. humboldti a species of the B. granulosus group.

The specific status and distribution of Bufo sterno-signatus Gunther, 1858, have been confusing since itsdescription. Shreve (1947) considered the taxon a sub-species of Bufo typhonius from South America. Rivero(1961) thought the toad resembled Bufo typhonius alatus,from Panama, and Porter (1964) synonymized thespecies with Bufo valliceps, from Central America. Re-cently, La Marca and Mijares-Urrutia (1996) based aredescription of B. sternosignatus on additional materialfrom Venezuela. Some Bufo populations from Colombiawere referred to this species in error (Velez-Rodrıguez,1999), and they were subsequently argued to representa new species of the Bufo typhonius (5 Bufo margaritifer)clade (Velez-Rodrıguez, 2004).

The systematic status of B. sternosignatus remainsenigmatic. Cei (1972), Duellman and Schulte (1992),and Velez-Rodrıguez (1999) placed it in the B. typhoniusgroup. Hoogmoed (1990) and Rivero (1961) consideredthe species identical to B. ‘‘typhonius’’ from Panama andadjacent areas, and La Marca and Mijares-Urrutia (1996)mentioned that B. sternosignatus probably is related toBufo granulosus. Herein, I describe the osteology of B.sternosignatus and compare it with the B. granulosus andB. typhonius groups.

MATERIALS AND METHODS

Museum codes for the specimens examined (Appen-dix 1) are as follows: CIEZAH, Coleccion Herpetologicadel Centro de Investigaciones en Ecologıa y ZonasAridas, Universidad Francisco de Miranda, Venezuela;ICN, Instituto de Ciencias Naturales, UniversidadNacional de Colombia; USNM, National Museum ofNatural History, United States of America.

Measurements of alcohol-preserved museum speci-mens are in millimeters and were recorded to the nearest0.1 mm with dial calipers. Sex and sexual maturity weredetermined by direct observation of the gonads in bothsexes and presence or absence of nuptial excrescences inmales. Osteological characters were examined fromcleared-and-stained specimens prepared in the mannerof Dingerkus and Uhler (1977). Osteological nomencla-ture is derived from Trewavas (1933), Trueb (1973, 1993),and Wild (1997). Morphological observations andillustrations were made with a stereoscope equippedwith a camera lucida.

OSTEOLOGY

The description is based on an adult female (CIEZAH515; 59.7 mm SVL).

Skull.—In dorsal aspect, the skull is triangular andmuch broader than long at its widest level, the angleof the jaws. Anterior margins of nasals are short andhave a blunt termination anterior to alary processes ofthe premaxillae (Fig. 1A–C). Nasals articulate with oneanother medially throughout most of their lengths.Posteromedially the margins diverge posterolaterallyfrom one another to expose a small part of thesphenethmoid; most of the posterior margin of eachnasal articulates with the anterior margin of the adjacentfrontoparietal; lateral margins form part of the lowsupraorbital crest. Posteroventrally, nasals are deeplycurved and thick, forming preorbital crests. The long,acuminate maxillary process overlies and extendsbeyond the preorbital process of the pars facialis ofthe maxilla articulating with it. Anterior to this process,there is another process that articulates with a corre-sponding anterior process of the maxilla forming aclose contact between the two bones. Dorsolateralportions of the nasals are thick, but they do not formcanthal crests; however, externally the skin forms acanthal ridge on each side. The nasals comprise lessthan half of the orbital margin.

Wide frontoparietals articulate throughout theirlengths except at their anteromedial ends wheremargins of the bones diverge anterolaterally from oneanother to expose a small part of the sphenemoidmedially. The lateral margins are slightly exostosed toform a low supraorbital crest and articulate with themedial expansion of the otic ramus of the squamosal.

The sphenethmoid is widely ossified ventrally; theanterior margin of this element almost reaches thelevel of the palatine processes of the premaxillae andlaterally the first third of the prevomers. The posteriormargin of the sphenethmoid lies at about two-fifths thelength of the orbit. Prootic and exoccipital are neitherfused to one another nor to the squamosal dorsolat-erally. Prootics are broadly separated from one anotherventromedially, and well ossified anterolaterally. Exoc-cipitals are fused to one another ventromedially but notdorsomedially. The small, hemispherical occipital con-dyles are separated from one another; the face of eachcondyle is oriented posteromedially. The occipitalartery is partially enclosed in a canal, uncovered bybone anteriorly, with a distinct foramen at each end.Operculum, stapes, and tympanic annulus are present.

Premaxillae are located at the anterior level of thenasals in lateral view; each bears a low pars dentalisand moderate pars palatina and a prominent, fanglike,palatine process medially. Premaxillae are separated byconnective tissue medially and articulate with the pars

palatina of the maxilla laterally. The alary process ofeach premaxilla is moderately long, broadly based, andtriangular, with the apex directed slightly anterolater-ally when viewed laterally.

Maxilla is robust in lateral aspect. The postorbitalportion of the pars facialis is expanded (as high as theanterior part), and almost in contact with the zygomaticramus of the squamosal. The pars facialis is welldeveloped in the orbital region, forming a slight sub-orbital crest. A long, acute process on the most anteriorpart of the pars facialis of the maxilla is directed towardthe septomaxilla and articulates with it. In ventral view,the maxilla has a long palatine process that articulateswith the vomer. The well-developed antorbital processarticulates with the maxillary process of the nasal, aswell as with the neopalatine medially, reaching the levelof the internal nares. Ventrally, each maxilla bears anindistinct pars dentalis and a narrow pars palatina; thepterygoid process is absent. The maxilla terminates inthe posterior region of the orbit and articulates with thequadratojugal.

Neopalatines are robust, curved bones each of whichinvests the planum antorbitalae along the anterior mar-gin of the orbit. Neopalatine is in partial contact withthe maxilla laterally and with the anterior process of thepterygoid posteriorly. The bone articulates with thesphenethmoid anterior to the level of the orbitonasalforamen and medially with the medial antorbital pro-cess of the pars facialis of the maxilla. The neopalatinebears a prominent ventral ridge.

Vomers are small, edentate bones, widely separatedfrom one another, each associated with the anterome-

dial margin of the choana. The anterior process is shortand truncate and articulates with a long and acuminatepalatine process of the maxillae. There are long andprominent pre- and postchoanal processes and a ven-trally projecting dentigerous process.

The moderate-sized septomaxilla is compact andtriangular and bears two processes posteriorly. Eachseptomaxilla is visible within the olfactory capsuleabove the articulation of the premaxilla and maxillain lateral view and articulates with the anterior parsfacialis process of the maxilla.

The anterior end of the alary cartilage (Fig. 1D) ishighly mineralized in the manner of a pair of ‘‘ossifiedplates’’ (in the infranasal region), cartilaginous dorsallyand totally ossified ventrally, directed toward the alaryprocesses of the premaxillae. The end of the septumnasi is partially mineralized.

The cultriform process of the parasphenoid is shortand relatively broad. The lateral margins are slightlyconvex. The acuminate anterior terminus lies at aboutthe midorbit. The posterolateral alae of the parasphe-noid are short, their leading edges underlain anterolat-erally by the medial rami of the pterygoids; the ventralsurface of each parasphenoid ala bears a bony ridge,and there is a pair of parallel ridges on the base of theparasphenoid corpus.

The pterygoids are robust elements. The anteriorramus is long and approximately parallel to the longi-tudinal axis of the skull; it has a broad articulation withthe maxilla. The medial ramus is more slender than theanterior ramus and about two-thirds as long; it extendsalong the anteroventral margin of the otic capsule and

FIG. 1. Skull of Bufo sternosignatus (female, CIEZAH 515), (A) dorsal view, (B) ventral view, (C) lateral view,(D) frontal view. The stippled area is cartilage.

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overlaps the anterolateral corner of the parasphenoidala. At the junction of the medial ramus and theposterolateral ramus, there is a high, thin crest; theposterolateral ramus is only about half the length ofthe medial ramus.

The squamosal is robust in lateral aspect. Thezygomatic ramus is expanded anteroventrally andreaches the medial level of the ventral ramus; it formsa thick postorbital crest that almost articulates with theposterodorsal expansion of the pars facialis of themaxilla. The otic ramus is thick, ornamented and formsa low, thick, supratympanic crest; this element articu-lates with the prootic, and frontoparietal and it is notfused with them. The ventral ramus is short, wide,not expanded, articulating with the quadratojugal. Inlateral aspect, the jaw articulation lies posterior to thefenestra ovalis.

Hyoid.—The cartilaginous corpus of the hyoid islonger than wide (Fig. 2A). The hyoglossal sinus hasa narrow U-shape and is twice as deep as wide. Eachslender hyale bears an expanded area at the level of the

anterolateral processes of the hyoid. The anterolateralprocesses are large, with a long anterior process anda short (or indistinct) posterior process. The postero-lateral processes are slender and long, with round tips.The posteromedial processes are ossified and short.They are distinctly separated from one another andfrom the cartilaginous corpus by connective tissue. Theanterior and posterior ends are wider than the medialregion and the posterior ends terminate with short,triangular cartilages.

Vertebral Column.—The axial column consists of eightprocoelous vertebrae, each of which is imbricate exceptPresacral I (Fig. 2B). The cervical cotyles of the atlas areType I of Lynch (1971), directed anteroventrally andseparated by a distinct notch. In order of decreasinglengths (exclusive of cartilaginous distal ends) of thetransverse processes of the presacral vertebrae and thesacrum are, as follow: IV � Sacrum . V . III . VI .VII . VIII . II. The transverse processes of Presacral IIare robust and expanded distally; they are wider at thetips than are those of Presacral III, and thinner at the

FIG. 2. (A) Hyoid of Bufo sternosignatus (female, CIEZAH 515), (B) dorsal view of vertebral column. The stippledarea is cartilage.

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tips than are those of Presacral IV. The transverseprocesses of Presacrals VI–VIII are widest at their basesand acuminate distally. Presacrals III–VI are directedposteriorly and VII–VIII are directed anteriorly. Thesacral diapophyses are expanded and have narrowbases (approximately one third width of lateral mar-gins). In dorsal aspect, the pre- and postzygapophysesare expanded but not elevated dorsally in lateral aspect.The neural spines are expanded laterally and notelevated; the urostyle bears a bicondylar articulationwith the sacrum and a thin, but prominent, longitudinalridge. The urostyle composes 40% of the total length ofthe axial column. The pectoral girdle is arciferal, and theomosternum is absent.

Variation.—Some variations (adult male, CIEZAH867; 36.4 mm SVL) may be the result of sexualdimorphism. The alary cartilage is totally ossified.The acuminate maxillary process of the nasal overliesand extends beyond the antorbital process of the parsfacialis of the maxilla but does not articulate with it;additionally, there is not articulation between these twobones anteriorly. The ventral surface of each para-sphenoid ala bears a bony ridge more pronounced thanin the female.

DISCUSSION

The osteology, musculature, internal, and externalmorphology of B. sternosignatus and several speciesassigned to the B. typhonius phenetic group werestudied as part of an investigation into their phyloge-netic relationships (Velez-Rodrıguez, 2004). One of theconclusions of that work is the presence of a ventrolat-eral process on the quadratojugal (Fig. 3A–B)—a syna-pomorphy for the species of the B. typhonius clade (newdefinition, Velez-Rodrıguez, 2004)—absent in B. sterno-signatus. Included in the phylogenetic study was B.humboldti (B. granulosus group), and B. sternosignatusresulted in a clade with it.

Bufo sternosignatus is similar to the members of the B.granulosus group (Pramuk 2000, 2002), by having a closearticulation between the nasals and the dorsal marginof the pars facialis of the maxilla, an anteroventral ex-pansion of the zygomatic ramus of squamosal reachingthe medial level of the ventral ramus (but withoutarticulating with the maxilla), the presence of the m.adductor longus and inguinal fat bodies (Da Silva andMendelson, 1999). On the other hand, unlike the skullsof members of B. granulosus group (Pramuk, 2000), B.sternosignatus has reduced co-ossification, the nasalbones compose less than half of the dorsal margin of theorbit, and prenasal bones are absent (but there is a greattendency of ossification of the anterior end of the alarycartilage and the infranasal region). It is clear thatfurther studies are needed with all the species assignedto B. granulosus group (Cei, 1972; Frost, 2002; Pramuk,2000; Narvaes, 2003), in addition to B. sternosignatus.Furthermore, the use of developmental series may helpto elucidate their phylogenetic relationships.

Acknowledgments.—I express my gratitude to R.Formas, my adviser at the Universidad Austral deChile. I especially thank R. Heyer and the herpetolog-ical staff of the National Museum of Natural History, L.Trueb and W. B. Duellman at the University of Kansas,L. Ford and the herpetological staff of the AmericanMuseum of Natural History, M. C. Ardila and J. D.Lynch at the Instituto de Ciencias Naturales, Universi-dad Nacional de Colombia, and J. E. Castillo from theInstituto von Humboldt of Colombia, for the loan ofspecimens and their hospitality while I visited the col-lections. Additionally, I am indebted to A. Mijares-Urrutia, from the Centro de Investigaciones enEcologıa y Zonas Aridas, Universidad Francisco deMiranda, Venezuela, L. A. Coloma from the PontificiaUniversidad Catolica del Ecuador, A. Resetar from theField Museum, C. Castro-M. from the Museu deZoologia da Universidade de Sao Paulo, W. Boehme

FIG. 3. Skull of Bufo typhonius (female, USNM 531318), (A) dorsal view, (B) ventral view. The stippled areais cartilage.

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from the Museum Alexander Koenig, R. Boistel fromthe Centre Scientifique d’Orsay, Universite Paris, A.Ohler from the Museum National d’Histoire Naturelle,G. Nilson from the Goteborg Natural History Museumand G. Schneider from the University of MichiganMuseum Zoology for providing specimens and asso-ciated information about them. I am especially gratefulto J. D. Lynch, J. Mendelson III (Utah State University),P. Narvaes (Universidade de Sao Paulo, Brasil), J.Nunez (Instituto de Zoologıa, Universidad Austral deChile), J. Pramuk, and L. Trueb (University of Kansas),who read and criticized earlier versions of themanuscript. M. Navarro and R. Estupinan executedthe drawings. The visit to National Museum of NaturalHistory was possible by a Short-term Visitor TravelGrant and to the American Museum of Natural Historyby a Collection Study Grant. My research on Bufonidaewas supported by the Deutsche AkademischeAustausch Dienst (DAAD) and the Direccion deInvestigacion y Desarrollo, Universidad Austral deChile (DID-200101).

LITERATURE CITED

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DA SILVA, H. R., AND J. R. MENDELSON III.1999. A neworgan and sternal morphology in toads (Anura:Bufonidae): descriptions, taxonomic distribution,and evolution. Herpetologica 55:114–126.

DINGERKUS, G., AND L. D. UHLER. 1977. Enzyme clearingof Alcian Blue stained whole small vertebrates fordemonstration of cartilage. Stain Technology 52:229–30.

DUELLMAN, W. E., AND R. SCHULTE. 1992. Description ofa new species of Bufo from northern Peru withcomments on phenetic groups of South Americantoads (Anura: Bufonidae). Copeia 1992:162–172.

FROST, D. R. 2002. Amphibian Species of the World: AnOnline Reference. V2.21 (15 July 2002). Electronicdatabase available at http://research.amnh.org/herpetology/amphibia/index.html.

HOOGMOED, M. S. 1990. Biosystematics of SouthAmerican Bufonidae, with special reference to theBufo ‘‘typhonius’’ group. In G. Peters and R.Hutterer (eds.), Vertebrates in the Tropics, pp.113–123. Museum Alexander Koenig, Bonn,Germany.

LA MARCA, E., AND A. MIJARES-URRUTIA. 1996. Taxonomyand geographic distribution of a northwesternVenezuelan toad (Anura, Bufonidae, Bufo sterno-signatus). Alytes 14:101–114.

LYNCH, J. D. 1971. Evolutionary relationships, osteolo-gy, and zoogeography of leptodactyloid frogs.Miscellaneous Publication, Museum of NaturalHistory, Univ. of Kansas 53:1–238.

NARVAES, P. 2003. Revisao taxonomica das especies deBufo do complejo granulosus (Amphibia, Anura,Bufonidae). Tese Instituto de Biociencias daUniversidade de Sao Paulo. Brazil.

PRAMUK, J. B. 2000. Prenasal bones and snout mor-phology in West Indian bufonids and the Bufogranulosus species group. Journal of Herpetology34:334–340.

———. 2002. Combined evidence and cladistic rela-tionships of West Indian toads (Anura: Bufonidae).Herpetological Monographs 16:121–151.

PORTER, K. R. 1964. Distribution and taxonomic statusof seven species of Mexican Bufo. Herpetologica19:229–247.

RIVERO, J. A. 1961. Salientia of Venezuela. Bulletin ofthe Museum of Comparative Zoology Harvard126:1–207.

SHREVE, B. 1947. On Venezuelan reptiles and amphib-ians collected by Dr. H. G. Kugler. Bulletin of theMuseum of Comparative Zoology Harvard 99:519–537.

TREWAVAS, E. 1933. The hyoid and larynx of the Anura.Philosophical Transactions of the Royal Society ofLondon B Biological Sciences 222 10:401–527.

TRUEB, L. 1973. Bones, frogs, and evolution. In J. G. Vial(ed.), Evolutionary Biology of the Anurans: Con-temporary Research on Major Problems, pp. 65–132. Univ. of Missouri Press, Columbia.

———. 1993. Patterns of cranial diversity among theLissamphibia. In J. Hanken and B. K. Hall (eds.),The Skull, Volume 2: Patterns of Structural andSystematic Diversity, pp. 255–343. Univ. of ChicagoPress, Chicago.

VELEZ-RODRIGUEZ, C. M. 1999. Presencia de Bufosternosignatus Gunther 1859 (Amphibia: Bufonidae)en Colombia. Revista de la Academia Colombianade Ciencias Exactas, Fısicas y Naturales 23 (Suple-mento Especial):411–416.

———. 2004. Sistematica de los sapos neotropicalespertenecientes al Grupo Bufo typhonius (Amphibia:Bufonidae). Unpubl. Ph.D. diss., Universidad Aus-tral de Chile, Voldivia.

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Accepted: 11 January 2005.

APPENDIX 1

The following specimens were examined: Bufo sterno-signatus CIEZAH 319 (adult female), CIEZAH 975(adult male), from Venezuela, San Diego, Sierra de SanLuis, Estado Falcon, approximately 1100 m. USNM121173-74, 162693-94, 166858, 291059-60 (adult males),from Venezuela, Distrito Federal, road between ColoniaTovar to El Limon, 850 m. USNM 259137 (adult male),from Venezuela, Carabobo, Bejuma 23 km north. ofPalmichal, 1000 m. Cleared-and-stained skeletons of B.sternosignatus CIEZAH 515 adult female, CIEZAH 867adult male, same locality of CIEZAH 319; Bufotyphonius USNM 531318 (adult female), USNM 531319(adult male), from Guyana.

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