Hsiou et al., 2010 - Colombophis

Hsiou et al., 2010 - Colombophis

(Parte 3 de 4)

fragmentation in this region. Much of the condylar surface is exposed in ventral view, where the precondylar constriction is moderately marked.

Remarks.—After comparison of Colombophis vertebrae, it became clear that some differences cannot be attributed to intraspecific or intracolumnarvariation,andhencewarrantthe erection of a new species. These differences are mainly the proportions of the vertebrae, the height of the neuralspine, the morphology of the paradiapophyses,and the robustness of the zygosphene.Theneuralarchandcentrumofthe midtrunkver− tebrae of C. spinosus are shorter than in C. portai. This is a re− sult of the zygapophyses being laterally oriented in C. spinosus, producing a short neural arch, and values of the centrumlengthmuchlowerthanthewidthoftheneuralarchin the middle (cl/naw < 1). In contrast, the zygapophyses are more anterolaterally directed in C. portai and the centrum length is subequal to or greater than the width of the neural arch in the middle (cl/naw 1). In addition, the paracotylar notches and subcentral grooves seem to be relatively more marked in C. spinosus than in C. portai. The neural spine is high, clearly distinctive, very robust, with the main axis verti− cal in C. spinosus, but it is very low and reduced to a small tu− bercle in C. portai. The dia− and parapophyseal articular sur− faces are weakly distinguishable in C. spinosus, but they are undistinguishable in C. portai. Furthermore, the zygosphene of C. portai is thin to moderate, whereas it is usually thicker in C. spinosus. Basedon thesecharacters,it is possible to support the recognition of two species of Colombophis.

Recently, Head et al. (2006: fig. 1A) assigned one pre− cloacal vertebra from the middle Miocene of Venezuela to Colombophis cf. C. portai (AMU−CURS 154). According to the authors, the specimen is morphologically indistinguish− able from the specimens of C. portai from the middle Mio− cene of the La Venta Fauna. Nevertheless, the description of this specimen and the direct observation of its features are consistent with the vertebral morphology of C. spinosus.A c− cording to the description of Head et al. (2006), this speci− men shows no paracotylar foramina (congruent with the intracolumnar variation of Colombophis) and has paradiapo− physes strongly divided. The latter is a character that con− trasts with the diagnosis of the genus, but according to our observations, AMU−CURS 154 displays paradiapophyses weakly divided into two articular facets, where the diapo− physis is slightly convex and the parapophysis is rather con− cave, which support its reference to C. spinosus. In addition, this vertebra is evidently short (neural arch and centrum), the zygapophyses are laterally oriented and define a very short interzygapophysealconstriction, the neuralspine looks higher than in C. portai, and the zygosphene is thick, all characters observed inC. spinosus.

Stratigraphic and geographic range.—Eight trunk vertebrae (UFAC−PV 1609, 2952, 2955, 2956, 3485 4027, 5716C, and 5716E)recoveredfrom the Talismã locality, Purus River; one vertebra (UFAC−PV 5424) collected at the Morro do Careca locality. All of them come from the Solimões Formation, late

Miocene, Amazonas State, Brazil. The vertebra IGM 184176 (1) belongs to the La Venta Fauna, La Victoria Formation (Duke University Locality 084), Honda Group, middle Mio− cene, Colombia. The material at the AMU−CURS is from the UpperMemberof the Socorro Formation, middle Miocene of Venezuela.

Discussion

Traditionally recognized as “Anilioidea”, this group of basal alethinophidians is comprised of taxa that retain certain liz− ard−like features and are as well specialized to fossorial habits (Greene,1997).“Anilioidea”isconsideredbysomeauthorsto be a paraphyletic group (Rieppel 1988; Rage 1998; Lee and Scanlon 2002; Vidal and Hedges 2002, 2004; Wilcox et al. 2002; Gower et al. 2005). Recent molecular evidence is now quite strong in favor of splitting Anilius (as close relative of tropidophiidss.s.) and Uropeltidaes.l. (Cylindrophis, Anomo− chilus, uropeltines),as closer relativesof booids, pythons and advanced snakes (Wiens et al. 2008). Traditionally,the “ani− lioids” include the South American genus Anilius (red pipe snake or false coral snake), the Asian Anomochilus (dwarf pipe snakes) and Cylindrophis (Asian pipe snake), and the Uropeltidaefamily (shield−tailedsnakes) (Greene 1997). The three former genera are generally included in the Aniliidae, although there is no consensus about its monophyly (Rage 1998;Lee and Scanlon 2002).Six fossil genera have been de− scribed for the group, and nearly all are tentatively referred to the family Aniliidae (Australophis Gómez, Báez, and Rou− gier, 2008; Colombophis Hoffstetter and Rage, 1977; Conio− phis Marsh,1892;Eoanilius Rage,1974;HoffstetterellaRage, 1998; and Michauxophis Bailon, 1988). Although placement amongthe “Anilioidea”is wellsupportedfor mostgenera,the set of snakes allocated to Coniophis shows a large range of variation and represents probably a paraphyletic or polyphy− letic grouping of pre−macrostomatan snakes (Rage 1998).

The genus Colombophis was reported from the middle

Miocene of Colombia and Venezuela, in northern South America (Hoffstetter and Rage 1977; Hecht and LaDuke 1997; Head et al. 2006). Hence, the new material described in this paper extends the record of the genus to the late Mio− cene of southwestern Brazilian Amazonia.

All previous descriptive works on Colombophis agree in including this genus in the “Anilioidea” (Hoffstetter and Rage 1977; Hecht and LaDuke 1997; Head et al. 2006), although comparisons with other snakes have not been reported. The new vertebral remains of Colombophis from the middle Mio− cene of Colombia and Venezuela, and the late Miocene of southwestern Brazilian Amazonia, provide some basis for re− vision of the genus and consideration of its affinities.

The diagnosis of the genus Colombophis was originally based on around 40 midtrunk vertebrae fromthemiddleMio− cene of the Villavieja Formation, Colombia (Hoffstetter and Rage 1977). According to the authors, the vertebral morphol− ogy of Colombophis is similar to that of the extant “anilioid” doi:10.4202/app.2009.1

HSIOU ET AL.—MIOCENE SNAKES FROM SOUTH AMERICA 375

Cylindrophis, differing in their size and their undivided para− diapophyses (Hoffstetter and Rage 1977). Later, Hecht and LaDuke (1997), based on new material from the same forma− tion, added a new character to the diagnosis of Colombophis: the unusual placement of the subcentral foramina, which oc− curs close to the sagittal plane and just posterior to the level of the paradiapophyses; however, this condition is also observed in most “Anilioidea” (our personal observation). Hecht and LaDuke (1997) made amistakeduring theEnglish translation of the French diagnosis of the genus as provided by Hoffstetter and Rage (1977), because according to the last authors, the articular facets of the zygapophyses are notice− ably inclined above the horizontal, whereas Hecht and LaDuke (1997) considered that they are slightly inclined.

Some features of Colombophis are shared with Dinilysia patagonica Woodward, 1901, a Late Cretaceous basal snake from Patagonian Argentina. Both are of medium to large size and have vertebrae with the following characteristics: depressed neural arch, long and strongly inclined zygapo− physes, short prezygapophyseal process, and a variable pres− ence of paracotylar foramina. However, Dinilysia shows a straight (not notched) posterior border of the neural arch (Rage and Albino 1989; Scanferla and Canale 2007). Despite variable neural spine height in Colombophis (see below), C. spinosus displays a well developed neural spine as in Dinilysia. In the latter taxon, however, the neural spine is blade−like and posteriorly inclined, with an elongated base, rising close to the dorsal edge of the zygosphene; thus, it is different from the neural spine of both C. spinosus and C. portai, which is restricted to the posterior end of the neural arch. Dinilysia also differs from Colombophis in having: a better developed haemal keel in midtrunk vertebrae, the ante− rior edge of the zygosphene strongly notched, and an anteri− orly widened vertebral centrum. According to Apesteguía and Zaher (2006), Najash rionegrina, the earliest limbed snake from Patagonian Argentina, shows the neural arch flat− tened without posterodorsal notch, but the vertebrae of this genus are characterized by the presence of parazygantral fo− ramina on each side of the zygantrum and the absence of prezygapophyseal process, as in the extinct Madtsoiidae, dif− fering considerably fromColombophis.

Some authors indicate a probable relationship between

Colombophis and the extant uropeltids (McDowell 1987; Szyndlar 1994); nevertheless, the large size of Colombophis and the presence of neural spine and haemal keel, especially in C. spinosus, contrast markedly with uropeltid vertebrae, which are small and strongly modified for fossorial habits, losing the neural spine and haemal keel. These and other characters, such as the long prezygapophyseal process, and condyles and cotyles markedly oval, differentiate the primi− tive Scolecophidia from Colombophis , although the frequent presence of large subcentral foramina is reminiscent of this group (Hoffstetter and Rage 1977).

In spite of numerousrecordsin most continents, the fossils assigned to the “Anilioidea” usually consist of isolated verte− brae, and the characters that support the identifications are thought to be mostly primitive. The vertebrae of the extant “Anilioidea” Anilius and Cylindrophis share the following characters also present in Colombophis: a clearly depressed neural arch; prominent and strongly inclined zygapophyses; short prezygapophyseal process; a shallow median notch in the posterior border of the neural arch; and a centrum not markedly widened anteriorly. In the comparison of Colom− bophis with extinct and extant “anilioids”, the inclination of the prezygapophyses at more than 20 is a character−state shared with Australophis, Hoffstetterella, Anilius,a nd Cylin− drophis (Rage1998;Gómezet al. 2008;ourpersonalobserva− tion). The exceptions are Eoanilius and Michauxophis,w hich displayalmosthorizontalprezygapophyses(Rage1974;Bailon 1988; Szyndlar 1994); and Coniophis, in which the condition is variable (Hecht 1959; Rage 1984, 1998; Albino 1990). Ac− cording to Lee andScanlon (2002),an inclination between15° and 30° is interpreted as an intermediate condition in modern snakes. Our observations support this statement.

A posterior margin of the neural arch not well−notched in dorsal view is observed in all genera of “Anilioidea” (Rage 1998; Gómez et al. 2008), although Coniophis has an almost rectilinear posterior edge (Albino 1990) and Eoanilius, Hof− fstetterela, and Colombophis have a relatively deeper median notch (Hoffstetter and Rage 1977; Rage 1998; our personal observation). The absence of a strong notch of the neural arch is considered a plesiomorphic condition in snakes (Lee and Scanlon 2002).

Colombophis shares with “anilioids”, especially with Ani− lius, Cylindrophis, Australophis,a nd Hoffstetterella, the pres− ence of a small and robust prezygapophyseal process (Rage 1998; Gómez et al. 2008; our personal observation), which is consideredan intermediatecondition(Lee and Scanlon2002) that, among other characters, distinguishes “anilioids” from more derived snakes, such as Acrochordidae and most Colu− broidea, which have longer processes (Rage 1984; Holman 2000; Lee and Scanlon 2002; Ikeda 2007).

As said above, the depressed neural arch of Colombophis and “anilioids” is frequently present in other primitive snakes such as Dinilysia, Najash, Scolecophidia, and Uropeltidae. The centrum not markedly widened anteriorly is found in the two last groups (Rage 1984; Rage and Albino 1989). Thus, the combination of character states that Colombophis shares with “anilioids” are mostly present in primitive snakes.

Other characters of Colombophis are less broadly distrib− uted. Concerning the neural spine, Colombophis differs from Australophis, Hoffstetterella, some species of Eoanilius, and Anilius, because these taxa have a thin, blade−like neural spine with an elongated base that rises close to or in the midline of the neural arch, being anteroposteriorly inclined. Colombophis spinosus shares with Hoffstetterella a neural spine relatively better developed than in the other mentioned genera, but it is higher in C. spinosus than Hoffstetterella. Other “anilioid” genera (the extant Cylindrophis and the ex− tinct Coniophis, Eoanilius, and Michauxophis) have a low and posteriorly restricted neural spine as in C. portai. Among snakes, the presence of a low neural spine is considered a de− rived condition by Lee and Scanlon (2002). This feature is common in extinct and extant “anilioids”, and implies that, if C. spinosus is considered an “anilioid”, it would be an excep− tion within this group. In conjunction with the position and shape of the neural spine, Colombophis shows a large smooth or slightly concave area between the dorsal margin of zygosphene and the neural spine. This character is also pres− ent in Cylindrophis, Coniophis, Michauxophis, and some Eoanilius specimens.

The dia− and parapophysial surfaces of the paradiapo− physes are slightly distinguishable in C. spinosus, whereas C. portai has indistinguishable paradiapophyses(Hoffstetter and Rage1977;HechtandLaDuke1997).Rage(1998)comments that the dia− and parapophysis are slightly different from one another in Hoffstetterella, Cylindrophis,a nd Michauxophis, whereas they are not distinguishable in Colombophis portai, Anilius, and some species of Coniophis, and variably distin− guishable in Eoanilius, Coniophis platycarinatus,a nd C. pre− cedens. The presence of slightly divided paradiapophyses is also observed in some specimens of Anilius (our personalob− servation)andAustralophis(Gómezetal.2008).According to some authors, distinguishable dia− and parapophysis is a de− rivedconditionfoundin allalethinophidiansnakes(Rieppelet al. 2002; Apesteguía and Zaher 2006), although it should be considered present in many but not all alethinophidians all (e.g.,all macrostomatans and various “anilioids”, Jean−Claude Rage, personal communication 2009). Thus, the presence of undivided paradiapophyses in C. portai is primitive.

Althoughthe haemalkeelisvariable alongthe column,itis more developed and prominent in the posterior portion of the vertebral centrum, which is in part different from some “ani− lioids”. In Hoffstetterella, the haemal keel is a low blade poorly delimited laterally by subcentral grooves (Rage 1998). In Coniophis, it is broadand flat, somewhatdelimited laterally bysubcentralgrooves(seeAlbino1990;Rage1998),buthasa very convex surface (also in Eoanilius, which displays a large convex ventral surface). Colombophis differs from Anilius in which the projecting part of the haemal keel extends further anteriorly. It differs from Cylindrophis because in this genus the centrumisextremely convex,althoughsomewhatrounded anteriorly like in Colombophis. Although showing a flattened haemal keel, Australophis somewhat resembles the condition observedin Colombophis, in which the keel is slightly promi− nent in the median portion of the vertebra, being delimited by the subcentral grooves(Gómezet al. 2008).In the mostposte− rior portion of the haemal keel of Australophis there are two rounded depressions, one on each side of the distal margin of the haemal keel (Gómez et al. 2008). This character contrasts with the presence of the laterally paired projections that Co− lombophis shows in the same place, reminiscent of the poste− riorapophysesofsomemadtsoiidsnakes(Rage1998;Scanlon 1997, 2005) and not reported in other “anilioid”genus. Scan− lon (1997, 2005) interpreted these projections as an autapo− morphic condition of madtsoiids, which could be correlated with intracolumnarvariation; however,its presencein Colom− bophis is probably an independent acquisition.

In addition, some characters of Colombophis are not pres− ent in any extant or extinct “Anilioidea”. The most conspicu− ous of these characters are the large size and the presence of paracotylar foramina in many vertebrae. The vertebrae of Colombophis are larger than those of all other fossil and ex− tant “anilioids” (Table 2); the considerable disparity in verte− bral size between specimens is consistent with intracolumnar variation. The presence of paracotylar foramina is irregular in Colombophis. Some specimens have one or more foram− ina on each side of the cotyle (Hoffstetter and Rage 1977; our personal observation), whereas others do not show any fo− ramina (our personal observation). Anilius and Cylindrophis, as well as the extinct “anilioid” taxa, do not exhibit para− cotylar foramina (Rage 1974, 1984; Bailon 1988; Albino 1990; Gómez et al. 2008). According to Lee and Scanlon (2002), the presence of paracotylar foramina on most or all vertebrae, as seems to be the case in Colombophis,i sa plesiomorphic condition.

Basedon the detailed comparisons made above,the affini− ties of Colombophis with “Anilioidea” still cannot be re− solved, because many characters are plesiomorphies, shared with other primitive snakes. Also, Colombophis is distin− guished from all known extinct and extant “anilioids” due to its greatvertebralsize and the frequentpresenceof paracotylar foramina. The posterior paired apophyses of the haemal keel in some vertebrae, and the high neural spine of C. spinosus, also contrast significantlywithall extinct and extant “anilioid” genera. The allocation of the genus into this probably para− phyletic group is not well supported at present.

The combination of characters found in Colombophis is not present in any other extant or fossil snake, supporting its identity as a distinct genus; however, the fact that many of these features are observed in primitive snakes suggests that Colombophis belongs among the broad array of basal ale− thinophidian snakes.

Conclusions

In this paper we report the first record of Colombophis from the Solimões Formation, late Miocene of Southwestern Bra− zilian Amazonia. This record extends the distribution of the genus to the southeast during the Miocene, and implies its survival until the late Miocene. Reassessment of the genus permits the recognition of the new species Colombophis spinosus. The allocation of the genus into the probably para− phyletic “Anilioidea” cannot be resolved for the moment and it should be considered a probable basal alethinophidian of uncertain affinities.

The presence of Colombophis in the middle Miocene of

Colombia and Venezuela, and the late Miocene of Brazil (Hoffstetter and Rage 1977; Hecht and LaDuke 1997; Head et al. 2006; this paper) suggests the possibility of general eco− logical similarity among these Miocene faunas. This resem− blance is also supported by the presence of the boid snake Eunectes and the teiid lizard Paradracaena in La Venta doi:10.4202/app.2009.1

HSIOU ET AL.—MIOCENE SNAKES FROM SOUTH AMERICA 377 fauna and Brazilian Amazonia (Hsiou and Albino 2009; Hsiou et al. 2009). Some authors report similarities among these faunas based on mammalian fossils, but finding more affinities of the southwestern Brazilian Amazonia with Uru− maco than with La Venta (Cozzuol 2006).

The Solimões Formation, southwestern Brazilian Ama− zonia, includes a freshwater vertebrate fauna (rodents, croco− diles, turtles, and freshwater fishes) and, together with paly− nological data, indicates open areas and forest galleries along rivers, swamps, and shallow lakes. It would have been sub− ject to variation in the water level in a seasonal dry−humid tropical climate (Latrubesse et al. 2007). For the Urumaco Fauna, in the Socorro Formation, there is a scenario that in− cludes deltaic and fluvial deposits (Hambalek et al. 1994) with crocodiles, freshwater turtles, and catfishes which in− habited swamps, associated with other kinds of catfishes, sharks, and sirenians frequent in estuarine environments and in large freshwater rivers (Aguilera 2004; Sánchez−Villagra 2006). The La Venta Fauna is a continental deposit, with di− verse and abundant freshwater fishes, turtles, and crocodili− ans indicative of aquatic habitats that developed in a tropical rainforest, mixed with forest/grassland mosaics and open grasslands (Kay and Madden 1997). The presence of similar fossil snakes in southwestern Brazilian Amazonia, Urumaco, and La Venta is consistent with these restorations.

The vertebralmorphology of Colombophis, especially that ofC.spinosus, is in partcompatible with the lifestyle proposed for Dinilysia patagonica due to the combination of medium− large size, depressed neural arch, and high neural spine. Ac− cordingtoAlbinoandCaldwell(2003),thevertebralmorphol− ogy of Dinilysia indicates a semi−burrowing or semi−aquatic lifestyle. Considering the proposed paleoenvironment for the Solimões Formation, the habitsof Colombophis arewell com− patible with a semi−aquatic lifestyle.

Acknowledgements

Thanks also to Jonas P. Souza−Filho, Moisés B. de Souza, and Andrea Maciente (UFAC) for loaning of the fossil material from southwestern Brazilian Amazonia; to Hussam Zaher (MZUSP) and Francisco L. Franco (IB) for the permission to visit the herpetological collections; toJavierGuerrero(UniversidadNacionaldeColombia,Bogotá,Colom− bia) and RichardMadden(DukeUniversity, Durham, USA) for permis− sion to study fossil snakes from La Venta Fauna (material that is part of the Duke University/INGEOMINAS project); to Orangel A. Aguilera (UNEFM−CIAAP)andRodolfoSánchez(AMU−CURS)forpermission to study the Miocene fossil snakes from Venezuela; to Raul O. Gómez (UBA,BuenosAires,Argentina) Aires for the measurements of Austra− lophis; to Marco A.G. França (USP, Ribeirão Preto, Brazil) and Elizete C. Holanda (PPGGeociências/UFRGS, Porto Alegre, Brazil) for many comments and suggestions; to Juan C. Cisneros (UFPI, Teresina) for language revision; and to Luís F. Lopes (IG/UFRGS) for photography; and to Richard L. Cifelli (University of Oklahoma, USA) and three anonymous referees for their careful reviews and helpful suggestions. We thank CNPq (Conselho Nacional de DesenvolvimentoCientífico e Tecnológico)for financialsupport to ASH duringher study at Universi− dade Federal do Rio Grande do Sul (PPGGeociências/UFRGS).

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(Parte 3 de 4)

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