Hsiou & Albino, 2009 - Presence of the Genus Eunectes (Serpentes, Boidae) in the Neogene of Southwestern Amazonia, Brazil

Hsiou & Albino, 2009 - Presence of the Genus Eunectes (Serpentes, Boidae) in the...

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Presence of the Genus Eunectes (Serpentes, Boidae) in the Neogene of Southwestern Amazonia, Brazil

ANNIE S. HSIOU1,2 AND ADRIANA M. ALBINO 3

1Secao de Paleontologia, Museu de Ciencias Naturais, FZB-RS, Av. Salvador Franca, 1427, CEP: 90690-0,

Jardim Botanico, Porto Alegre, RS, Brazil; E-mail: anniehsiou@gmail.com 3CONICET, Departamento de Biologıa, Universidad Nacional de Mar del Plata, Funes 3250, 7600 Mar del Plata, Argentina; E-mail: aalbino@mdp.edu.ar

ABSTRACT.—The extant genus Eunectes was first reported for the Middle Miocene of Colombia, represented by the extinct species Eunectes stirtoni. Here, we describe vertebral remains referable to this genus collected in the Neogene Solimoes Formation at the Talisma locality, situated on the right-hand bank upstream of the Purus River, in the South of Amazonas State, Brazil. The material consists of isolated mid- and posterior trunk vertebrae characterized by the following combination of features that distinguishes the genus from other Neotropical boids: large size, slightly depressed neural arch, relatively low neural spine, robust and moderately thick zygosphene, with a prominent median tubercle, paracotylar foramen irregularly present, and a strong lateroventral projection of the paradiapophyses on the posterior trunk vertebrae. The presence of Eunectes in the Solimoes Formation represents the first fossil record of snakes from the southwestern Brazilian Amazonia and supports the origin of this genus in the Miocene or before.

The Neotropical boids, represented by the genera Boa, Corallus, Epicrates, and Eunectes, constitute a well-supported clade of snakes (Burbrink, 2005; Noonan and Chippindale, 2006). The genus Eunectes (Anacondas) includes large semiaquatic snakes that occur in rivers and fresh water lakes, from Venezuela and Colombia to Argentina (Peters and Oreja-Miranda, 1970; Stafford, 1986). Currently, four species are recognized: Eunectes murinus, Eunectes deschauenseei, Eunectes notaeus, and Eunectes beniensis. Among them, the Green Anaconda, E. murinus, has the broadest distribution, occurring in forested environments of Bolivia, Brazil, Colombia, Ecuador, Guiana, French Guiana, Peru, Trinidad, and Venezuela. Eunectes deschauenseei (Dark-Spotted Anaconda) lives in the savanna of northeastern Brazil (including Marajo Island) and the coastal regions of French Guiana, whereas E. notaeus (Yellow Anaconda) occurs in Mato Grosso State of Brazil and eastern Bolivia to northern Argentina (Henderson et al., 1995). The least known species is E. beniensis (Beni Anaconda), restricted to Bolivia (Dirksen, 2002). Despite its broad recent distribution, fossils of the genus Eunectes are known only from the Middle Miocene of Colombia and represented by the extinct species Eunectes stirtoni (Hoffstetter and Rage, 1977). However, the validity of this species has been questioned (Hecht and La- Duke, 1997).

The aim of this paper is to describe the vertebral remains of snakes referable to the genus Eunectes coming from the probable Late Miocene Solimoes Formation at the Talisma˜ locality (southwestern Brazilian Amazonia) and to discuss their significance. Geological Setting and Biochronology.—The ver- tebral remains were collected at the fossiliferous locality of Talisma (08u489220S, 68u489120W), situated on the right-hand bank upstream of the Purus River, in Amazonas State, between the mouth of the Iaco River and the municipality of Manuel Urbano, Brazil (Fig. 1A). According to Cozzuol (2006), the section is dominated by fine sediments, mainly silts and clays, with gypsum and calcite veins in the lower part and manganese stains in the upper part, both probably digenetic. The deposits are characterized by massive bedding with no evident lamination. Two fossiliferous levels were found at 1.7 and 7 m above water level (Fig. 1B).

The age of the fossils found in the Solimoes

Formation at Talisma and their relations to other South American fossiliferous localities are controversial because of poorly established correlations between the different stratigraphical levels of the distinct fossiliferous localities where the formation is exposed, which is further complicated by the absence of radiometric datings (Cozzuol, 2006; Latrubesse et al., 2007). According to Latrubesse (1992) and Latrubesse et al. (1997), the mammal fauna of Southwestern Brazilian Amazonia was deemed to correspond to the Huayquerian (Late Miocene) and possibly reached the Montehermosan2Corresponding Author.

Journal of Herpetology, Vol. 43, No. 4, p. 612–619, 2009 Copyright 2009 Society for the Study of Amphibians and Reptiles

(Late Miocene-Early Pliocene). Based on palynological data obtained in typical fossiliferous localities, Latrubesse et al. (2007) suggested a Late Miocene age for the Solimoes Formation. The snake material we studied was collected at the Talisma locality, which is considered by some authors as belonging to the Huayquerian- Montehermosan (Late Miocene/Pliocene) because of the presence of the rodents Potamarchus murinus and Neopliblema horridula (Santos et al., 1993; Negri, 2004). According to Santos and Negri (1993), the faunal set of xenarthrans (Tardigrada) suggests, on one hand, a probable affinity with the fauna of the Santacrucian Age of Argentina (Early-Middle Miocene) and, on the other, a relation with the Laventan Age of Colombia (Middle Miocene). According to Negri (2004; unpubl. data), the faunistic association of Tardigrada in this locality would indicate an older age, correlatable and close to the Laventan (13.5–1.8 Ma, Madden et al., 1997). Here, we follow the arguments of Latrubesse et al. (2007) and assume a probable Late Miocene age for the Solimoes Formation.

The specimens are satisfactorily preserved and are stored at UFAC (Rio Branco, AC, Brazil). They include three midtrunk vertebrae and one posterior trunk vertebra very well preserved and three incomplete midtrunk vertebrae. Skeletons of extant boids were used for comparisons (Appendix 1). Osteological nomenclature and measurements follow Auffenberg (1963), Hoffstetter and Gasc (1969), Rage (1984), LaDuke (1991a,b), and Lee and Scanlon (2002). Systematic arrangement used is based on Noonan and Chippindale (2005). Measurements are expressed in millimeters.

FIG. 1. Location map (A) and the stratigraphic profile of the fossiliferous locality Talisma (B) (adapted from Cozzuol, 2006; Photo taken from w.ufac.br).

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Vertebral Measurements.—cl, centrum length; coh, condyle height; cow, condyle width; cth, cotyle height; ctw, cotyle width; h, total high of the vertebrae; naw, neural arch width at interzygapophyseal ridge; nch, neural canal height; ncw,neural canal width; nsh, neural spine height; po-po, distance between postzygapophyses; prpr, distance between prezygapophyses; pr-po, distance between pre- and postzygapophyses of the same side; prl, prezygapophysis length; prw, prezygapophysis width; zh, zygosphene height; zw, zygosphene width.

Institutional Abbreviations.—HAA, private herpetological collection of Adriana Albino; HASH, private herpetological collection of Annie Schmaltz Hsiou; IB, Instituto Butantan, Sao Paulo; MCN.D., Didactic Collection of Herpetology, Museu de Ciencias Naturais, Fundacao Zoobotanica do Rio Grande do Sul, Porto Alegre; MZUSP, Museu de Zoologia, Universidade de Sao Paulo, Sao Paulo; UFAC-PV, Paleovertebrate Collection of the Laboratorio de Pesquisas Paleontologicas, Universidade Federal do Acre, Rio Branco.

Systematic Paleontology Serpentes Linnaeus, 1758

Alethinophidia Nopsca, 1923 Macrostomata Muller, 1831

Booidea Gray, 1825 Boidae Gray, 1825

Eunectes Wagler, 1830

Eunectes sp. Figure 2

Referred Specimens.—Three almost complete midtrunk vertebrae (UFAC-PV 2951, 2954/2960, 3475) and one almost complete posterior trunk vertebra (UFAC-PV 3476).

Description.—The specimens are very well preserved. In general view, the vertebrae are large and robust. All of the vertebrae are wide, high and short, with a vertebral centrum shorter than the neural arch width (cl , naw). In

FIG.2 . Eunectes sp. Midtrunk vertebrae, UFAC-PV 2951 (A), UFAC-PV 2954/2960 (B), and UFAC-PV 3475 (C); posterior trunk vertebra, UFAC-PV 3476 (D); in (1) anterior, (2) posterior, (3) lateral, (4) dorsal, and (5) ventral views; scale-bars 5 10 m.

614 A. S. HSIOU AND A. M. ALBINO anterior view, a wide and robust zygosphene, with fairly long articular facets, is observed. The zygosphene is much wider than the cotyle (zw . ctw) and shows a slightly convex or rectilineous dorsal edge. The prezygapophyses are inclined above the horizontal plane on the midtrunk vertebrae (Fig. 2A–C), and nearly horizontal on the posterior trunk vertebra (Fig. 2D). The prezygapophysial process is well preserved in the posterior vertebra; it is short and stands a little beyond the articular facet (Fig. 2D). The neural canal is triangular and bears three internal crests: one located on the floor and two on the lateral walls, which together produce a trilobated aspect. In the midtrunk vertebrae, the cotyle is oval, slightly flattened dorsoventrally (ctw . cth), whereas it is round in the posterior trunk vertebra (ctw 5 cth). In only one specimen (UFAC-PV 2954/ 2960), there is a large pair of paracotylar foramina, one on each side of the cotyle. The paradiapophyses are fragmented hindering further detail; however, they are apparently robust and lateral-ventrally oriented. In the posterior trunk vertebra, a large lateroventral expansion of the paradiapophyses is observed, resembling a large transverse process (Fig. 2D).

In posterior view, the neural arch roof is slightly depressed in the midtrunk vertebrae (Fig. 2A–C) and more depressed in the posterior trunk vertebra (Fig. 2D). The posterodorsal notch of the neural arch is quite deep, and the neural spine (only preserved in UFAC-PV 3475) is relatively low, with a vertical crest that is the continuation of the posterior edge of the neural arch. The zygantrum is robust and deep, with the small zygantral foramina located on each side of the vertebra midline. The postzygapophyses are slightly inclined dorsally. The condyle is oval, slightly flattened dorsoventrally in the midtrunk vertebrae (cow . coh) and nearly round in the posterior trunk vertebrae (cow , coh).

In lateral view, the neural spine is robust, well developed but relatively low, slightly inclined posteriorly (observed in UFAC-PV 3475, Fig. 2C). It is anteroposteriorly shortened and starts posterior to the roof of the zygosphene. Lateral foramina are present on each side of the neural arch. The centrum is short, showing a welldefined and delimited precondylar constriction. The main axis of the condyle is slightly inclined upward. Ventrally to the condyle, a posteriorly projected haemal keel is observed, which nearly reaches the precondylar constriction.

In dorsal view, the neural arch is wider than long (pr-pr . pr-po) and relatively wider than the total height of the vertebra (pr-pr . h). The articular facets of the prezygapophyses are broad, long (prl . prw) and subtriangular, with its main axis anterolaterally oriented. The anterior edge of the zygosphene is slightly concave but shows a prominent median tubercle anteriorly projected and located just above the neural canal in the midtrunk vertebrae (Fig. 2A–C). In the posterior vertebra, the tubercle resembles a ‘‘tongue’’ that projects anteriorly above the dorsal edge of the neural canal (Fig. 2D). The roof of the neural arch shows a pronounced flexion that starts at the level of the upper angle of each zygantrum up to the basis of the articular facets of the zygosphene. The neural arch presents, on the posterior edge, a deep notch in the middle, beginning at the mentioned flexion. The interzygapophyseal ridge, extending between the prezygapophysis and postzygapophysis on each side of the vertebra, is curved and short but not much constricted.

In ventral view, the vertebral centrum is short (cl , naw) and triangular, wider anteriorly, with subcentral ridges well defined. The haemal keel is well developed longitudinally on the midline of the ventral surface of the centrum. It originates at the ventral edge of the cotyle, becoming more prominent and wider in the midportion of the vertebral centrum. There is a pair of small subcentral foramina, one on each side of the haemal keel. The postzygapophyses show large articular facets with a subtriangular form.

cf. Eunectes sp. Figure 3

Referred Specimens.—Three incomplete midtrunk vertebrae (UFAC-PV 2958, 2959, and 3477).

Description.—The specimens UFAC-PV 2958 and 2959 are fragments of nearly complete midtrunk vertebrae. The first specimen is the right side of a precloacal vertebra, and the second, the left side. Neither specimen presents the dorsal portion of the neural arch. In these samples, it is possible to observe the anterolateral orientation of the prezygapophyses and the

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presence of a short prezygapophysial process (more visible on the ventral surface of the articular facet). The paradiapophyses are quite fragmented and lateroventrally oriented. The vertebral centrum is short and anteriorly broadened, with a well-developed and thin haemal keel on the ventral surface. The condyle is large and slightly flattened dorsoventrally. The specimen UFAC-PV 3477 is rather fragmented and, because of the depressed aspect of the neural arch from a posterior view, seems to be a vertebra of the posterior trunk region. The poor preservation and fragmentation of the material allow us only a tentative assignation to the genus Eunectes.

Comparisons and Comments on the Characters.—

The material described in this paper shares the following combination of vertebral characters with the genera ofNeotropical boids: very robust, high, short, and wide vertebrae; neural arch not strongly depressed; neural spine well developed; posterior edge of neural arch with a marked notch; robust zygosphene; low inclination of the articular facet of the prezygapophysis (less than 15u); short prezygapophyseal process; vertebral centrum shorter than the width of the neural arch; delimited precondylar constriction; haemal keel in the vertebrae of the midtrunk region instead of a hypapophysis; presence of subcentral, lateral and paracotylar foramina (Rage, 2001;

Lee and Scanlon, 2002; Szyndlar and Rage, 2003; Albino and Carlini, 2008).

The vertebrae are assigned to the extant genus Eunectes on the basis of the following features: large size; slightly depressed neural arch; moderately low neural spine; robust and moderately thick zygosphene with a prominent median tubercle; paracotylar foramen irregularly present; and a strong lateroventral orientation of the paradiapophyses on the posterior trunk vertebrae.

Within the Neotropical boids, the midtrunk vertebrae are similar to samples of midsized individuals of the genera Eunectes and Boa, differing from the smaller size of Corallus and Epicrates.I n Eunectes and Corallus, as in the fossils, the midtrunk vertebrae are usually lower than in Boa and Epicrates.

The neural arch of the fossil material and

Eunectes is slightly depressed on the midtrunk vertebrae, differing from the condition in Boa and Corallus (except Corallus cropanii), which have a high neural arch, and in Epicrates, which shows an intermediate condition (Rage, 2001; pers. obs.).

The midtrunk vertebrae of the fossil material show a lower neural spine than in Boa and Epicrates. Rage (2001) argues that the neural spine is high in Boa, Corallus cropanii, Epicrates, and Eunectes, but less high in other Corallus species. These conclusions do not coincide with our observations of the osteological material (Appendix 1) where vertebrae of Eunectes have a proportionally low neural spine. This character seems to be variable among species and specimens. Nevertheless, the neural spine of Corallus is anteroposteriorly elongated, whereas it is shortened in the fossils as in Eunectes.

FIG. 3. cf. Eunectes sp. Midtrunk vertebrae, UFAC-PV 2958 (A) in dorsal (1) and ventral (2) views; UFAC-PV 2959 (B) in dorsal (1) and ventral (2) views; and UFAC-PV 3477 (C); in (1) anterior, (2) posterior, (3) lateral, (4) dorsal, and (5) ventral views; scale bars 5 10 m.

616 A. S. HSIOU AND A. M. ALBINO

The zygosphene of Eunectes, Epicrates, and

Corallus are distinctively wider and thinner than in Boa, but Eunectes shows a more robust zygosphene than the other two genera (Camolez, 2006; pers. obs.). According to Albino and Carlini (2008), Boa constrictor shows a very thick and robust zygosphene, different from that of the other genera. The zygosphene of the fossil material is wide and moderately thick, resembling the condition in Eunectes. Another feature in the zygosphene is a conspicuous median tubercle that projects anteriorly, between the dorsal edge and the neural canal, on the midtrunk vertebrae of the fossil material and Eunectes. In the fossil posterior trunk vertebra, this tubercle is tongue-shaped, projecting above the dorsal edge of the neural canal, as in posterior trunk vertebrae of extant specimens of Eunectes. The anterior edge of the zygosphene in the vertebrae of Boa shows a V-shaped notch in dorsal view, or it is often concave, without any trace of a median tubercle (Albino and Carlini, 2008). According to Camolez (2006), Epicrates presents an anterior blade on the zygosphene, whereas Corallus shows a ‘‘crenate’’ zygosphene, as that described by Auffenberg (1963).

The relative length of the centrum and the proportions of the prezygapophyseal surfaces observed in the fossil specimens and Eunectes also distinguishes them from Boa, which has a shorter centrum and longer prezygapophysis than the other genera (Albino and Carlini, 2008). The fossil posterior trunk vertebra shows a larger lateroventral expansion of the paradiapophyses, resembling a large transverse process, as observed in posterior vertebrae of extant specimens of Eunectes through direct comparisons (Appendix 1).

According to Kluge (1991), the presence of paracotylar foramina on both sides of the cotyle is a derived character state, shared, within Neotropical boids, by Boa and some species of Corallus. However, it was also observed in one fossil specimen here studied (UFAC-PV 2954/ 2960) and in two extant specimens of E. murinus (MCN.D. 306 and 342). The presence of this foramen in extant specimens of E. murinus is irregular; often they only appear on one side of the cotyle, rarely a pair, although the presence of one pair on each side of the cotyle has also been observed. The fossil vertebrae are distinguished from Boa, Corallus annulatus, and C. cropanii because in these genera the foramina are always present (Kluge, 1991; Rage, 2001; Albino and Carlini, 2008). The polarity of this foramen is controversial (Kluge, 1991; Rage, 2001) but its presence in one fossil specimen studied here represents a similarity with the species E. murinus.

According to Camolez (2006), the species of

Eunectes do not show differences in the morphology of the precloacal vertebrae, although some differences are noticeable in the caudal vertebrae. Unfortunately, no postcloacal vertebrae have been preserved among the fossils, making their identification to the species level impossible at the moment, apart from the similarity in the presenceofparacotylarforamina inonespecimen as in E. murinus. Additionally, there are distinctions in the body dimensions of the extant species that can be compared with the studied fossils. The extant species of Eunectes stand out for being large snakes, among which, E. murinus is considered one of the largest snake known, with individuals reaching 1.4 m (Pope, 1961, 1962; Rivas, 1999). Eunectes murinus (usually 3 m for males and 6 m for females, Waller and Micucci, 1993; Rivas and Burghardt, 2001) is much larger than E. notaeus (generally 3 m for females) and E. deschauenseei (2 m in length) (Waller and Micucci, 1993). According to our observations, the vertebral fossil material shows a similar size to vertebrae belonging to midsized individuals of the species E. murinus.

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