1 REPTILIA: TESTUDINES: PODOCNEMIDIDAE Podocnemis sextuberculata
Catalogue of American Amphibians and Reptiles 913
Iverson, J. B., L. Schneider, and R. C. Vogt. 2017. Podocnemis sextuberculata.
Podocnemis sextuberculata Cornalia Six-tubercled River Turtle, Iaçá, Pitiú, or Cupiso
Podocnemis sextuberculata Cornalia 1849:13. Figure 1 Mature female Podocnemis sextuber- Type locality: “Fl. Amazonum” [=Ama- culata in Parana da Floresta (a tributary of the zon River], South America. Holotype (a Rio Branco which is a tributary of the Rio Negro), hatchling): Not located; originally in the Roraima, Brazil. Photograph by Richard C. Vogt. Milano Museum (Roger Bour, personal communication). Collected by G. Oscu- CONTENT. No subspecies are recognized. lati (Vanzolini 1977b), date unknown (see Remarks). Not examined by authors. DEFINITION. Podocnemis sextuberculata Podocnemis expansa: Gray 1856:61 (in part). is one of the smaller species of Podocnemis, Podocnemis pitiu Silva Coutinho 1868:150. reaching a carapace length of only 34 cm Type locality: “l’Amazone” [Amazonas, (Vogt 2008a, 2008b, 2008c). The domed cara- Brazil]. Holotype specimen, collector, pace is elliptical and broader behind the cen- and collection date unknown. Not exam- ter. The posterior carapacial rim is serrated ined by authors. in juveniles, but only slightly so or smooth in Bartlettia pitipii Gray 1870:720. Type lo- adults; a cervical indentation may be present. cality: “Lakes of the Upper Amazons.” A blunt medial keel is present on vertebrals Syntypes (Four mentioned by Gray, but V2 and V3. All vertebrals are broader than only three listed by Boulenger [1889] long with V1 and V5 the smallest, and V5 and in the catalog of the British Mu- posteriorly expanded. Surfaces of the carapa- seum of Natural History of London cial scutes are usually smooth in adults and [BMNH]): BMNH 1946.1.22.90 (adult in show few, if any growth annuli. The carapace alcohol), 1947.3.5.82 (adult, stuffed), and is gray to olive brown. The plastron is large, 1947.3.5.83 (adult, skeleton), collected by but does not completely cover the carapacial Edward Bartlett (date unknown). Not ex- opening; the anterior lobe is rounded in front amined by authors. and the posterior lobe is broader posterior- Emys amazonica: Baur 1893:213 (in part). Re- ly. The anal scutes are decidedly tapered and sult of inappropriate synonymy of E. am- much narrower than the femorals; a shallow azonica Spix 1824 (= Podocnemis expan- medial posterior notch is present. A unique sa) with P. sextuberculata Cornalia and character (which gives this turtle both its sci- Bartlettia pitipii Gray. entific and English common names) is the Bartlettia pitipiti: Williams 1954:281. Lapsus. presence of six pairs of prominent tubercles Podecnemis sextuberculata: Medem 1960:347. on the plastron of juveniles. These tubercles Lapsus. occur at the base of the bridge on the pec- Podocnemys sextuberculosa: Voženílek toral and abdominal scutes and at the outer 1981:85. Lapsus. posterior point of the femorals. These protu- Podocnemis sextuber culata: Chegodayev berances disappear with age, although those 2002:82. Lapsus. on the pectoral scutes may persist into adult- 2
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? 1000 km ? ? Map 1. Distribution of Podocnemis sextuberculata derived from Ferrara et al. 2017. A single dot may represent multiple adjacent localities; question marks adjacent to dots indicate unverified localities.
Figure 2. Mature adult female Podocnemis sex- Figure 3. Mature adult female Podocnemis sex- tuberculata with spotted head pattern. This un- tuberculata. Photograph taken in the Mamirauá usual pattern only occurs in tributaries of the Rio Sustainable Development Reserve, Amazonas, Branco, Roraima, Brazil. Photograph by Richard Brazil by Rafael Bernhard. C. Vogt. 3
Figure 4. Plastron of adult female Podocnemis sextuberculata demonstrating persistent protu- berances on pectoral scutes. Photograph taken in the Mamirauá Sustainable Development Reserve, Amazonas, Brazil by Rafael Bernhard. Figure 5. Plastron views of adult females (top row) and adult males (middle and bottom rows). Females have V-shaped notches in their anal hood. A long intergular separates the gulars. scutes, and adult males have larger U-shaped in- The bridge is not as broad as the width of the dentations in their anal scutes. The plastral color- plastral posterior lobe. Both plastron and ation in males and females can range from solid bridge are yellow to gray or brown. The broad light yellow to cream or mottled brown; the dark- head has a protruding snout and notched er colorations often are stains absorbed from the upper jaw. There is only a single weak ridge water they live in. Photograph taken in the Ma- on the triturating surface of the maxilla. The mirauá Sustainable Development Reserve, Ama- premaxillae separate the maxillae and extend zonas, Brazil by Rafael Bernhard. to the choanal rim. The incisive foramina lie completely within the premaxillae. There is DIAGNOSIS. The body size is small rel- no vomer. The interparietal scale is elongat- ative to other Podocnemis (to only 34 cm ed and widely separates the parietals, which, carapace length; Vogt 2008a, 2008b, 2008c). although also elongated, do not touch be- The species name derives from the presence hind the interparietal. Large subocular scales of three pairs of prominent protuberances are usually present. A deep groove lies be- on the sides of the plastron, and the axillary tween the orbits, and the tympanum is about pair is often still obvious in adults (Williams as broad as the orbit. One or two chin bar- 1954). Several characters can be used to dis- bels are present. The head is olive to reddish tinguish Podocnemis sextuberculata from its brown with cream-colored jaws. The neck is five congeners: the forehead is grooved, the dark gray to olive dorsally but lighter colored masseteric scale does not reach the orbit, the ventrally; limbs are gray to olive. However, interparietal scale usually widely separates the head coloration in the Rio Branco drain- the parietal scales, large subocular scales are age is different: most females retain the juve- present, the jugal bone contacts the parietal nile color pattern of light yellow or light green bone, the vomer is absent, the shell is always markings on the head (see Remarks). Three smooth, the dorsal surface of marginal six is large scales occur on the posterior margin of more than half as wide as long, there are three the hind foot. Males have longer, thicker tails large scales on each hind foot and two chin than do females. barbels are present (Williams 1954). 4
Williams (1954). Cervical vertebrae were de- scribed by Williams (1950), hatchling anato- my by Malvasio et al. (2002), jaw musculature by Schumacher (1954), neural bone variation by Pritchard (1988), plastral anatomy by Ca- dena et al. (2012b) and Gaffney et al. (2006), throat morphology by Magalhães et al. (2014) and Vogt et al. (1998), and comparisons with other species by Müller (1935), Siebenrock (1902), and Williams (1954). The karyotype was described by Ayres et al. (1969), Barros et al. (1976), Bull and Legler (1980), Fantin Figure 6. Normal patterned adult female (left) and dos Santos Monjeló (2011), Gunski et al. and male Podocnemis sextuberculata from Rio (2013), Killebrew (1975), Ortiz et al. (2005), Trombetas, Para, Brazil. Adult males are small- Rhodin et al. (1978), and Ventura et al. (2014). er than adult females. Photograph by Richard C. Vogt. ILLUSTRATIONS. Color photographs were published by Alves et al. (2012), Balensiefer et PHYLOGENETIC RELATIONSHIPS. The al. (2007), Bartlett and Bartlett (2003), Bonin relationships among the six species of Podoc- et al. (1996, 1998, 2006a, 2006b), Castaño-Mo- nemis are still uncertain. A tree based on un- ra (2002), Ceballos et al. (2012), Ferrara et published mitochondrial DNA data was pre- al. (2017), Ferri (1999, 2002), Ferronato and sented by Iverson et al. (2007: erythrocephala Morales (2012), Franklin (2007), Kato (1992), (sextuberculata (lewyana (unifilis (expansa, Koshikawa (1996), Lehr (2002), Nascimen- vogli))))), one based on mitochondrial and to et al. (2012), Obst (1986a, 1986b), Obst nuclear DNA sequences was published by et al. (1984, 1988), Páez (2013), Pritchard Vargas-Ramírez et al. (2008: expansa (vog- (1979), Rogner (1996), Rueda-Almonacid et li (sextuberculata (unifilis (lewyana, eryth- al. (2007), Soini and Cóppula (1995), Vetter rocephala))))), and one based on combined (2005), Vogt (2008a, 2008b, 2008c), and Zhou morphological and molecular data was pub- (2004). Color illustrations were presented lished by Cadena et al. (2012a: expansa (vog- by Bonin et al. (1996, 1998, 2006a, 2006b) li (sextuberculata (erythrocephala (lewyana, and Freiberg (1981). Black-and-white pho- unifilis))))). The molecular phylogeny pub- tographs were published by Carillo de Es- lished by Pereira et al. (2017), based on 13 pinoza (1970), Ernst and Barbour (1989), mitochondrial and nuclear gene loci, is iden- Ferreira (1923), Gaffney et al. (2011), Mitter- tical to that published by Vargas-Ramírez et meier (1975), Neill (1965), Pritchard (1979), al. (2008). and Smith (1979a, 1979b). Black-and-white illustrations were presented by Bonin et PUBLISHED DESCRIPTIONS. General al. (1996, 1998, 2006a, 2006b), Boulenger descriptions were provided by Bonin et al. (1889), Cadena (2011), Castaño Mora (2002), (1996, 1998, 2006a, 2006b), Carvalho et al. Gaffney et al. (2011), Gray (1870), Honegger (2002), Castaño Mora (2002), Ceballos et et al. (1985), King and Burke (1989), Muel- al. (2012), Ernst and Barbour (1989), Hoge ler (1998), Siebenrock (1902), Wermuth and (1952), Honegger et al. (1985), King and Mertens (1961). and Williams (1954). Burke (1989), Mittermeier (1975, 1978), Neill (1965), Pritchard (1967, 1979), Siebenrock DISTRIBUTION. Podocnemis sextubercu- (1902, 1904), Vogt (2008a, 2008b, 2008c), and lata is known in the Amazon River drain- 5 age of northern Brazil, southern Colombia and northeastern Peru (Castro 2007; Iverson A 1986, 1992; Lehr, 2000; Ramo 1982; The IUCN Conservation Monitoring Centre 1988). Dis- tributional information was published for Colombia by Ceballos-Fonseca (2000), Ce- ballos et al. (2012), and Medem (1958, 1960, 1969); for Brazil by Da Silva et al. (2016) and Hoogmoed and de Avila-Pires (1990); and for Perú by Carrillo de Espinoza (1970), Carrillo de Espinoza and Icochea (1995), Dixon and Soini (1977, 1986), Ferronato and Morales (2012), Lehr (2002), and Rodriguez and Knell (2004a, 2004b). Extralimital introductions B were listed by Iverson and Etchberger (1989), King and Krakauer (1966), and Kraus (2009).
FOSSIL RECORD. No fossils are known; however, the Eocene Podocnemis olssoni is similar to living Podocnemis sextuberculata (Schmidt 1931).
PERTINENT LITERATURE. General re- views were published by Bartlett (1996), Cantarelli and Herde (1989), Ceballos et al. C (2012), David (1994), Ferrara et al. (2017), Freiberg (1981), Köhler (2004); Moll and Moll (2004), Monzel (2016), Rueda-Almonacid et al. (2007), Schmidt (1931) and Vogt (2008a, 2008b, 2008c). Other information is listed by topic: behavior (Emmons 1989; Malvasio et al. 2003; Nascimento 2002; Venegas and Gagliardi 2013); captive longevity records Figure 7. Hatchlings of Podocnemis sextubercu- (Bowler 1977; Obst 1986a, 1986b; Slavens lata from Rio Trombetas, Para, Brazil. A. Emerg- and Slavens 1991, 2000); captive mainte- ing hatchling. B. Hatchlings. C. Plastron of hatch- nance (Fachín-Terán et al. 1992; Lima 2000); ling displaying six distinct tubercles, giving this capture methods and tracking technologies species its name. Photograph by Richard C. Vogt. (Barboza et al. 2013a; Guilhon et al. 2011); checklists and nomenclature (Artner 2003, 2008; Frank and Ramus 1995; Fritz and Havaš Souza and de Barros Molina 2007; Strauch 2007; Fróes 1957; Goeldi 1906; Hutchins et al. 1890; Turtle Taxonomy Working Group 2014, 2003; Iverson 1985, 1986, 1992; Lamar 1997; 2017; Voženílek 1981; Welch 1994; Wermuth Luederwaldt 1926; Medem 1968; Mertens and Mertens 1961, 1977); conservation (Al- and Wermuth 1955; Mittermeier and Wilson finito 1978; Andrade et al. 2001; Barboza 1974; Młynarski and Wermuth 1971; Mo- et al. 2013b; Camillo et al. 2012; Cantarelli rales-Betancourt et al. 2015; Nascimento et 1994; Cantarelli and Herde 1989; Cantarel- al. 2012; Rhodin et al. 2008; Siebenrock 1909; li et al. 2014; Castaño-Mora 1997; Da Silva 6 and Fachín Terán 2015; Da Silva et al. 2011; Bernhard 2001; Dixon and Soini 1977, 1986; Eisemberg et al. 2017b; Fachín-Terán et al. Erickson et al. 2015; Fachín-Terán et al. 2006; 2003; Fagundes et al. 2016; Forero-Medina et Ferrara et al. 2014; Ferronato and Morales al. 2014; Gomes Lustosa et al. 2016; Groom- 2012; Foote 1978; Freda et al. 2016; Haller bridge 1982; IUCN/SSC Tortoise and Fresh- 2002; Haller and Rodrigues 2006; Ihering water Turtle Specialist Group 1989; Johns 1904; Malvásio 2001; Malvasio et al. 2002; 1987; May et al. 2011; Medem 1958; Mioran- Medem 1960, 1969, 1976; Mittermeier 1978; do et al. 2013; Nöllert 1992; Petzold 1976; Orenstein 2001a, 2001b, 2012; Pezzuti and Pezzuti et al. 2010b; Raeder 2003; Schneider Vogt 1999; Pezzuti et al. 1999, 2000; Portel- et al. 2011b; Soini 1995b, 1995c, 1997, 1999; inha 2010; Santos 2006; Soini 1995a, 1995b, Soini and Cóppula 1995; Soini and Correa 1996; Soini and Cóppula 1995; Soini and de 1995; Vásquez and Tovar 2007; Venegas and Soini 1995a, 1995b; Vanzolini 1977a, 2001; Gagliardi-Urrutia 2013a, 2013b; Vinke and Vanzolini and Gomes 1979); taxonomy and Vinke 2009; Vogt 2008a, 2008b, 2008c; Vogt systematics (Baur 1893; Cadena et al. 2012a; et al. 2017); density/biomass (Vogt and Vil- Honegger et al. 1985; King and Burke 1989; larreal-Benitez 1997); developmental anom- Vargas Ramirez et al. 2008; Viana et al. 2007; alies (Pereira et al. 2014; Perrone et al. 2016); Wood 1979, 1983; Wood and Diaz de Gam- diet (Da Cunha 2013; De Almeida et al. ero 1971); vocalization (Ferrara et al. 2014). 1986; Eisemberg et al. 2017a; Fachín-Terán and Vogt 2014; Fachín-Terán et al. 1995); ef- REMARKS. This species was first described fects of dams (Alho 2011); genetic and mo- on page 13 of Cornalia (1849), but the de- lecular aspects (Corrêa 1978; Oliveira et al. scription was reprinted on page 312 in the 2011; Silva et al. 2011; Viana et al. in press); Appendix of Osculati (1850; see also Oscu- habitat (Da Cunha et al. 2014); hematology lati 1854). Vanzolini (1977b) commented on (Oliveira et al. 2011); historical collections the locality of the type specimen. Because the (Monzel 2016); human attitudes (Alho et al. population in the Rio Branco drainage is iso- 2015; Alves et al. 2012; Pezzuti et al 2010a); lated from all other populations of this species human use for food (Alcântara et al. 2013; by about 1800 km, the genetics of this popu- Fachín-Terán et al. 2004; Fachín Terán et al. lation are being currently studied (by Richard 1996, 2000a, 2000b; Hernández and Espín C. Vogt) to determine whether specific status 2003; Kemenes and Pezzuti 2007; Klemens is warranted. 2000; Klemens and Thorbjarnarson 1995; Lehr 2002; Lemos Lopes et al. 2014; Lopes et ETYMOLOGY. The specific name is from al. 2012; Mittermeier 1978; Morales-Betan- the Latin for six tubercles (sex = six; tuber- court et al. 2015; Pantoja-Lima et al. 2014; culum = a knob or hump), and refers to the Santos 1942, 1955, 1981; Thorbjarnarson et three tubercules on each side of the plastron, al. 2000); mercury and other trace element which are clearly visible in juveniles but dis- bioaccumulation (Burger et al. 2010; Schnei- appear with age. der 2007; Schneider et al. 2010, 2011a); mor- phogenesis (Fabrezi et al. 2009); movements ADDITIONAL VERNACULAR NAMES. (Perrone et al. 2014); parasites (Pineda-Cata- The local Brazilian vernacular name Iaçá lan et al. 2013; Soares et al. 2014); physiology (Mittermeier et al. 1980) is sometimes spelled (Duncan and Marcon 2009; Frair et al. 1978); Aiaça (Mittermeier and Wilson 1974), Aiaçá predation (Bernhard and Vogt 2007; Da Silva (Mittermeier et al. 1980), Aiucá (Mittermeier and Best 1982; Maffei and da Silveira 2013; et al. 1980), Ayacá (Mittermeier et al. 1980), Soini and Cóppula 1995); reproduction (Al- Ayassá (Medem 1968; Mittermeier et al. finito 1978; Bermudez-Romero et al. 2015; 1980) or in Colombia, Ayasá (Medem 1960). 7
In Brazil this species is also known as Pitiú Alves, R. R. N., L. S. Vieira, G. G. Santana, W. (Baillie and Groombridge 1996; Mittermei- L. S. Vieira, W. O. Almeida, W. M. S. Sou- er and Wilson 1974; Mittermeier et al. 1980; to, P. F. G. P. Montenegro, and C. B. Pe- Sokolov 1988), Jurara-pitiu (Vogt 2008a, zzuti. 2012. A review on human attitudes 2008b, 2008c), Juara-pitiú, Cambeua, Cam- toward reptiles in Brazil. Environmental beva (Mittermeier et al. 1980) or Cambêua Monitoring and Assessment 184:6877– (Vogt 2008a, 2008b, 2008c). In Colombia and 6901. Perú this species is known as Cupiso (Baillie Andrade, P. C. M., A. C. Lima, R. G. Silva, and and Groombridge 1996; Carrillo de Espinoza J. A. M. Duarte. 2001. Manejo sustentá- 1990; Medem 1968; Morales-Betancourt et al. vel de quelônios (Podocnemis unifilis, P. 2015) or Teparo (Vogt 2008a, 2008b, 2008c). In sextuberculata, P. expansa e P. erythroce- French this species is known as Podocnémide phala) nos municípios de Terra Santa e tuberculée and Tortue de l’Amazone à six tu- Oriximiná – Paras e Nhamunadá e Parin- bercules (Wrobel 2004). In German this spe- tins – Amazona, “Projeto Pé-de-Pincha”. cies is known as Höcker-Schienenschildkröte Revista de Extenção da Universidade do (Artner 2003; Sokolov 1988; Wrobel 2004). Amazonas. PROEXT/FUA, Manaus / AM This species has also been referred to as the 1:1–25. six-tubercled greaved turtle (Breen 1974) and Artner, H. 2003. Die rezenten Schildkröte- six tubercled Amazon River Turtle (Sokolov narten der Erde. Emys 10(6):iv–xxxviii. 1988; Wrobel 2004). We consider the use of Artner, H. 2008. The world’s extant turtle spe- yellow-headed side-necked turtle (Campbell cies, Part 1. Emys 15(3):4–32. 1974), (six tubercled) Amazonian side-neck Ayres, M., M. M. Sampaio, R. M. S. Barros, L. (Sokolov 1988), and Amazon River Turtle B. Dias, and O. R. Cunha. 1969. A karyo- (Lamar 1997) as erroneous. logical study of turtles from the Brazilian Amazon region. Cytogenetics 8:401–409. LITERATURE CITED Baillie, J. and B. Groombridge (editors). 1996. Alcântara, A. de S., D. F. da Silva; and J. C. B. 1996 IUCN Red List of Threatened Ani- Pezzuti. 2013. Effects of the hydrological mals. IUCN, Gland, Switzerland. 70 + 368 cycle and human settlements on the pop- + 10 pp. ulation status of Podocnemis unifilis (Te- Balensiefer, D. C. and S. M. Holzhausen No- studines: Podocnemididae) in the Xingu velle. 2007. Os Bichos de Casco (R. C. River, Brazil. Chelonian Conservation Vogt, Coordenador). INPA – Instituto and Biology 12:134–142. Nacional de Pesquisas da Amazônia. Ma- Alfinito, J. 1978. Identificação dos principais naus, Brazil. Unpaginated [30 pp.]. tabuleiros de tartarugas no rio Amazonas Barboza, R. S. L., M. S. L. Barboza, and J. C. B. e seus afluentes. Boletim Técnico / Insti- Pezzuti. 2013a. Práticas de pesca de que- tuto Brasileiro de Desenvolvimento Flo- lônio na Várzea Amazíonica (Santarém- restal 5:27–84. -Pará). Amazônica. Revista de Antropo- Alho, C. J. R. 2011. Environmental effects of logia 5(3) Especial:622–653. hydropower reservoirs on wild mammals Barboza, R. S. L., G. H. Rebelo, R. S. L. Bar- and freshwater turtles in Amazonia: A re- boza, and J. C. B. Pezzuti. 2013b. Plano de view. Oecologia Australis 15:593–604. manejo comunitário de jacarés na várzea Alho, C. J. R., R. E. Reis, and P. P. U. Aquino. do baixo rio Amazona, Santarém – PA, 2015. Amazonian freshwater habitats ex- Brasil. Biotemas 26:215–226. periencing environmental and socioeco- Barros, R. M., M. M. Sampaio, M. F. Assis, M. nomic threats affecting subsistence fishe- Ayres, and O. R. Cunha. 1976. General ries. Ambio 44:412–425. considerations on the karyotypic evolu- 8
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