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Diagnosis: Siphonops annulatus can be distinguished by the following combination of characters: a maximum known total length of 450 mm (Maciel and Hoogmoed 2011); annuli numbering 78–98 (Taylor 1973); annular grooves that completely encircle the body, except for three or four posteriormost annuli near the vent (Maciel and Hoogmoed 2011).
Description: Siphonops annulatus measures 286-450 mm in total length (lower end of range, Taylor 1968; higher end of range, Maciel and Hoogmoed 2011). The total length is 17-26x the body width (Taylor 1968). This species has a cylindrical body, slightly wider than deep (Maciel and Hoogmoed 2011). The number of primary annuli ranges from 78-98 (Taylor 1968). Primary annuli completely encircle the body except for the anteriormost primary annulus and several posteriormost annuli near the vent (Maciel and Hoogmoed 2011). The head is narrower than the body and is longer than wide (Maciel and Hoogmoed 2011). Eyes are small and externally visible (Taylor 1968), in open sockets that are elevated just above the surface of the head (Maciel and Hoogmoed 2011). The tentacle aperture is closer to the eye than the nostril (Taylor 1968). The snout projects beyond the mouth (Maciel and Hoogmoed 2011). Nuchal grooves are distinct on both the dorsum and venter, except where the second collar is partially fused on the ventral surface with the first primary annulus (Maciel and Hoogmoed 2011). A dorsal tranverse groove is present on each collar, though it is less distinct and somewhat shorter on the first collar (Maciel and Hoogmoed 2011). On the first collar, the ventral transverse groove may be present or absent (Maciel and Hoogmoed 2011). Dermal scales are absent (Maciel and Hoogmoed 2011). The vent is at the terminus of the body and no true tail is present (Maciel and Hoogmoed 2011). A large unsegmented terminal shield extends from the anterior of the vent to the posteriormost part of the body (Maciel and Hoogmoed 2011). The vent opening may be I-shaped, T-shaped, or subcircular (Taylor 1968). Anal denticulations number 9-10 (Maciel and Hoogmoed 2011). The skull is stegokrotaphic, with closed temporal regions (Kleintech et al. 2008). Premaxillary-maxillary teeth are monocuspid and reach a maximum number of 43 (Taylor 1968). Prevomerine-prepalatine teeth are also monocuspid, reach a maximum number of 47 (Taylor 1968), and are smaller than premaxillaries/maxillaries (Maciel and Hoogmoed 2011). Dentary teeth are monocuspid, reach a maximum number of 32 (Taylor 1958), and are slightly larger than premaxillaries/maxillaries (Maciel and Hoogmoed 2011). Only the right lung is developed in Siphonops annulatus; the left lung is atrophied (Kuehne and Junqueira 2000). The male cloaca is simple, with paired sets of longitudinal ridges that are positioned dorsally, ventrolaterally, and ventromedially, and lacks blind sacs; the female cloaca is also simple, with five major ridges but no transverse folds (Wake 1972).
This caecilian is bluish-black to slate in color, with grooves edged in white or cream (Taylor 1968). The ventral coloration is primarily dark ultramarine (Taylor 1968). The head is lighter in color on the dorsal surface, with small white spots at the tentacle aperture and nostril (Taylor 1968). A white spot also covers the vent area (Taylor 1968). Females brooding young are paler than other adults (Wilkinson et al. 2008).
Distribution and Habitat
Country distribution from AmphibiaWeb's database: Argentina, Bolivia, Brazil, Colombia, Ecuador, French Guiana, Guyana, Paraguay, Peru, Suriname, Venezuela
Siphonops annulatus is thought to have the broadest known distribution of any terrestrial caecilian species (Taylor 1968; Wilkinson et al. 2008), though it has also been pointed out that this species needs taxonomic review (Lavilla et al. 2010). It is found in tropical South America ranging east of the Andes from northern Colombia, Ecuador, Peru, Venezuela, and the Guianas, south through most of Brazil to (probably) Paraguay and into northern Argentina (Lavilla et al. 2010). In Argentina, this species is found in the provinces of Misiones and Corrientes (Lavilla et al. 2000; Álvarez et al. 2002). In Bolivia, it is found in Beni, La Paz, Pando and Santa Cruz (de la Riva et al., 2000) . In Brazil it occurs in the states of Espírito Santo (Tonini et al. 2010) and São Paulo (Araújo et al. 2009). In Colombia this species has been reported from the Villavicencio region at the base of the Cordillera Occidental by Lynch (2000) and Lynch (2006). In Venezuela it is found in the states of Barinas (Reinthaler and Fistar 2002; Barrio-Amorós and Rodríguez, C. M.) and Portuguesa (Lavilla et al. 2010-confirm). Its presence in Paraguay is assumed but has not been confirmed (Brusquetti and Lavilla 2006). Dunn (1942) reported this species to be present in Suriname, and it is listed in Nussbaum and Hoogmoed (1979), but this has not been confirmed by more recent collecting expeditions (Maciel and Hoogmoed 2011). This species is generally found below 800 m asl. (Taylor 1968). It is fossorial and occurs in a variety of habitats; in Brazil, for instance, it has been recorded from Caatinga (Freitas and Silva 2007), Cerrado (Colli et al. 2002), the Atlantic forest (Taylor 1968; Tonini et al. 2010), and Amazonian Brazil (Maciel and Hoogmoed 2011). Lynch (2006) remarked that this species appeared somewhat tolerant of dry conditions, finding it common under decomposing African oil palm tree trunks even in disturbed habitat such as grazed pastures.
Life History, Abundance, Activity, and Special Behaviors
Siphonops annulatus lives in damp environments rich in organic matter where invertebrates are plentiful. It is common in humus-rich soils to a depth of 20 cm, particularly in cacao plantations of southern Brazil (Jared et al. 1999).
Siphonops annulatus is oviparous (first reported by Göldi 1899) with large, transparent eggs (Wilkinson et al. 2008). Females have been observed to curl their bodies around their eggs, but do not display aggressive egg-defending behavior (Jared et al. 1999). Wilkinson et al. (2008) reported that litters ranged from 5-16 offspring. Hatchlings are small, approximately 40 mm in length, altricial, and whitish, with bodies much narrower than their heads (Wilkinson et al. 2008). The offspring withdraw when disturbed, but readily return to their original positions when the disturbance is gone (Jared et al. 1999). This behavior suggests that the mother and young may use chemical communication to locate one another (Jared et al. 1999).
S. annulatus exhibits an unusual form of parental care known as maternal dermatophagy, where the offspring consume maternal skin for nourishment. Attending mothers have specialized skin, enriched in lipids. Offspring have specialized dentition. In contrast to adult S. annulatus, which bear a single row of monocuspid teeth in the lower jaw, older nestlings (140 mm in total length) have 44 spoon-shaped teeth on the lower jaw arranged alternately in three rows, with each nestling tooth bearing multiple claw-like cusps on the distal side. Feeding bouts are short, involve the entire clutch simultaneously, and lasting only about seven minutes, followed by long periods of quiescence. In captivity, one family group was observed to undergo two bouts of feeding which were separated by 64 hours. During feeding, the offspring move rapidly over and around the mother, biting her lipid-rich skin and peeling off its outer layer. The mother remains calm while the young frenetically tear pieces of skin by spinning along their long body axis, even struggling with one another over the same piece of skin. The young continue to search for and eat fragments of skin even after the mother's skin has been peeled off (Wilkinson et al. 2008). To view a video of skin feeding, see the BBC link: http://news.bbc.co.uk/2/hi/science/nature/7235205.stm.
In addition to maternal dermatophagy, offspring may imbibe liquid exuded from the maternal cloacal opening. An attending female, coiled up, was observed to raise her body terminus vertically, exposing the vent; offspring congregated around the vent, pressing against it and apparently consuming the clear liquid exuded from the maternal vent. This imbibing behavior has not yet been observed in other amphibians; the content and function of the imbibed fluid are unknown (Wilkinson et al. 2008). It can be seen in the same BBC link provided above: http://news.bbc.co.uk/2/hi/science/nature/7235205.stm.
Maternal dermatophagy is also known from a second, distantly related African caecilian species (Boulengerula taitanus), suggesting that skin feeding is an ancient form of caecilian parental care and may have persisted for more than 100 million years (Wilkinson et al. 2008).
The diet of wild adult S. annulatus most likely includes soil-dwelling invertebrates, such as earthworms, termites, crickets, slugs, and snails (Jared et al. 1999). Potential predators include burrowing mammals, ants, and snakes (Jared et al. 1999), such as the colubrid Clelia clelia (Sawaya 1937) or the aniliid Anilius scytale (Greene 1983).
This species has toxic skin secretions, which have been noted to cause partial paralysis or death in rats and the anurans Bufo ictericus and Leptodactylus ocellatus (Sawaya 1940, cited in Jared et al. 1999).
There is extensive literature on the morphology, histology, and physiology of Siphonops annulatus. Comparative analyses have been conducted on morphology of caecilian gonads and fat bodies, including S. annulatus (Wake (1968); morphology of the caecilian kidneys and urogenital ducts (Wake 1970a); morphology of the caecilian bladder (Wake 1970b); morphology of the caecilian cloaca, (Wake 1972). For histology of the kidney and bladder of Siphonops annulatus, see Carvalho and Junqueira (1999); for histology of the trachea and lung, see Kuehne and Junqueira (2000); for granulocyte cytochemistry and morphology, see Gutierre et al. (2008); for the morphology of the capillary bed of the central nervous system, see Craigie (1941); for brain morphology, see Kuhlenbeck (1922); for comparative analyses of caecilian jaw-closing mechanics, using S. annulatus and two other species of caecilians, see Kleinteich et al. (2008); for caecilian metabolic activity and respiratory and circulatory physiology, see Bennett and Wake (1974), Mendes (1941), Sawaya (1941). and Mendes (1945).
Trends and Threats
Siphonops annulatus occurs in many protected areas, such as Reserva Biológica de Duas Bocas, in the state of Espírito Santo, southeastern Brazil (Tonini et al. 2010). It can tolerate disturbed habitat (Lavilla et al. 2010).
Species authority: Mikan (1820). Older literature may refer to Siphonops annulatus but encompass several different forms now considered distinct (Wake 1972).
Bachmann, K., Goin, O. B., and Goin, C. J. (1972). ''Nuclear DNA amounts in vertebrates.'' Evolution of Genetic Systems. H. H. Smith, eds., Gordon and Breach, New York.
Bennett, A. F., and Wake, M. H. (1974). ''Metabolic correlates of activity in the caecilian Geotrypetes seraphini.'' Copeia, 1974(3), 764-769.
Brusquetti, F., and Lavilla, E. O. (2006). ''Lista comentada de los anfibios de Paraguay.'' Cuadernos de Herpetologia, 20, 3-79.
Carvalho, E. T. C. and Junqueira, L. C. U. (1999). ''Histology of the kidney and urinary bladder of Siphonops annulatus (Amphibia-Gymnophiona).'' Archives of Histology and Cytology, 62, 39-45.
Colli, G. R., Bastos, R. P., and Araujo, A. F. B. (2002). ''The character and dynamics of the Cerrado herpetofauna.'' The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna. P. S. Oliveira and R. J. Marquis, eds., Columbia University Press, New York.
Craigie, E. H. (1941). ''The capillary bed of the central nervous system in a member of a second genus of Gymnophiona - Siphonops.'' Journal of Anatomy, 76, 56-64.
De la Riva, I., Köhler, J., Lötters, S. and Reichle, S. (2000). ''Ten years of research on Bolivian amphibians: updated checklist, distribution, taxonomic problems, literature and iconography.'' Revista Espanola de Herpetologia, 14, 19-164.
Dunn, E. R. (1942). ''The American caecilians.'' Bulletin of the Museum of Comparative Zoology, 91(6), 439-540.
Freitas, M. A., and Silva Santos, T. F. (2007). Guia Ilustrado: A Herpetofauna das Caatingas e Áreas de Altitude do Nordeste Brasileiro. USEB, Pelotas.
Gower, D. J., and Wilkinson, M. (2005). ''Conservation biology of caecilian amphibians.'' Conservation Biology, 19(1), 44-45.
Greene, H. W. (1983). ''Dietary correlates of the origin and radiation of snakes.'' American Zoologist, 23, 431-441.
Gutierre, R. C., Egami, M. I., Antoniazzi, M. M., and Jared, C. (2008). ''Cytochemistry and morphology of granulocytes of the caecilian Siphonops annulatus (Amphibia, Gymnophiona).'' Comparative Clinial Pathology, 17, 221-228.
Göldi, E. A. (1899). ''Über die Entwicklung von Siphonops annulatus.'' Zoologische Jahrbücher. (Abt. Syst.), 12, 170-173.
Jared, C., Navas, C. A., and Toledo, R. C. (1999). ''An appreciation of the physiology and morphology of the caecilians (Amphibia: Gymnophiona).'' Comparative Biochemistry and Physiology, 123, 313–328.
Kleinteich, T., Haas, A., and Summers, A. P. (2008). ''Caecilian jaw-closing mechanics: integrating two muscle systems.'' Journal of the Royal Society Interface, 5, 1492-1504.
Kuehne, B., and Junqueira, L. C. U. (2000). ''Histology of the trachea and lung of Siphonops annulatus (Amphibia, Gymnophiona).'' Revista Brasileira de Biologia, 60, 167-172.
Kuhlenbeck, H. (1922). ''Zur Morphologie des Gymnophionengehirns.'' Jenaische Zeitschrift für Naturwissenschaft , 58, 453-484.
Lavilla, E., Hoogmoed, M., Reichle, S., Baldo, D., Wilkinson, M., and Measey, J. 2010. Siphonops annulatus. In: IUCN 2011. IUCN Red List of Threatened Species. Version 2011.2. www.iucnredlist.org. Downloaded on 05 April 2012.
Lavilla, E.O., Ponssa, M.L., Baldo, D., Basso, N., Bosso, A., Cespedez, J., Chebez, J.C., Faivovich, J., Ferrari, L., Lajmanovich, R., Langone, J.A., Peltzer, P., Ubeda, C., Vaira, M., and Vera Candioti, F. (2000). ''Categorización de los Anfibios de Argentina.'' Categorización de los Anfibios y Reptiles de la República Argentina. E. O. Lavilla, E. Richard, and G. J. Scrocchi, eds., Asociación Herpetológica Argentina, Tucumán, Argentina.
Mendes, E. G. (1945). ''Contribuição para a fisiologia dos sistemas respiratório e circulatorio de Siphonops annulatus (Amphibia-Gymnophiona).'' Boletim da Faculdade de Philosophia Ciências e Letras da Universidade de São Paulo , 1945, 25-67.
Mendes, E. G. (1941). ''Sobre a respiração (esofágica, traquéal, e cutânea) do Siphonops annulatus (Amphibia-Gymnophiona).'' Boletim da Faculdade de Philosophia Ciências e Letras da Universidade de São Paulo, 1941, 283-304.
Mikan, J. C. (1820). Delectus Florae et Faunae Brasiliensis. Vindobonae, Antonii Strauss.
Nussbaum R. A., and Hoogmoed, M. S. (1979). ''Surinam caecilians, with notes on Rhinatrema bivittatum and the description of a new species of Microcaecilia (Amphibia, Gymnophiona).'' Zool. Meded. Rijksmus. Nat. Hist. Leiden, 54, 217-235.
Sawaya, P. (1941). ''Contribuição para o estudo da fisiologia do sistema circulatório do anfíbio Siphonops annulatus (Mikan).'' Boletim da Faculdade de Philosophia Ciências e Letras da Universidade de São Paulo , 1941, 207-270.
Sawaya, P. (1937). ''Die Blindwühle Siphonops annulatus (Mikan) als Nahrung der ‘Mussurana.’ Pseudoboa cloelia (Daud.).'' Zoologischer Anzeiger, 118, 169-171.
Sawaya, P. (1940). ''Sobre o veneno das glandulas cutaneas, a secreção e o coração de Siphonops annulatus.'' Boletim Faculdade de Filosofia, Ciências e Letras, Universidade de São Paulo, Serie Zoologia, 4, 207-270.
Taylor, E. H. (1973). ''A caecilian miscellany.'' University of Kansas Science Bulletin, 50, 188-231.
Taylor, E.H. (1968). The Caecilians of the World. A Taxonomic Review. University of Kansas Press, Lawrence, Kansas.
Wake, M. H. (1968). ''Evolutionary morphology of the caecilian urogenital system. Part I. The gonads and the fat bodies.'' Journal of Morphology, 126, 291-331.
Wake, M. H. (1970). ''Evolutionary morphology of the caecilian urogenital system. Part II. The kidneys and the urogenital ducts.'' Acta Anat., 75, 321-358.
Wake, M. H. (1970). ''Evolutionary morphology of the caecilian urogenital system. Part III. The bladder.'' Herpetologica, 26, 120-128.
Wake, M. H. (1972). ''Evolutionary morphology of the caecilian urogenital system. Part IV. The cloaca.'' Journal of Morphology, 136, 353-365.
Wilkinson, M., Kupfer, A., Marques-Porto, R., Jeffkins, H., Antoniazzi, M. M., and Jared, C. (2008). ''One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona).'' Biology Letters, 4, 358-361.
Written by Nelly Chow and Kellie Whittaker (nelly AT berkeley.edu), UC Berkeley
First submitted 2010-02-02
Edited by Kellie Whittaker (2012-05-16)
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