Siphonops annulatus (Mikan, 1822)
|Species Description: Mikan, JC. 1822. “Delectus Florae et Faunae Brasiliensis.” Fasicule 2. Vindobonae: Antonii Strauss.|
© 2018 Mauro Teixeira Jr (1 of 15)
Siphonops annulatus measures 286 - 450 mm in total length (Taylor 1968; Maciel and Hoogmoed 2011), which is 17 - 26 times the body width (Taylor 1968). The head is narrower than the body and is longer than wide (Maciel and Hoogmoed 2011). The skull is stegokrotaphic, with closed temporal regions (Kleintech et al. 2008). The premaxillary-maxillary teeth are monocuspid and reach a maximum number of 43 (Taylor 1968). The prevomerine-prepalatine teeth are also monocuspid, reach a maximum number of 47 (Taylor 1968), and are smaller than premaxillaries/maxillaries (Maciel and Hoogmoed 2011). The dentary teeth are monocuspid, reach a maximum number of 32 (Taylor 1958), and are slightly larger than premaxillaries/maxillaries (Maciel and Hoogmoed 2011). The 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. This species has a cylindrical body, slightly wider than deep (Maciel and Hoogmoed 2011). The 78 – 98 primary annuli (Taylor 1968) completely encircle the body except for the anteriormost primary annulus and several posterior most annuli near the vent (Maciel and Hoogmoed 2011). The 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. A dorsal transverse groove is present on each collar, though it is less distinct and somewhat shorter on the first collar. On the first collar, the ventral transverse groove may be present or absent. Dermal scales are absent. The vent is at the terminus of the body and no true tail is present. A large, unsegmented terminal shield extends from the anterior of the vent to the posterior most part of the body (Maciel and Hoogmoed 2011). The vent opening may be I-shaped, T-shaped, or subcircular (Taylor 1968). There are 9 – 10 anal denticulations (Maciel and Hoogmoed 2011). The male cloaca is simple, with paired sets of longitudinal ridges that are positioned dorsally, ventrolaterally, and ventromedially, and lack blind sacs. The female cloaca is also simple, with five major ridges but no transverse folds (Wake 1972). Only the right lung is developed in Siphonops annulatus; the left lung is atrophied (Kuehne and Junqueira 2000).
Siphonops annulatus can be distinguished from Gymnopis syntrema due to the former having larger maximum known total length of 450 mm (Maciel and Hoogmoed 2011), annuli numbering 78 – 98 (Taylor 1973), and annular grooves that completely encircle the body except for three or four posterior most annuli near the vent (Maciel and Hoogmoed 2011).
In life, this caecilian is bluish-black to slate in color, with grooves edged in white or cream. The ventral coloration is primarily dark ultramarine. The head is lighter in color on the dorsal surface, with small white spots at the tentacle aperture and nostril. A white spot also covers the vent area (Taylor 1968). Females brooding young are paler than other adults (Wilkinson et al. 2008).
While caring for the eggs, females are the typical greyish-blue of the species, however, after hatching the maternal color changes to opaque whitish blue. This is the only time that there is obvious external sexual dimorphism (Jared et al. 2019).
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. 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 (presumably) 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 2010) and Portuguesa (Lavilla et al. 2010). 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) in a variety of fossorial habitats but is most common in damp environments, rich in organic matter where invertebrates are plentiful (Jared et al. 1999).
Life History, Abundance, Activity, and Special Behaviors
Siphonops annulatus 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. However, S. annulatus is most well known in damp environments with rich organic matter where invertebrates are plentiful. It is also common in humus-rich soils to a depth of 20 cm, particularly in cacao plantations of southern Brazil (Jared et al. 1999).
In captivity, two copulating pairs were observed for a very brief time. Both times the individuals stayed belly up with an increase in gular movements (Jared et al. 2019).
Siphonops annulatus is oviparous (first reported by Göldi 1899) with large, transparent eggs in clutches of 5 – 16 eggs (Wilkinson et al. 2008). Eggs are laid in humid, well protected, but shallow nests at the bases of large trees within roots that act as walls. Within the nests there was a round chamber just big enough to fit the coiled mother’s body. The vitelline membranes of adjacent eggs formed connecting strings in egg litters just after oviposition. Strings can get crossed and the clutch resembles ‘a bunch of grapes’ (Jared et al. 2019). Females have been observed to curl their bodies around their eggs, but do not display aggressive egg-defending behavior (Jared et al. 1999).
The diet of wild adult S. annulatus most likely includes soil-dwelling invertebrates, such as earthworms, termites, crickets, slugs, and snails. 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).
Siphonops 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 and 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 only last approximately 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 link: http://news.bbc.co.uk/2/hi/science/nature/7235205.stm, and this from newscientist: https://www.youtube.com/watch?v=6K6szXrBHwM&feature=youtu.be.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).
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).
Development of offspring takes the biggest leap within the first week, body mass increases around 130%. In captivity, during parental care mothers were not observed eating. Once the young become independent the mothers go back to feeding normally (Jared et al. 2019).
When offspring are removed or separated from their mother for a short period of time, they will return to her. Rejoining or finding the mother appears to depend on the offspring but the behavior suggests that the mother and young may use chemical communication to locate one another (Jared et al. 2019)
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).
This species was featured in News of the Week on September 25, 2023:
Do caecilians face selective pressure from elapid snake predators? A study by Mancuso et al (2023) searched for clues in neurotoxin fighting systems in 37 caecilian species, representing all currently known families of caecilians in the Americas, Africa, and Asia, and the Seychelles. Three types of caecilian resistance neurotoxins were identified. The study demonstrated that resistance to alpha-neurotoxins convergently evolved at least fifteen times across the caecilian tree (three times in Africa, seven times in the Americas, and five times in Asia). In addition, several species were shown to possess multiple resistance modifications acting synergistically, thus they concluded that caecilians must have undergone at least 20 separate events involving the origin of toxin resistance. In contrast, resistance in non-caecilian amphibians was found to have arisen only five separate times. Together, the mutations underlying resistance in caecilians constitute a robust signature of positive selection, which strongly correlates with elapid presence through both space (sympatry with caecilian-eating elapids) and time (Cenozoic radiation of elapids). This study demonstrates the extent of convergent evolution that can be expected when a single widespread predatory adaptation triggers parallel evolutionary arms races at a global scale. (Written by Vance Vredenburg).
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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.
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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.
Originally submitted by: Nelly Chow and Kellie Whittaker (first posted 2010-02-02)
Description by: Michelle S. Koo, (updated 2023-09-23)
Distribution by: Michelle S. Koo (updated 2021-03-18)
Life history by: Michelle S. Koo (updated 2021-03-18)
Trends and threats by: Michelle S. Koo (updated 2021-03-18)
Edited by: Kellie Whittaker, Maxine Weber, Michelle S. Koo (2023-09-23)
Species Account Citation: AmphibiaWeb 2023 Siphonops annulatus: Ringed Caecilian <https://amphibiaweb.org/species/1939> University of California, Berkeley, CA, USA. Accessed Dec 2, 2023.
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Citation: AmphibiaWeb. 2023. <https://amphibiaweb.org> University of California, Berkeley, CA, USA. Accessed 2 Dec 2023.
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