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Home , Chthonerpeton, Gegeneophis, Siphonops, Siphonops annulatus, Siphonops paulensis

Short Communication

SALAMANDRA 41 1/2 91-94 Rheinbach, 20 May 2005 ISSN 0036-3375

Short Communication

Observations on the reproductive ecology of paulensis BOETTGER, 1892 (: ) in

INKA M ONTERO, STEFFEN R EICHLE & ALEXANDER KUPFER

Abstract. show a remarkable diversity of reproductive modes. Due to their secretive lifestyle, basic information on the natural life history of many is lacking. Here we present the first detailed observations of a clutch of the oviparous caecilian . The clutch, guarded by a female, contained four eggs (mean diameter 7.68 ± 0.32 mm). Two unpigmented hatchlings were recorded after 17 days. The available data on the reproductive biology of South-American Siphonops is discussed. Key words. ; oviparity; reproduction.

Caecilians are tropical, limbless, primarily other amphibians (e. g. WAKE 1977). Here, we subterranean amphibians (e. g. DUNN 1942, present data on reproductive parameters for TAYLOR 1968, HIMSTEDT 1996). They show a the oviparous caecilian Siphonops paulensis high diversity of reproductive modes associ- BOETTGER, 1892 from a field site in Bolivia. ated with parental care (WAKE 1977, WILKIN- Siphonops paulensis is a widely distrib- SON & NUSSBAUM 1998). Some caecilians have uted South American caecilian. DUNN (1942) the presumed ancestral life cycle and later TAYLOR (1968) list records from of oviparity with aquatic larvae, as known for (San Ignacio), (Rio Grande many frogs and salamanders (e. g. KUPFER et do Norte, Goiás, Matto Grosso, Rio de Ja- al. 2005). Other oviparous caecilians have neiro, Sao Paulo), (Guaira and Vil- direct development of juveniles with no lar- val stage. Females of oviparous caecilians guard clutches in terrestrial egg chambers (e. g. SARASIN & SARASIN 1887-1890, SANDERSON 1937, GANS 1961, SESHACHAR et al. 1982, HIM- STEDT 1991, MEASEY et al. 2003, FUNK et al. 2004, KUPFER et al. 2004, MEASEY 2004). Other caecilians are viviparous (MOODIE 1978, WAKE 1980, EXBRAYAT & DELSOL 1985, NUSSBAUM & PFRENDER 1998, MEASEY & DI B ER- NARDO 2003) with at least two modes of vivi- parity, characterised by differences in the degree of independence of the newborn (e. g. LOADER et al. 2003). Documenting and inter- preting the reproductive diversity and the Fig. 1. Female Siphonops paulensis attending a evolution of parental care of caecilians has clutch of eggs (A). Two newborns recently hatched been considered key to comparisons with (B).

© 2005 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT) http://www.salamandra-journal.com 91 Short Communication larica) and Bolivia (Buenavista and Santa 13 December 2000. They were kept in a Cruz). In Bolivia, S. paulensis is distributed plastic box (40 × 40 × 60 cm) in humid soil in the departments Beni and Santa Cruz, in taken from the field site. The diameter of four the Cerrado, Chiquitania Dry Forests and eggs, including all gelatinous capsules Gran Chaco ecoregions (DE LA RIVA et al. ranged from 7.4 to 8 mm (mean 7.68 ± 0.32 2000). Siphonops paulensis prefers open ha- mm), the female had a total length of 302 bitats or loose lowland forest formations, mm. The guarding female and the clutch whereas the sympatric S. annulatus (MIKAN, were inspected on eleven consecutive days 1820) is reported from rainforests, transition from 14 to 25 December 2000 between 9.00 lowland forests and Pre-Cambrian Shield Hu- to 12.00 or 21.00 to 0.00 hrs. Most of the mid forests (DE LA RIVA et al. 2000). time, the female was coiled around the Three adult S. paulensis were found in clutch, occasionally being hidden in the soil. disturbed forest near the Piraí river in the city On 22 December 2000, two non-pigmented, of Santa Cruz de la Sierra, Departamento pinkish hatchlings were observed in the box Santa Cruz, Bolivia. The area is one of the (Fig. 1B). The remaining two eggs were not last remnants of the riverside forest of the found and might have been ingested by the river Piraí within the city boundaries. The female or the young. The two hatchlings vegetation is dominated by typical riparian measured 35 and 36 mm. No external gills or species such as Erythrina poeppigiana, E. gill slits were observed. The hatchlings were dominguenzii, Tipuana tipu (Fabaceae), Tri- completely helpless and did not burrow in plaris americana (Polygonaceae), Gallesia the soil. Both died on 25 December 2000, integrifolia (Phytolaccaceae), Erythrina three days after hatching. poeppigiana, E. dominguenzii (Fabaceae), Members of the genus Siphonops are Ceiba sp. (Bombacaceae), Senna spectabilis thought to be oviparous (WAKE 1992, W ILKIN- (Caesalpineaceae), Inga adenophylla (Mi- SON & NUSSBAUM 1998) with direct develop- mosaceae), Hura crepitans (Euphorbiaceae), ment and lacking an aquatic larval stage Batocarpus amazonicus (Moraceae) and Vi- (NUSSBAUM 1979). In the first record of ovipar- tex cymosa (Verbenaceae). The understory ity in the genus Siphonops, GOELDI (1899) mainly comprises species of Solanaceae and reported a clutch of six eggs with embryos in Piperaceae, and the palm tree Bactris major an advanced stage of development of Sipho- (Arecaceae) dominates in less dense under- nops cf. annulatus from Theresopolis (Bra- story. The caecilians were collected on 6 zil), found in December. The egg diameter December 2000 (afternoon air temperature (including all egg capsules) was 8.5 mm × 10 28.5 °C). Heavy rainfall was recorded during mm, very similar to our measurements from the week between 29 November to 5 Decem- Bolivia. GANS (1961) gave a detailed report ber before the collection was made including on egg-laying in a female Siphonops paulen- 5 December (rainy season in Santa Cruz usu- sis from Primavera (Alto Paraguay), observed ally lasts from November to February). All from January 28 to 29. The freshly laid clutch three individuals were found under rotten contained six eggs. The total diameter of the logs. Two adult immediately bur- eggs ranged from 4.3 to 4.5 mm, a much rowed into soil when encountered. One fe- lower value than in the data discussed above. male remained coiled around a clutch of four It is likely that egg size increases during eggs (Fig. 1A). embryonic development as observed in other The site was revisited several times be- oviparous caecilians (e. g. Ichthyophis cf. tween 7 and 13 December 2000. When kohtaoensis TAYLOR, 1960; see KUPFER et al. checked, the female was always found coiled 2004). JARED et al. (1999) reported on female around her clutch and never left despite be- S. annulatus with clutches and newborns. ing disturbed. For further observations and Similar to Siphonops paulensis, females of S. measurements in the laboratory, the female annulatus were reported as non aggressive and the clutch were taken from the field on when guarding the clutch and after birth; the

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mother remains with the young (JARED et al. Cruz. Special thanks to ROSSY MONTAÑO and LUCIN- 1999). Whether female S. paulensis from DO GONZALES (Department of Herpetology), for Bolivia have a similar postnatal parental care helping us with work facilities and collection per- remains unclear. To the best of our knowl- mits. Thanks to the University NUR for permitting edge, the field observation of a mother guar- us to work on their property. We are grateful to MARK WILKINSON for valuable comments on the ding a clutch of eggs, and later in the labo- and natural history of siphoniform cae- ratory guarding newborn young, is the first cilians. DAVID GOWER and JOHN MEASEY kindly for S. paulensis. WILKINSON & NUSSBAUM improved earlier versions of the manuscript. AK is (1998) report on a unique foetal-like denti- currently sponsored by a Marie-Curie fellowship tion in young and S. MEIF-CT-2003-501675. paulensis from Brazil, a feature also known from altricial young of the West-African cae- ciliid Geotrypetes seraphini (DUMÉRIL, 1859) References (PARKER & D UNN 1964). Geotrypetes seraphi- ni are thought to feed their postnatal young DE LA RIVA, I., J. K ÖHLER, S. LÖTTERS & S. REICHLE (2000): Ten years of research on Bolivian with secretions of the skin (O’REILLY et al. amphibians: updated checklist, comprehensive 1998). M. WILKINSON, R.A. NUSSBAUM and C. literature, taxonomic problems, and iconogra- JARED (unpubl. observ., as reported in PENNISI phy. – Rev. Esp. Herp., 14: 19-164. 1999) have similar evidence for juvenile DUNN, E.R. (1942): The American caecilians. – nourishment in Siphonops annulatus. Bull. Mus. Comp. Zool. Harvard, 91: 439-540. Siphonops paulensis inhabits and breeds EXBRAYAT , J.M. & M. DELSOL (1985): Reproduc- in anthropogenic close to the city of tion and growth of Typhlonectes compressi- Santa Cruz (see also MONTERO 2003). Addi- caudus – a viviparous gymnophione. – Copeia, tional specimens were collected at the Uni- 1985: 950-955. versity campus (NKA 152, Natural History FUNK, W.C., G. FLETCHER-LAZO, F. NOGALES-SOR- Museum Noel Kempff Mercado, Santa Cruz) NOSA & D. ALMEIDA-REINOSO (2004): First de- scription of a clutch and nest site for the genus and within various private properties (refer- Caecilia (Gymnophiona: Caeciliidae). – Herpe- ence specimen NKA 4556). Furthermore, tol. Rev., 35: 128-130. MUÑOZ (2000) reported on Siphonops pau- GANS, C. (1961): The first record of egg laying in lensis from the city centre of Santa Cruz the caecilian Siphonops paulensis BOETTGER. – (Calle Ballivian, near the plaza central). This Copeia, 1961: 490-491. demonstrates the tolerance of this species to GOELDI, E.A. (1899): Ueber die Entwicklung von anthropogenic pressures as has been reported Siphonops annulatus. – Zool. Jb. Syst., 12: 170-173. for some other caecilians (OOMMEN et al. GOWER, D.J. & M. WILKINSON (2005): Conserva- 2000, MEASEY 2004, GOWER & WILKINSON tion biology of caecilian amphibians: a review. 2005). – Conserv. Biol, 19: 45-55. The remarkable diversity of reproductive HIMSTEDT, W. (1991): Zur Biologie und Larvenent- modes, including various levels of parental wicklung der thailändischen Blindwühle Ich- care that are extensive relative to the other thyophis kohtaoensis. – Veröff. Naturh. Mus. major amphibian groups, makes caecilians Schloss Bertholdsburg, 6: 16-24. ideally suited for evolutionary reproductive HIMSTEDT, W. (1996): Die Blindwühlen. – Neue studies. We hope our observations are useful Brehm Bücherei, Bd. 630. Magdeburg, (West- in building up an evolutionary comparative arp), 159 pp. framework. JARED, C., C.A. NAVAS & R.C. TOLEDO (1999): An appreciation of the physiology and morphology of the Caecilians (Amphibia: Gymnophiona). – Comp. Bioch. Physiol., 123: 313-328. Acknowledgements KUPFER, A., J. NABHITABHATA & W. HIMSTEDT (2004): Reproductive ecology of female caeci- We would like to thank people at the Natural lian amphibians (genus Ichthyophis): a baseline History Museum Noel Kempff Mercado in Santa study. – Biol. J. Linn. Soc., 87: 207-217.

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KUPFER, A., J. NABHITABHATA & W. HIMSTEDT ramaswamii (Amphibia: Gymnophiona) in (2005): Life history of amphibians in the sea- southern Kerala. – Curr. Sci., 79: 1386-1389. sonal tropics: , community and popula- O’REILLY, J.C., D. FENOLIO , L.C. RANIA & M. tion ecology of a caecilian (genus Ichthyophis). WILKINSON (1998): Altriciality and extended – J. Zool. (Lond.). parental care in the West African caecilian LOADER, S.P, M. WILKINSON, D.J. GOWER & C.A. Geotrypetes seraphini (Gymnophiona: Caeci- MSUYA. (2003): A remarkable young Scoleco- liidae). – Am. Zool., 38: 187A. morphus vittatus (Amphibia: Gymnophiona: PARKER, H.W. & E.R. DUNN (1964): Dentitional Scolecomorphidae) from the North Pare metamorphosis in the Amphibia. – Copeia, Mountains, Tanzania. – J. Zool. (Lond.), 259: 1964: 75-86. 93-101. PENNISI, E. (1999): Society for integrative and MEASEY, G.J. (2004): Are caecilians rare? An East comparative biology: meeting spotlights crea- African perspective. – J. East Afric. Nat. Hist., tures great and small. – Science, 283: 623-625 93: 97-117. SANDERSON, I.T. (1937): treasure. – New MEASEY, G.J. & M. DI BERNARDO (2003): Estimating York (The Viking Press), 325 pp. juvenile recruitment to a population of the semi- SARASIN, P. & F. SARASIN (1887-1890): Ergebnisse aquatic caecilian, Chthonerpeton indistinctum naturwissenschaftlicher Forschungen auf Cey- (Gymnophiona; ), in southern lon in den Jahren 1884-1886. Band II: Zur Brazil. – J. Herpetol., 47: 371-373. Entwicklungsgeschichte und Anatomie der MEASEY, G.J., D.J. GOWER, O.V. OOMMEN & M. Ceylonesischen Blindwühle Ichthyophis gluti- WILKINSON (2003): A pilot mark-recapture stu- nosus. – Wiesbaden (C.W. Kreidels Press), dy of the caecilian amphibian Gegeneophis 343 pp. ramaswamii (Amphibia: Gymnophiona: Cae- SESHACHAR, B.R., T.A. BALAKRISHNA , K. SHAKUNTA- ciliidae) in southern India. – J. Zool. (Lond.), LA & K.R. GUNDAPPA (1982): Some unique 261: 129-133. features of egg laying and reproduction in MONTERO, I. (2003): Zu den Amphibien in Santa Ichthyophis malabarensis (TAYLOR) (Apoda; Cruz de la Sierra, einer Grossstadt in Bolivien. Amphibia). – Curr. Sci., 51: 32-34. – Amphibia, 2: 3-6. TAYLOR, E.H. (1968): The caecilians of the world: MOODIE, G.E.E. (1978): Observations on the life a taxonomic review. – Lawrence (University of history of the caecilian Typhlonectes compres- Kansas Press), 845 pp. sicaudus (DUMÉRIL & BIBRON) in the Amazon WAKE, M.H. (1977): The reproductive biology of basin. – Can. J. Zool., 56: 1005-1008. caecilians: an evolutionary perspective. – pp. MUÑOZ, I. (2000): Sobre las cecilias. – pp. 17-19 in 73-101 in TAYLOR, D.H. & S.I. GUTTMAN (eds.): MUÑOZ, I., (ed.): Naturaleza, ecología urbana y The reproductive biology of amphibians. – turismo. Articulos periodísticos. – Santa Cruz New York (Plenum Press). (Prefectura del Departamento de Santa Cruz). WAKE, M.H. (1980): Reproduction, growth and NUSSBAUM , R.A. (1979): The taxonomic status of population structure of the Central American the caecilian genus Uraeotyphlus PETERS . – caecilian Dermophis mexicanus. – Herpetolo- Occ. Pap. Mus. Zool. Univ. Michigan, 687: 1- gica, 36: 244-256. 20. WAKE, M.H. (1992): Reproduction in caecilians. – NUSSBAUM, R.A. & M.E. PFRENDER (1998): Revision pp. 112-120 in HAMLETT, W.C. (ed.): Repro- of the African caecilian genus Schistometopum ductive biology of South American vertebrates. PARKER (Amphibia: Gymnophiona: – New York & Berlin (Springer Press). Caeciliidae). – Misc. Pub. Mus. Zool. Univ. WILKINSON, M. & R.A. NUSSBAUM (1998): Caecilian Michigan, 187: 1-32. viviparity and amniote origins. – J. Nat. Hist., OOMMEN, O.V., J.G. MEASEY , D.J. GOWER & M. 32: 1403-1409. WILKINSON (2000): Distribution of Gegenophis

Manuscript received: 4 October 2004 Author‘s addresses: INKA MONTERO, Zoologisches Forschungsinstitut und Museum Alexander Koenig, Adenauerallee 160, D-53113 Bonn, Germany, E-Mail: [email protected]; STEFFEN REICHLE, Fundación Amigos de la Naturaleza, Casilla 2241, Santa Cruz de la Sierra, Bolivia, E-Mail: [email protected]; ALEXANDER KUPFER, Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom, E-Mail: [email protected].

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