A Dicephalic Caecilian Larva, Ichthyophis Bannanicus (Amphibia: Gymnophiona: Ichthyophiidae), from Southeast Guangxi, China
Total Page：16
File Type：pdf, Size：1020Kb
Asian Herpetological Research 2011, 2(4): 230–233 DOI: 10.3724/SP.J.1245.2011.00230 A Dicephalic Caecilian Larva, Ichthyophis bannanicus (Amphibia: Gymnophiona: Ichthyophiidae), from Southeast Guangxi, China Yongjian BEI1, 2, Shaoquan MENG1, 2*, Jianda LI1, Jianru FENG1, Jianbing ZHOU1 and Guifen LI1, 2* 1 College of Life Science and Technology, Yulin Normal University, Yulin 537000, Guangxi, China. 2 Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection of Ministry of Education, Guangxi Normal University, Guilin 541004, Guangxi, China. Abstract We describe the first case of dicephalism in a caecilian larva, Ichthyophis bannanicus, from southeastern Guangxi, China. The two heads of the larva are united at the anterior one-third of the body. It is measured as: body mass 0.6 g, total length 42.4 mm, body width at middle 5.4 mm, head length 2.1 mm, head width 2.5 mm, snout length 1.5 mm, internarial distance 0.9 mm, and interorbital distance 1.7 mm. Compared to normal conspecific larvae, it is smaller except for the internarial distance, body mass and body width at midbody. Keywords Gymnophiona, Ichthyophis bannanicus, dicephalism, larvae 1. Introduction with populations recorded from Yunnan, Guangxi and Guangdong (Yang and Su, 1976; Wen, 1983; Pan et al., Abnormalities of development are frequently reported 1985). I. bannanicus inhabits subtropical or tropical moist in vertebrates. Malformations are common in mammals lowland forests, streams and agricultural land (Wen, (Wu et al., 2002), and reptiles (such as lizards: Pleticha, 1998). It was once considered to be endemic to southern 1968, Spadola and Insacco, 2009; turtles: Vanni and China (Fei et al., 2006), but a recent report shows that Nistri, 1987, Diong et al., 2003; snakes: Heasman, 1933; its range may extend to Northern Vietnam and Thailand Belluomini, 1959; Da Cunha, 1968; De Lema, 1982, (Li et al., 2010). This paper reports the first case of 1994; Khaire and Khaire, 1984; Mitchell and Fieg, 1996; dicephalism in a caecilian larva, Ichthyophis bannanicus Oros et al., 1997; Maryan, 2001; Hosser and Gibbons, (Amphibia: Gymnophiona), with information on its 2003; de Albuquerque et al., 2010). The phenomena external morphology and differences from its normal of developmental malformations in amphibians have conspecific larvae. generally been described from the orders Urodela and Anura (Johnson et al., 2002; Andrew and Johnson, 2003), 2. Methods with malformations in the order Gymnophiona never been described in the literature, especially at the larval stage. 2.1 Study site The study area is located in the suburb of Ichthyophis bannanicus is the only known species of Beiliu City (22°46.966–48.053 N, 110°15.944–17.574 Gymnophiona in China, which was first described in 1984 E; 127–222 m above sea level) in southeastern Guangxi, (Yang, 1984). This species ranges in southern China, China. Primary forest was removed in the 1960s, with the region now being used mostly for rice farming. In * Corresponding author: Profs. Shaoquan MENG and Guifen LI, from the study area only some patches of secondary forest the College of Life Science and Technology, Yulin Normal University, China, with their research focusing on conservation biology of remain near rivers, brooks, and rice paddies. There are amphibians. distributions of mixed wood and broad-leaved forests in E-mail: [email protected] (Shaoquan MENG); [email protected] (Guifen LI) the hills around the study sites. The subtropical climate Received: 13 August 2011 Accepted: 21 November 2011 in the study area is strongly influenced by alternating dry No. 4 Yongjian BEI et al. A Dicephalic Caecilian Larva, Ichthyophis bannanicus 231 and rainy (monsoon) seasons. Usually, the rainy season starts in early March, and then ends in October, with most rain falling between May and August. 2.2 Morphological measurement We have studied the reproductive ecology of I. Bannanicus in the field, with three clutches being observed in August 2010. In total, 126 larvae were found in three nests with one dicephalic larva being found among them, with a rate of malformation being approximately 0.8%. We collected 22 larvae, including the malformed and measured morphological characters immediately in the field to the nearest 0.1 mm with a vernier caliper or 0.1 g by a balance, including total length (TL), body mass (BM), body width at middle (BWM), head length (HL), head width (HW), interorbital distance (IOD), internarial distance (IND), and snout length (SL). These measurements were made based on the methods of Nussbaum and Gans (1980), Kupfer and Müller (2004), and Nishikawa et al. (2008). 3. Results 3.1 Description of I. bannanicus larvae The dicephalic caecilian larva, which has not been reported previously in Gymnophiona, exhibits two heads that are united at the anterior one-third of the body (Figure 1 A). The normal Figure 1 Dicephalic (A) and normal larvae (B) of I. bannanicus. larvae maintain the characteristic elongate, limbless phenotype with a single anterior-posterior axis (Figure 1 B). Eyes, caudal fin and gill openings can be seen clearly in the dicephalic and normal I. bannanicus larvae, were well developed and seemed to function properly. Body color in the dicephalic larva was lighter when compared to normal conspecifics. 3.2 Morphological characters of I. bannanicus larvae The dicephalic larva was compared with twenty-one normal larvae in body characters. The body size of the dicephalic larva was smaller than that of the normal larvae, except IND, BM and BWM (Figure 2). For example, the mean length of the normal larvae was 72.3 mm and that of the dicephalic larva only 42.4 mm. 4. Discussion Figure 2 Comparison of body characteristics of the dicephalic and normal larvae of I. bannanicus. The phenomena of developmental malformations in amphibians have only been described in the orders rare, with the only reports being on three anuran larvae Urodela and Anura, and are generally regarded as (Loyed, 1897; Lebedinsky, 1921; Dragoiu and Busnitza, appendicular malformations such as missing and partially 1927) and four urodelan larvae (Pereira and Rocha, missing limbs, multiple extra limbs and digits, incomplete 2004; Velo-Antón et al., 2007; Fernández-Álvarez et al., limb formation, misshapen eyes and tails, skin lesions, 2011). In reptiles, such as lizards and snakes, two-headed and whole-body (Johnson et al., 2001a, 2001b; Andrew individuals have long been known to exist (Spadola and Johnson, 2003 ). Dicephalism in wild amphibians is and Insacco, 2009; Mcallister and Wallach, 2006; de 232 Asian Herpetological Research Vol. 2 Albuquerque et al., 2010). Gymnophiona (caecilian) References are one of the three orders of extant Amphibia, whose fossorial and secretive lifestyle has made it difficult or Andrew R. B., Johnson P. T. J. 2003. The complexity of deformed impossible for field studies. It is difficult or find and amphibians. Frontiers Ecol Environ, 1: 87–94 Belluomini H. E. 1959. Bicefalia em Xenodon merremii (Wagler, observe them in the field (Gower and Wilkinson, 2005). 1824) (Serpentes). Memórias do Instituto Butantan, 28: 85–89 As far as can be determined, this appears to be the first Blaustein A. R., Belden L. K. 2003. Amphibian defenses against reported instance of dicephalism in Gymnophiona. UV-B radiation. Evol Develop, 5: 189–197 In recent decades, the amphibian malformation was Blaustein A. R., Johnson P. T. J. 2003. The complexity of found at a higher frequency (Ouellet et al., 1997; Gardiner deformed amphibians. Front Ecol Environ, 1(2): 87–94 et al., 2003). Hypotheses for this include UV radiation Boone M. D., Bridges C. M. 2003. The problem of pesticides: Implications for amphibian populations. In Semlitsch R. D. (Ed.), (Blaustein and Belden, 2003), inbreeding (Williams et al., Amphibian Conservation. Washington D. C., USA: Smithsonian 2008), parasites (Sessions and Ruth, 1990; Johnson et Institution Press, 152–167 al., 1999), and environmental contamination (Ouellet Burkhart J. G., Ankley G., Bell H., Carpenter H., Fort D., et al., 1997; Sparling et al., 2000, 2001; Burkhart et al., Gardiner D., Gardner H., Hale R., Helgen J. C., Jepson P., 2000; Boone and Bridges, 2003; Reeves et al., 2010) of Johnson D., Lannoo M., Lee D., Lary J., Levey R., Magner various sorts. Some studies show that many malformed J., Meteyer C., Shelby M. D., Lucier G. 2000. Strategies for assessing the implications of malformed frogs for environmental amphibians occur in agricultural areas where insecticides health. Environ Health Perspect, 108: 83–90 and fertilizers are applied extensively (Ouellet et al., 1997; Da Cunha O. R. 1968. Um teratodimo derodimo em Jiboia Hayes et al., 2002a, 2002b). The amphibians are sensitive (Constrictor constrictor (Linn., 1766)) (Ophidia; Boidae). to pollution, and can easily absorb pollutants through Boletim Museu Paraense Emílio Goeldi série Zool, 67: 1–17 the skin. The skin absorbs chemical contaminants from de Albuquerque N. R., Arruda W. S., Costa A. S., Galharte R. C. V. L., Vargas G. H., Moreno I. H. 2010. A dicephalic agricultural run-off that results from an indiscriminate yellowanaconda snake, Eunectes notaeus (Serpentes: Boidae), use of pesticides, herbicides and fertilizers (Doyle, 1998; from Southern Pantanal, Brazil. J Nat Hist, 44: 1989–1994 Morell, 1999; Roy, 2002; Blaustein and Johnson, 2003; De Lema T. 1982. Descriçao de dois especimens bicefalos de Xu et al., 2004). Liophis miliaris (Linnaeus, 1758) (Serpentes, Colubridae). Bicephalous animals are scarcely reported in Iheringia, série Zool, 61: 1–17 amphibians, but frequently in snakes (de Albuquerque De Lema T. 1994. Descriçao de um exemplar com bifurçao axial de Echinantera cyanopleura (Cope, 1885) (Serpentes, Colubridae, et al., 2010; Fernández-Álvarez et al., 2011). We luckily Xenodontinae). Acta Biol Leopoldensia, 16: 113–117 found the first dicephalic caecilian larva in field. The Diong C. H., Tan L. K. A., Leh C. M. U. 2003. Axial bifurcation previous researches and findings indicate that the anomaly in a bicephalic Chelonia mydas embryo.