Phyllomedusa 15-2.Indd

Short CommuniCation Draco (Squamata: Agamidae) from peninsular Malaysia and one species from Cambodia

Stephen R. Goldberg1, Charles R. Bursey2, and L. Lee Grismer3 1 2 Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania, 16146, USA. 3 Department of Biology, La Sierra University, Riverside, California, 92505, USA. E-mail: [email protected].

Keywords: endoparasites, Flying Lizards, Nematoda, new hosts.

Palavras-chave: endoparasitas, lagartos-planadores, Nematoda, novos hospedeiros.

The genus Draco Linnaeus, 1758 contains Herein, we provide preliminary lists of some 40 species of lizards that collectively range Draco from from southern India and Indochina, east to the Peninsular Malaysia and one species from Philippines, and south through the Malay Cambodia (Table 1). Draco abbreviatus ranges Peninsula and throughout the Indo-Australian from Thailand, southward through peninsular Archipelago and East to the Key Islands of Malaysia to Singapore, Sumatra, and Borneo Indonesia (Grismer 2011, Uetz and Hosek 2015). (Grismer 2011); D. blanfordii occurs in parts of There are few reports of helminths from Draco. Myanmar, Thailand, northern peninsular Bain et al Malaysia, and Indonesia (Grismer 2011); D. Conispiculum ramachandrani Bain, Kouyate formosus ranges from southern Thailand, and Baker, 1982, from Draco maximus southward throughout the Malay Peninsula Boulenger, 1893 collected in Malaysia. Tkach et (Grismer 2011); D. sumatranus occurs in al. (2011) described Rhabdias mcquirei Tkach, Thailand, peninsular Malaysia, Singapore, Kuzmin and Brown, 2011, and Kuzmin et al. Sumatra, and Borneo (Das 2010); D. taeniopterus (2012) described R. odilebaini Kuzmin, Tkach ranges from Myanmar, central Thailand, and and Bush, 2012; both nematode species are from central Cambodia, south to northern peninsular Draco spilopterus Malaysia (Grismer 2011); and D. maculatus on Luzon Island, Philippines. (from Cambodia) ranges from southern China, southward to northern peninsula Malaysia (Grismer 2011). Draco Received 25 January 2016 were borrowed from the herpetology collection Accepted 24 May 2016 of La Sierra University (LSUHC), Riverside Distributed December 2016

Phyllomedusa - 15(2), December 2016 175 Goldberg et al.

Physocephalus Strongyluris calotis Orneoascaris sandoshami Gonofilaria rudnicki Abbreviata achari Helminth 1. Table helminths: D. abbreviatus (ND. blanfordii

(N D. formosus (N D. maculatus findings are new host records. host new are findings blanfordii Number of helminths ( helminths of Number (ND. sumatranus (ND. taeniopterus cysts (N ( N and later stored in 70% ethanol. The body cavity = 2), = was opened by a longitudinal incision and the N 6 4 1 - - D. abbreviatus D. formosus D. gastrointestinal tract was removed by cutting 100 100 100 % - -

N across the esophagus and rectum. The esophagus,

), prevalence (P as %). Mean (X) and range (r) in 11 in (r) range and (X) Mean %). as (P prevalence ), stomach, small intestine, large intestine, and 6.0 4.0 1.0 X - - ( N

(6) (4) (1) dissecting microscope for helminths. Nematodes r - - = 2), = 14 N 1 - - - D. sumatranus D. D. blanfordii (100) 100

% - - - Anderson et al. (2009) and Gibbons (2010) and 1.0 7.0 X - - - to species by comparison with the original

1–13 descriptions. Helminths were deposited in the (1) ( N r - - - = 3), =

N 1 2 - - - D. formosus

D. taeniopterus D. II). Parasite terminology follows that of Bush et 50 50 % - - - al. (1997). Number of helminths, prevalence

1.0 2.0 (%), mean, and range are in Table 1. All 13 X - - - reported occurrences of Nematoda are new host (1) (2) r - - - records. Draco ( N N 4 9 - - - = 3), and 5 from Cambodia: from 5 and 3), =

D. maculatus Abbreviata achari (Mirza, 1935) lizards from peninsular Malaysia: peninsular from lizards 20 20 % - - - (infection sites: stomach, small intestine); Mullin, 1973 (body cavity); 4.0 4.5 X - - - Orneoascaris sandoshami (Yuen, 1963) (small (2–7)

(4) intestine); Strongyluris calotis Baylis and r - - - Daubney, 1923 (small and large intestines); N 5 1 - - - Physocephalus sp. (larvae in cysts in stomach D. sumatranus

100 wall). 33 % - - -

D. maculatus D. Abbreviata achari was described from 1.7 1.0

X Calotes versicolor (Daudin, 1802) collected in - - -

Hyderabad, Deccan, India (Mirza 1935). Soota D. abbreviatus D. (1–3) (1) r - - - and Chaturvedi (1969) redescribed the species

( from C. versicolor from Odisha, (formerly N N 3 2 - - - D. taeniopterus

= 5). All helminth All 5). = Orissa) India. Goldberg et al. (2003) recorded it 33 33 % from C. versicolor from Pakistan. Abbreviata - - - (

N achari has the widest distribution in the current 3.0 2.0 X - - - = 1), = Draco

(3) (2) (Table 1). Peninsular Malaysia is a new locality r - - D. record.

Phyllomedusa - 15(2), December 2016 176 Helminths of six species of lizards of the genus Draco

was described from two (1994) reported larvae of Physocephalus sp. in species of agamid lizards, Gonocephalus stomach granulomas of Sceloporus cyanogenys bornensis (Schlegel, 1851) and Acanthosaura Cope, 1885 (as Sceloporus serrifer). Fourth- armata stage larvae or mature nematodes were not Malaysia, by Mullin (1973). An immature female G. rudicki also was found in Limnonectes Physocephalus is not possible. macrodonRana Draco abbreviatus was infected with three macrodon) (Mullin 1973). Orneoascaris sandoshami (Yuen, 1963) species was infected by two nematode species. originally was described as Amplicaecum Draco blanfordii was infected with the most sandoshami by Yuen (1963) from the Malayan individuals of nematodes (15), and D. formosus Horned Frog, Megophrys nasuta (Schlegel, had the fewest (3). Mean number of helminths 1858) (Megophryidae), collected in Singapore, infecting each species of Draco but was reassigned to its current position by Sprent (1985). Orneoascaris sandoshami was reported in Gonocephalus abbotti Cochran, 1922 Draco lizards—Abbreviata achari, by Goldberg et al. (2005), Aphaniotis fusca rudnicki, Orneoascaris sandoshami, and (Peters, 1864) (Goldberg et al. 2015a), Larutia Physocephalus trifasciata (Tweedie, 1940) (Goldberg et al. intermediate hosts to complete their life cycles 2015b), Bronchocela cristatella (Kuhl, 1820) (Anderson 2000). is (Goldberg et al. 2015d), Gonocephalus bellii, transmitted by haematophagous vectors G. grandis (Gray, (Anderson 2000). The remaining species, 1845) (Goldberg et al. 2016) from peninsular Strongyluris calotis Malaysia and Acanthosaura cardamomensis cycle, no intermediate host), infection by egg ingestion (Anderson 2000). Holden, 2010, from Cambodia (Bursey et al. Draco 2015). suggests that this lizard genus is infected by Strongyluris calotis is widely distributed in generalist helminths, capable of infecting a Asian agamid lizards (Baker 1987) and also has variety of lizard hosts. This is also the case for been reported in agamids of Palestine (Rayyan et species of Cnemaspis (Goldberg et al. 2015c) al. 2013) and Pakistan (Goldberg et al. 2003). and Gonocephalus (Goldberg et al. 2016) from Strongyluris calotis was present in four species of Draco lizards (Table 1). The species also was Draco (Uetz and Hosek 2015), additional species found in the agamid lizards, B. cristatella (Goldberg et al. 2015d), Gonocephalus bellii helminths infecting this genus. G. grandis from peninsular Malaysia (Goldberg et al. 2016). Acknowledgments. Infective larvae of Physocephalus sexalatus (Molin, 1860) have been found encapsulated in dissections. tissues of numerous species of dung beetles; encapsulated infective larvae are common in tissues of amphibians, reptiles, birds, and References hosts (Anderson 2000). Development to the Anderson, R. C. 2000. Nematode Parasites of Verte- adult form occurs when they are ingested by brates: Their Development and Transmission. 2nd ed. mammals (Anderson 2000). Goldberg et al.

Phyllomedusa - 15(2), December 2016 177 Goldberg et al.

Goldberg, S. R., C. R. Bursey, and H. J. Holshuh. 1994. 2009. Keys to the Nematode Parasites of Vertebrates. Physocephalus sp. (Spirurida, Spirocercidae) larvae in Archival Volume stomach granulomas of the blue spiny lizard, Sceloporus Publishing. 463 pp. serrifer Journal of Wildlife Diseases 30: Goldberg, S. R., C. R. Bursey, and S. R. Telford Jr. 2003. Nematoda). Bulletin du Museum National d’Histoire Metazoan endoparasites of 11 species of lizards from Naturelle, Section A. 4: Pakistan. Comparative Parasitology 70: Baker, M. R. 1987. Synopsis of the Nematoda parasitic in Grismer, L. L. 2011. Lizards of Peninsular Malaysia, amphibians and reptiles. Memorial University of Singapore and Their Adjacent Archipelagos. Frankfurt Newfoundland, Occasional Papers in Biology 11 am Main. Edition Chimaira. 728 pp. Bursey, C. R., S. R. Goldberg, and L. L. Grismer. 2015. New Kuzmin, Y. M., V. V. Tkach, and S. E. Bush. 2012. A new species of (Nematoda; Filarioidea; species of Rhabdias (Nematoda: Rhabdiasidae) from Onchocercidae) and other helminths in Acanthosaura agamid lizards on Luzon Island, Philippines. Journal of cardamomensis (Sauria; Agamidae) from Indochina Parasitology 98: Peninsula. Acta Parasitologica 60: Mirza, M. B. 1935. Physaloptera achari n. sp. from Calotes versicolor with a short note on abnormalities in the 1997. Parasitology meets ecology on its own genus Physaloptera. Proceedings of the Academy of terms: Margolis et al., revisited. Journal of Parasitology Sciences of the United Provinces of Agra and Oudh 83: Allahabad 5: Das, I. 2010. A Field Guide to the Reptiles of South-East gen. et sp. n. Asia, Myanmar, Thailand, Laos, Cambodia, Vietnam, (Nematoda: Filarioidea) from Malaysian lizards. Peninsular Malaysia, Singapore, Sumatra, Borneo, Proceedings of the Helminthological Society of Java, Bali. London. New Holland Publishers, Ltd. 376 pp. Washington 40: Gibbons, L. M. 2010. Keys to the Nematode Parasites of Rayyan, A., B. Al-Zain, and A. Al-Hindi. 2013. Gastro- Vertebrates. Supplementary Volume. intestinal parasites of the roucktail rock agama, Laudakia International Publishing. 416 pp. stellio from Gaza Strip, Palestine. Journal of Biology 1: Goldberg, S. R., C. R. Bursey, and L. L. Grismer. 2005. Gonocephalus abbotti Soota, T. D. and Y. Chaturvedi. 1969. On two new nematodes Endoparasites. Herpetological Review 36: 450. of the genus Abbreviata Travassos, 1920, along with redescription of a third, Abbreviata achari (Mirza, Goldberg, S. R., C. R. Bursey, and L. L. Grismer. 2015a. 1935). Proceedings of the Indian Academy of Science Aphaniotus fusca (Peninsular Earless Agama). Sect. B 69: Endoparasites. Herpetological Review 46: 87. Sprent, J. F. A. 1985. Ascaridoid nematodes from amphibians Goldberg, S. R., C. R. Bursey, and L. L. Grismer. 2015b. and reptiles: Orneoascaris. Annales de Parasitologie Larutia trifasciata (Three-banded Larut Skink). Humaine et Comparée 60: Endoparasite. Herpetological Review 46: 259. Tkach, V. V., Y. Kuzmin, and R. M. Brown. 2011. Rhabdias Goldberg, S. R., C. R. Bursey, and L. L. Grismer. 2015c. mcguirei sp. nov. (Nematoda, Rhabdiasidae) from the Gastrointestinal helminths of nine species of Cnemaspis Draco spilopterus (Squamata, Agamidae) (Squamata: Gekkonidae) from Peninsular Malaysia, one of the northern Philippines. Acta Parasitologica species from Cambodia and Thailand and two species 56: from Vietnam. Journal of Natural History 49: 2691. Uetz, P. and J. Hosek (eds.). 2015. The Reptile Database. Eletronic Database accessible at http://www.reptile- Goldberg, S. R., C. R. Bursey, L. L. Grismer, and J. Arreola. database.org. Captured on 22 December 2015. 2015d. Bronchocela cristatella (Green Crested Lizard). Endoparasites. Herpetological Review 46: Yuen, P. H. 1963. Two new species of the genus Amplicaecum Baylis from Malayan amphibians. Parasitology 53: Goldberg, S. R., C. R. Bursey, and L. L. Grismer. 2016. 94. Gonocephalus lizards (Squamata: Agamidae) from Peninsular Malaysia. Editor: Jaime Bertoluci 70:

Phyllomedusa - 15(2), December 2016 178 Helminths of six species of lizards of the genus Draco

Appendix I. Draco La Sierra University (LSUHC), Riverside, California, USA.

Draco abbreviatus (N August 2005. Draco blandfordii (N E), June 2008. Draco formosus (N 2002. Draco maculatus (N E), June 2007. Draco sumatranus (N Draco taeniopterus (N

Appendix II.Draco spp. taken from the herpetology collection of La Sierra University (LSUHC), Riverside, California, USA.

Draco abbreviatus: Abbreviata achari Strongyluris calotis 94146); Draco blanfordii: Abbreviata achari Strongyluris calotis Draco formosus: Strongyluris calotis Draco maculatus: Abbreviata achari Physocephalus sp.Draco sumatranus: Abbreviata achari Orneoascaris sandoshami Draco taeniopterus: Abbreviata achari Strongyluris calotis

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