Gastrointestinal helminths of nine species of Cnemaspis (Squamata: Gekkonidae) from Peninsular Malaysia, one species from Cambodia and Thailand and two species from Vietnam

A total of 12 species of Cnemaspis (N = 104) from Southeast Asia were examined for gastrointestinal helminths. Samples consisted of nine species (n = 86) from Peninsular Malaysia: Cnemaspis affinis (n = 4); Cnemaspis baueri (n = 17); Cnemaspis biocellata (n = 12); Cnemaspis grismeri (n = 8); Cnemaspis kumpoli (n = 11); Cnemaspis limi (n = 9): Cnemaspis monachorum (n = 7); Cnemaspis pemanggilensis (n = 10); Cnemaspis peninsularis (n = 8); one species (n = 5) from Cambodia and Thailand, Cnemaspis chanthaburiensis (n = 5); and two species (n = 13) from Vietnam: Cnemaspis nuicamensis (n = 6) and Cnemaspis tucdupensis (n = 7). The aggregate helminth community consisted of one species of Cestoda, Cylindrotaenia malayi and nine species of Nematoda: Bakeria schadi, Meteterakis singaporensis, Parapharyngodon maplestoni, Maxvachonia sp., Physalopteroides sp., Physalopteridae gen. sp., Riticulariidae gen. sp., Seuratoidea gen. sp., Ascaridoidea gen. sp. Meteterakis singaporensis had the largest number of individuals (457) and greatest prevalence (24%). Twenty-eight new host records are reported.


Introduction
There are currently 50 species of Cnemaspis, rock geckos (sensu Grismer et al. 2014), known from Southeast Asia, with disjunct distributions extending from southern Vietnam, Laos, southwestern Cambodia and Thailand southward through the Malay Peninsula . In this paper, we examined the following species of Cnemaspis for helminths: Cnemaspis affinis (Stoliczka, 1870) is known only from Peninsular Malaysia, Pulau Pinang Penang . Cnemaspis baueri Das and Grismer, 2003 is known only from Peninsular Malaysia: Pulau Aur, Johor (Das and Grismer 2003) and the rocky island of Dayang (Grismer et al. 2006b). Cnemaspis biocellata  is known only from Peninsular Malaysia where it extends at least 40 km through the karst system of the Banjaran Nakawan from Thale Ban National Park, Satun  southward through Wang Kelian and Perlis State Park . Cnemaspis grismeri Wood, et al. 2013 is known only from Peninsular Malaysia, Gua Asar, Bukit Kepala Gajah limestone massif, Lenggong, Perak, Malaysia (Wood et al. 2013). Cnemaspis kumpoli Taylor, 1963 ranges from southern Thailand south to the Isthmus of Kra (Taylor 1963) to extreme northern Malaysia . Cnemaspis limi Das and Grismer, 2003 is known only from Peninsular Malaysia: Pulau Tioman and Pulau Tioman of the Seribuat Archipelago . Cnemaspis monachorum Grismer et al. 2009 is known only from the karst formations Pulau Langkawi and Pulau Langgong, Kedah, Peninsular Malaysia . Cnemaspis peninsularis Grismer et al. 2014 ranges from central Peninsular Malaysia to Singapore . Cnemaspis pemanggilensis Grismer and Das, 2006 is known only from Peninsular Malaysia, Pulau Pemanggil, Johor . Also studied was one species Cnemaspis chanthaburiensis Bauer and Das, 1988 from southeast Thailand (Chantuburi Chon Buri), and Cambodia (NW Cardamon Mts) ) and two species from Vietnam, Cnemaspis nuicamensis Grismer and Van Tri, 2007 known from the type locality Nui Cam Hill, Tinh Bien District, An Giang Province, Vietnam (Grismer and Van Tri 2007) and Cnemaspis tucdupensis Grismer and Van Tri, 2007 also known from the type locality Tuc Dup Hill, Tri Ton District, An Giang Province, Vietnam (Grismer and Van Tri 2007). In this paper, we list helminths of nine species of Cnemaspis from Peninsular Malaysia, one species from Cambodia and Thailand and two from Vietnam as part of an ongoing survey of amphibians and reptiles from Peninsular Malaysia. We establish the initial helminth list for all species of Cnemaspis examined in this paper.
The body cavity was opened with a longitudinal incision and the gastrointestinal tract was removed by cutting across the oesophagus and rectum. The oesophagus, stomach, small intestine and body cavity were examined separately for helminths. Nematodes were cleared in lactophenol; cestodes were stained in haematoxylin and mounted in Canada balsam. All were examined under a compound microscope and identified. Helminths were deposited in the Harold W. Manter Laboratory (HWML), University of Nebraska, Lincoln, USA (Appendix 2). Parasite terminology is in accordance with Bush et al. (1997).

Results
Lizard sample size, helminth number, prevalence, mean intensity of infection ± SD and range are presented in Table 1. Twenty-eight new host records are reported.

Cestoda
Nematotaeniidae Cylindrotaenia malayi was originally described from the frog Polypedates leucomystax (Rhacophoridae) collected in Penang, Malaysia (Jones 1987). Cnemaspis tucdupensis represents the second host reported for Cylindrotaenia malayi and is a new host record. Nematoda Molineidae Bakeria schadi was recently described from Cnemaspis mcguirei from Peninsular Malaysia (Bursey et al. 2014). Bakeria schadi in C. affinis, C. biocellata, C. grismeri, C. limi, C. monarchum and C. pemanggilensis are new host records. Heterakidae Meteterakis singaporensis was described from Duttaphrynus (as Bufo) melanostictus from Singapore by Inglis (1958), and was also found in C. mcguirei from Peninsular Malaysia by Bursey et al. (2014). Congeners of Meteterakis are mainly restricted to Southeast Asia and the Philippines (Baker 1987) and also occur in Papua New Guinea (Goldberg et al. 2010). Meteterakis singaporensis had the largest number of individuals (457) and greatest prevalence (24%). Meteterakis singaporensis in C. affinis, C. baueri, C. biocellata, C. grismeri, C. kumpoli, C. nuicamensis and C. pemanggilensis are new host records. Pharyngodonidae Parapharyngodon maplestoni, described by Chatterji (1933) from the lizard Calotes versicolor (Agamidae) from Burma (currently Myanmar), has a wide distribution pattern including Thailand of Southeast Asia (Goldberg and Bursey 2001). Members of the Pharyngodonidae, such as P. maplestoni, have direct (monoxenous) life cycles and infection most likely occurs when contaminated substrate is ingested as lizards forage for food; a colonising P. maplestoni needs only to find suitable habitat occupied by other lizards. This lack of dependence on an intermediate host is likely to increase the efficiency of P. maplestoni in infecting additional lizards, probably contributes to the broad distribution of this species and may be partly responsible for its success in establishing in two species of geckos, Nactus multicarinatus and N. pelagicus, on various islands in Vanuatu, Oceania (Goldberg et al. 2011). Parapharyngodon maplestoni in C. baueri and C. pemanggilensis are new host records.
Cosmocercidae Species of Maxvachonia are known to occur in the digestive tracts of amphibians and reptiles from Australia, Madagascar and New Guinea (Baker 1987). Maxvachonia sp. in C. chanthaburiensis is a new host record. Table 1. Number of helminths (N), prevalence (P, as percentage) mean intensity (MI) ± 1 standard deviation (SD) and range (R) for 12 species of Cnemaspis. All are new host records. Species of Physalopteroides are common in the Southern Hemisphere and are known from Africa, South America, Australia, South America and also Cuba (Baker 1987). Physalopteroides sp. in C. peninsularis is a new host record.
Physalopteridae gen. sp. include three subfamilies which occur in the stomachs of reptiles, birds and mammals, where they firmly attach to the gastric mucosa; only species in the Physalopterinae have been studied (Chabaud 1975). Encysted physalopterid larvae are common in the digestive tracts of reptiles (Jones 1995). As development to the adult does not occur, infected reptiles serve as paratenic (transport) hosts. Physalopteridae in C. limi and C. nuicamensis are new host records.
Cucullanidae Seuratoidea gen. sp. are a disparate group of helminth genera, that are thought to connect the Cosmocercoidea to the advanced Ascaridida or Spirurida (Chabaud 1978). Le- Van-Hoa (1966) experimentally found the intermediate hosts of Seuratum nguyenvanaii, a parasite of the house shrew in Vietnam, were the cockroaches Blatta orientalis and Periplaneta americana. Seuratoidea gen. sp. in C. biocellata and C. grismeri are new host records. Riticulariidae The Riticulariidae is composed of a homogeneous group of about 50 species, divided into two genera and several subgenera (Quentin 1969a(Quentin , 1969bChabaud 1975). They are heteroxenous and likely require an insect intermediate host (Anderson 2000). Riticulariidae gen. sp. in C. grismeri is a new host record.
A total of 577 helminths (one cestode, 576 nematodes) were collected from 73 (70.1%) of the 104 individuals examined. Of these, 525 were mature individuals representing six species; 52 were larvae representing four species. It should be noted that although 10 helminth species were in the sample, no host species harboured more than four species: two host species harboured four helminth species; four host species harboured three; two harboured two; four harboured one. On average, there were 2.33 ± 1.55 (range 1-4) helminth species per host species. Hanski (1982) introduced the concept of core and satellite speciesthat is, core species occur with relatively high prevalence and abundance while satellite species occur less frequently and with less abundance. Roca (1993) defined core species as those with greater than 30% prevalence and satellite species as those with prevalences between 10 and 30%. In this study (Table 1), M. singaporensis (28%) represents a core species, while B. schadi (14%) represents a satellite species. The remaining seven species have prevalences of less than 10%. Roca (1993) suggested the prevalence of encysted larval nematodes in a lizard population may indicate the importance of the host in food webs because lizards can serve as transport (paratenic) hosts. In conclusion, it appears Cnemaspis from Southeast Asia are dominated by two species of generalist helminths, B. schadi and M. singaporensis. We should note that our conclusions are based upon our host sample; further surveys of these hosts will no doubt increase the number of harboured helminths and change prevalence values.

Disclosure statement
No potential conflict of interest was reported by the author(s).