Intestinal parasites of unisexual and bisexual lizards Darevskia spp. (Lacertidae) from Northeastern Anatolia

Caucasian rock lizards (Darevskia spp.) are small saurians of the family Lacertidae ranging from western Asia and south-eastern Europe (Ananjeva et al., 2006; Arnold et al., 2007). Although they are ecologically similar to the European rock lizards they include not only bisexual species but also parthenogenetic forms (Darevsky, 1978; Tarkhvishnili, 2012).

Parasitological knowledge of the parasites of the Caucasian rock lizards is still fragmentary with only a few recent studies investigating the parasite communities in deep. In particular no helminthological data are known for many species whereas data are partial and scarce for others, focusing mainly on taxonomy and faunistic studies (Schad et al., 1960; Markov & Bodganov, 1962; Sharpilo, 1962, 1976; Saygi, 1993). Recently some studies have paid attention on helminths of several species of Darevskia from Armenia (Sargsyan & Harutyunyan, 2012; Sargsyan, 2013; Sargsyan et al., 2013). Even more recently, Roca et al. (2015, 2016) analysed the helminth communities in unisexual endemic lizards from Turkey and the structure of helminth community of D. rudis across northern Anatolia.

Studies available on these Turkish species conclude that, as in other Palaearctic lacertid lizards, their helminth communities are poor and isolationist (Roca & Hornero, 1994; Galdón et al., 2006), although Roca et al. (2016) pointed out that D. rudis had richer diversity than other continental Palaearctic rock lizards such as Podarcis hispanica, Podarcis muralis, Podarcis bocagei or Podarcis carbonelli.

In this study, we encompass a parasitological analysis of several species of Darevskia from Turkey whose helminthfauna is unknown. Specifically we addressed the following objectives: (i) characterization richness and diversity patterns of the helminth communities; (ii) characterization of the helminth species parasitizing the host as either specialists or generalists; and (iii) comparison of the helminth communities with those of other Darevskia hosts, and other Palaearctic rock lizards.

Four bisexual and two unisexual species of the genus Darevskia (Table 1), all belonging to the herpetological collection of the Fauna and Flora Research and Application Center, Dokuz Eylul University (Turkey), were examined (see addendum for accession numbers). Populations were sampled in July 2010 from northeastern and eastern Anatolia, with altitude levels ranging from 1370 to 2086 m a.s.l. In this region, climate changes from Oceanic in the Black Sea coast to Continental in Eastern Anatolia due to abrupt increase in thermal amplitude and aridification (Sensoy et al., 2008).

Lizards were dissected for parasitological examination. This method still ensures a much better detection and quantification of intestinal parasites with a few specimens than some non-invasive techniques (Jorge et al., 2013). Helminths were processed in accordance with the usual techniques in parasitology (Hornero, 1991). The parasite vouchers were deposited in the parasitological collection of the Department of Zoology of University of Valencia, Spain, with the species name accompanied by the host code (see addendum for accession numbers).

The use of descriptive ecological terms follows Bush et al. (1997). Brillouin’s index was used for calculating diversity according to Magurran (2004). Criteria of Edwards & Bush (1989) and Roca & Hornero (1994) were used in the consideration of the helminth species as specialists or generalists.

Only three helminth species were found, the cestode Nematotaenia tarentolae and the nematodes Spauligodon saxicolae and Strongyloides darevskyi. Table 2 shows the global prevalence, intensity and abundance of infection of the hosts. Table 3 shows the species richness and abundance in the helminth infracommunities of each host species. The presence of helminths found, and their infection parameters are shown in Table 4.

N. tarentolae and S. darevskyi occupied the small intestine whereas S. saxicolae was found in the rectum. S. saxicolae was found in all host species analysed except in D. armeniaca, and, thus, it was the main or the only component of their irrespective helminth infracommunities. N. tarentolae was found in D. parvula and D. valentini, and S. darevskyi was only recorded in D. armeniaca.

All the helminths found in the Darevskia lizards studied are common in reptiles from the South and South East Europe and the west of the former USSR (Schad et al., 1960; Markov & Bogdanov, 1962; Sharpilo, 1976; Saygi, 1993; Roca et al., 2015, 2016).

The most common helminth in the communities of the analysed hosts is the pharyngodonyd nematode Spauligodon saxicolae (found under two morphotypes, see Jorge et al., 2014; Roca et al., 2016) which should be considered as rock lizards specialist (sensuEdwards & Bush [1989], but also see Roca & Hornero [1994]), since it has been recorded from Darevskia and Podarcis lizard species (Sharpilo, 1976; Roca et al. 1986); Strongyloides darevskyi is in fact a true Darevskia specialist since it has been recorded only from species of this genus (Roca et al., 2016). The cestode N. tarentolae is a generalist species found in many different lizard genera (Roca et al., 1985).

Apart from S. saxicolae no other pharyngodonid were found in any of the searched hosts. This deviates from the usual pattern found in different European lacertid lizards, in which other Spauligodon species frequently share reptile hosts with members of the genera Skrjabinodon (but see Jorge et al., 2014) and Parapharyngodon (García-Adell & Roca, 1988; Roca et al., 1986, 2009; Roca & Hornero, 1994). This contributes to the simple helminth communities found in the studied lizards, as evidenced by the low values of helminth richness, abundance, and diversity (Table 3).

Although depauperate and isolationist helminth communities are common in reptiles (Aho, 1990; Roca & Hornero, 1994), the Darevskia spp. analysed here show the lowest diverse helminth communities within the Palaearctic lacertid lizards. Our results for the two parthenogenetic species are in accordance with those obtained by Roca et al. (2015), who found the extremely poor helminth communities in the also parthenogenetic Darevskia uzzelli and D. bendimahiensis, when compared with their sexual relatives. Similar patterns have also been recorded for the teiid lizards genus Aspidocelis in North America (i.e. McAllister, 1990). Accordingly, in our study, the unisexual D. armeniaca shows the lowest values of helminth species richness and abundance, and the other parthenogenetic form, D. unisexualis, shows lower helminth abundance comparing to the bisexual forms and one of the lowest values of the helminth richness. Nevertheless, the very low values of species richness, abundance and diversity also appeared in the bisexual forms analysed, prevents to infer more general trends on the separation of unisexual and bisexual Darevskia spp. in relation to their helminthfauna. These very poor helminth communities probably are better explained by some biotic characteristics of the hosts, such as the small body size and a low number of interactions with other vertebrates acting as predators or alternative hosts. Moreover, abiotic characteristics, such as climate and vegetation, may also modify the possibilities of lizard hosts for recruiting parasites (Roca et al., 2015). Finally, differences in susceptibility between sexual and asexual lizards have been invoked to explain differences in parasite rates (Moritz et al., 1991). However, Hanley et al. (1995) argued that other factors than host reproductive mode, such as transmission rates (Anderson & May, 1982) or parasite virulence are important in determining patterns of parasitism. Global prevalence of infection of all the searched hosts (Table 2), both unisexual and bisexual, were lower than those found in the bisexual D. rudis across northern Anatolia (Roca et al., 2016), and also were lower for the values of species richness, abundance and diversity. The small range and number of Darevskia populations analysed here likely provided less diversity of environments and recruitment opportunities, rather than intrinsic specific differences, which results in poorer helminth communities than those harboured by D. rudis, a host species with much wider geographical distribution and ecological valence (Roca et al., 2016).

Also all the searched hosts show poorer helminth communities and lower prevalence of infection than other continental Palaearctic rock lizards of the genus Podarcis. As suggested by Roca (2015), probably it might be better explained by the ecological characteristics of hosts and environment than in terms of the phylogeny of the lizard hosts.