A Contribution to the Nematode Fauna of Two Agamid Lizards from Afghanistan.

Information on the recent herpetological and related parasitological collections are very rarely available for Afghanistan. We examined two species of the family Agamidae, Laudakia nuristanica and Paralaudakia caucasia for the presence of the intestinal helminth fauna. Overall, we examined 13 specimens of these lizards and found three species of helminths (Abbreviata achari, Thelandros masaae, T. taylori) in a single specimen of L. nuristanica and four species (A. achari, T. baylisi, T. taylori, P. kasauli) in three specimens of P. caucasia. Here in, we present the first report on the helminth fauna from L. nuristanica, record a new helminth host for P. caucasia and three new country records for the helminth fauna of Afghanistan.

Introduction

Afghanistan is a country situated between two main biogeographical realms, the Palearctic and Oriental (Wagner et al., 2016; Jablonski et al., 2019b). Due to the political instability in Afghanistan for the past 40 years, studies in the field of zoology are rarely seen. However, during the so-called “Golden Age” starting in 1930s of the 20th Century and ending in the mid-1970s, the herpetological field research increased in the country, resulting in the majority of current knowledge (Wagner et al., 2016; Jablonski et al., 2019a). The same is true for parasites related research on amphibians and reptiles of Afghanistan (Chatterji, 1935; Akhtar, 1939; Baruš et al., 1970, 1972; Baruš & Tenora, 1976; Baker, 1987). However, since those times we have only limited new herpetologically related data from the country (Jablonski et al., 2019b). The herpetofauna of Afghanistan currently contains 117 species, with the most species recorded in the family Agamidae (26 taxa; Wagner et al., 2016; Jablonski et al., 2019b). This family is represented in Afghanistan by common, widely distributed species, as well as local endemics.

We examined specimens of two recently collected members of the Agamidae from Afghanistan, Laudakia nuristanica (Anderson & Leviton, 1969) and Paralaudakia caucasia (Eichwald, 1831), for helminth parasites.

Laudakia nuristanica, described from the Nuristan Province in Afghanistan, is an endemic species for eastern part of the Hindu Kush range, and is currently known from the eastern Afghanistan and northwestern Pakistan (Chitral District; Sindaco & Jeremčenko, 2008; Baig et al., 2012). On the other hand, P. caucasia is, besides Afghanistan, known from eastern and southern Georgia, Armenia, Azerbaijan, Dagestan, southern Turkmenistan, northeastern Turkey, Iran, Iraq, and northwestern Pakistan (Szczerbak, 2003; Sindaco & Jeremcenko, 2008). Whereas nematode parasites of P. caucausia were previously studied in different countries of the species range (e.g. Goldberg et al., 2003; Yildirimhan et al., 2006; Molavi et al., 2018, see Tab. 1), nothing is known about the helminths of P. caucasica from Afghanistan. Moreover, there are no published helminth records for L. nuristanica, and we therefore establish the helminth list for this latter species.

Table 1

An overview of the helminths recorded in Paralauakia caucasia.

Species	Family	Region or country	Used hosts taxonomy	References
Oochoristica tuberculata (Rudolphi, 1819)	Anoplocephalidae	Turkey	Paralaudakia caucasia	Yildirimhan et al. (2006)
Abbreviata achari (Mirza, 1935)	Physalopteridae	Pakistan	Calotes versicolor	Goldberg et al. (2003)
Abbreviata uzbekistanica Bogdanov and Markov, 1955	Physalopteridae	Central Asia	Paralaudakia caucasica	Andrusko and Markov (1956)
Abbreviata uzbekistanica Bogdanov and Markov, 1955	Physalopteridae	Turkmenistan	Paralaudakia caucasica	Bogdanov and Markov (1955)
Foleyella candezei (Fraipoiont, 1882) Seurat, 1917	Onchocercidae	Central Asia	Paralaudakia caucasica	Sharpilo (1976)
Foleyella candezei (Fraipoiont, 1882) Seurat, 1917	Onchocercidae	Turkey	Paralaudakia caucasia	Yildirimhan et al. (2006)
Oswaldofilaria chlamydosauri Breinl, 1912	Onchocercidae	Iran	Paralaudakia caucasia	Molavi et al. (2018)
Oxyuris cincta Linstow, 1897	Pharyngodonidae	Transcaucasia	Agama caucasica	Sharpilo (1962)
=Thelandros inquirendum
Parapharyngodon dogieli Markov and Bogdanov, 1965	Pharyngodonidae	Central Asian SSR	Agama caucasica	Sharpilo (1976)
Parapharyngodon kasauli (Chatterji, 1935) Markov and Bogdanov, 1965	Pharyngodonidae	Central Asian SSR	Agama caucasica	Sharpilo (1976)
Parapharyngodon szczerbaki Radchenko and Shapiro, 1975	Pharyngodonidae	Central Asian SSR	Agama caucasica	Sharpilo (1976)
Parapharyngodon tyche Sulahian and Schacher, 1968	Pharyngodonidae	Turkey	Laudakia caucasia	Yildirimhan et al. (2006)
Saurositus agamae agamae Macfie, 1924	Onchocercidae	USSR	Agama caucasica	Sharpilo (1976)
Skrjabinodon pigmentatus (Markov and Bogdanov, 1961)	Pharyngodonidae	Iran	Laudakia caucasia	Rezazadeh et al. (2012)
Baruš and Coy Otero, 1974
Spauligodon lacerate Sharpilo, 1966	Pharyngodonidae	Iran	Laudakia caucasia	Rezazadeh et al. (2012)
Thelandros baylisi (Chatterji, 1935) Petter, 1966	Pharyngodonidae	Iran	Laudakia caucasia	Rezazadeh et al. (2012)
Thelandros markovi Radchenko and Sharpilo, 1975	Pharyngodonidae	Central Asian SSR	Agama caucasica	Radchenko and Sharpilo (1975)
Thelandros markovi Radchenko and Sharpilo, 1975	Pharyngodonidae	Central Asian SSR	Agama caucasica	Sharpilo (1976)
Thelandros popovi Markov and Bogdanov, 1963	Pharyngodonidae	Central Asian SSR	Agama caucasica	Sharpilo (1976)
Thelandros szczerbaki Radchenko and Sharpilo, 1975	Pharyngodonidae	Turkestan and Caucasus, USSR	Agama caucasica	Radchenko and Sharpilo (1975)
Thubunaea baylisi Akhtar, 1939	Physalopteridae	Central Asian SSR	Agama caucasica	Sharpilo (1976)
Thubunaea baylisi Akhtar, 1939	Physalopteridae	Turkey	Laudakia caucasia	Yildirimhan et al. (2006)

Materials and Methods

We found nematodes in four specimens: one adult female of L. nuristanica (DJ8013 [nematodes] = Pakistan Museum of Natural History (PMNH) 4353 [host]) collected on 14 August 2018 at Saiad (34.9995°N, 69.3305°E, WGS84, 1,478 m elevation), Bagram District, Parwan Province, Afghanistan; one adult female of P. caucasia (DJ8011 = PMNH 4411) collected on 13 August 2018 at Chaikal (34.8968°N, 69.1445°E, WGS84, 1,585 m elevation), Parwan Province, Afghanistan; one adult female of P. caucasia (DJ8016 = PMNH 4410) collected on 15 August 2018 at Maymana, (35.9343°N, 64.7812°E, WGS84, 859 elevation) Faryab Province, Afghanistan; and one subadult male of P. caucasia (DJ8019 = PMNH 4412) collected on 13 August 2018 in Samarbagh (34.8359°N, 69.0755°E, WGS84, 1,930 m elevation), Parwan Province, Afghanistan. All these specimens were collected by hand. The specimens of lizards were euthanized, preserved in 10 % formalin, maintained in 70 % ethanol and utilized in helminthological examination. The lizards were identified using identification keys in Anderson and Leviton (1969) and Baig et al. (2012). Overall, we examined 13 specimens of these lizards (seven of L. nuristanica, six of P. caucasia) and deposited them in the herpetological collection of Pakistani Museum of Natural History (PMNH), Islamabad, Pakistan under the voucher numbers PMNH 4346-4347, 4349-4353 (L. nuristanica) and 4410-4415 (P. caucasia). All other examined specimens (9) were without helminth parasites. The research related to animals complied with all the relevant national regulations and institutional policies for the care and use of animals.

The helminthological examination proceeded as follows: the body cavity of examined lizards was opened by a longitudinal incision and the digestive tract was removed and opened. The esophagus, stomach and small and large intestine were examined for helminths utilizing a dissecting microscope. Found nematodes were placed on a glass slide in a drop of lactophenol, a cover slip was added and identifications were made from these temporary wet mounts. The nematodes were preserved in 96 % ethanol, maintained in 70 % ethanol and deposited in the collection of the first author at the Department of Zoology, Comenius University in Bratislava, Slovakia. This collection was subsequently provided to the Harold W. Manter Parasitology Laboratory (HWML), The University of Nebraska, Lincoln, Nebraska, USA. Identifications of nematodes made utilizing Anderson et al. (2009), Gibbons (2010) and comparisons to the original descriptions in Mirza (1935), Chatterji (1935), Adamson and Nasher (1984).

Results and Discussion

In L. nuristanica, we found one Abbreviata achari (Mirza, 1935) (family Physalopteridae), two Thelandros masaae Adamson and Nasher, 1984 (family Pharyngodonidae) and six Thelandros taylori (Chatterji, 1935). Abbreviata achari, was originally described from Calotes versicolor (Daudin, 1802) collected in India (Mirza, 1935), and is also known from Paralaudakia caucasica and Trapelus agilis (Olivier, 1807) from Pakistan (Goldberg et al., 2003). Thelandros masaae was originally described from Acanthocercus yemenensis (Klausewitz, 1954) of Saudi Arabia (Adamson & Nasher, 1984) and is also known from Acanthodactylus cantoris Günther, 1864 and Laudakia nupta from Pakistan (Goldberg et al., 2003). Thelandros taylori was originally described from Saara hardwickii (Gray, 1827) collected in India and Afghanistan (Chatterji, 1935) and has also been reported from Laudakia nupta (De Filippi, 1843) from Pakistan (Goldberg et al., 2003), Laudakia tuberculata (Gray, 1827) from India, Turkmenistan and Afghanistan (Goldberg et al., 2003), Laudakia stellio (Linnaeus, 1758) from Turkey (Yildirimhan et al., 2006), and Paralaudakia himalayana (Steindachner, 1867) from Turkmenistan (Baker, 1987). Voucher helminths were deposited in the Harold W. Manter Parasitology Laboratory (HWML), The University of Nebraska, Lincoln Nebraska as Abbreviata achari, (HWML 110809), Thelandros masaae (HWML 110810) and Thelandros taylori (HWML 110811). Laudakia nuristanica represents a new host record for Abbreviata achari, Thelandros masaae and T. taylori. Thelandros massae and T. taylori represents new country records for Afghanistan.

In P. caucasia, four nematodes species were found. One specimen of Abbreviata achari was found in DJ8011; 27 specimens of Thelandros baylisi (Chatterji, 1935), 20 specimens of T. taylori and two Parapharyngodon kasauli (Chatterji, 1935) (family Pharyngodonidae) were found in DJ8016; 93 specimens of T. taylori were found in DJ8019. Previous reports of helminths in P. caucasia are summarized in Table 1. Voucher specimens of Thelandros taylori were deposited as (HWML 110812). Thelandros taylori in P. caucasica is a new host record. Afghanistan is a new country record for A. achari.

Of the nine genera of Nematoda reported to occur in P. caucasia, four of them are monoxenous (no intermediate host): Oxyuris, Parapharyngodon, Spauligodon and Thelandros and five are heterozenous (utilize intermediate host): Abbreviata, Foleyella, Oswaldofilaria, Saurositus and Skrjabinodon (Anderson, 2000). The one species of Cestoda, Oochoristica is heteroxenous (Conn, 1985). This indicates infection by helminths utilizing different life cycles.

None of the helminths found in either P. caucasia or L. nuristanica were restricted to either species. Each of these helminths infected other hosts indicating that these are generalist helminths. In conclusion, it appears that the occurrence of a particular helminth in a lizard species is the result of chance, reflecting opportunistic feeding habits and the availability of food of appropriate size, rather than phylogenetic affinities. As additional lizards from Afghanistan are examined for parasites, we expect the helminth lists for these lizards will grow.