A helminthological research on three Lacertid lizards species:Acanthodactylus harranensisBaran etal, 2005, Acanthodactylus schreiberi Boulenger, 1878, and Mesalina brevirostris Blanford, 1874, collected from South and South-eastern regions of Turkey

The Southeastern Anatolia Region of Turkey is a region which influenced by both Mediterranean and continental climatic factors (Rosen, 1998). The region has geographically arid character. According to our current literature knowledge, there is not any helminthological study for the lacertid lizards species in this arid region from Turkey. But, there are some limited helminthological studies of the other lizards species (Gekkonidae and Amphisbaenidae) distributed in close to this region: Mimioğlu et al (1963) were reported cysticercoids of Joyeuxiella pasqualei from Hemidactylus turcicus in Adana province, and they also examined the transmission of this helminth to cats. Similiarly, Tınar (1982,1983) recorded a nematode species Pharyngodon laevicauda) and a cestode species (Joyeuxiella pasqualei) in H. turcicus from Adana province. Yıldırımhan etal. (2008) were reported one nematoda (Spauligodon laevicauda) and one acanthocephala species (Macracanthorhynchus catulinus) in H. turcicus from Hatay province and Yıldırımhan et al. (2009) were also observed two nematode taxa (Macropharyngodon micipsae and Thelastomatoid nematoda) in Blanus strauchi from Hatay province. The genus Acanthodactylus Wiegmann, 1834 is inhabited dry and sparsely vegetated regions is a large genus of lacertid lizard widespread in the Iberian Peninsula, all of North Africa and in the Arabian Peninsula, the Middle East (northward to S Turkey, including Cyprus), S Iran, Pakistan, Afghanistan, and NW India (Anderson, 1999).

A. harranensis, Baran et al, 2005 is known from a single locality, including the ruins of the Ancient University in Harran, Şanlıurfa, Turkey and an area covered by hardened grey sand with intermixed blocks of sedimentary fossiliferous rocks. The vegetation is a step, with scattered shrubs mostly less than 50 cm high. It has a plumped body with a total length up to 25 cm (Baran et al., 2005; Baran et al., 2012).

A. schreiberi Boulenger, 1878 is a smaller lizard species than the A. harranensis with a total length of up to 23 cm and found in known Cyprus and Turkey (Tamar et al., 2014). The specimens of A. schreiberi were found within a grassy-bushy-sandy area in Turkey (Baran et al., 2012).

M. brevirostris Blanford, 1874 is distributed from the Sinai Desert (southern tip and Tiran Island), Northern Saudi Arabia, Jordan, Lebanon, Iraq, Kuwait, South Western Iran, the islands of the Arabian Gulf, Pakistan, the Iranian Plateau, Bahrain, Qatar to United Arab Emirates (Ilgaz et al., 2005). Its specimens can be found in the semi-desert plain amongst the numerous small stones. Also the various shrubs and annual grasses are commonly used as refuges. The total body length is up to 17 cm (Ilgaz et al., 2005). So far, there have been no helminthological reports on A. harranensis, A. schreiberi, and M. brevirostris from Turkey. In this examination, helminths of these three lacertid species in Turkey are being reported for the first time.

The lizard samples were studied in this study, were obtained from Dokuz Eylül University, Faculty of Science, Department of Biology, Zoology Museum Collection in İzmir, Turkey. Lizards were collected by hand between 2002 and 2009, in spring and summer seasons (April to June), from four different localities in South and South-eastern part of Turkey. A. schreiberi (1) (Botaş, Adana, 39 m asl, 36°53'1.01" N; 35°55'59.06" E), A. harranensis (3) (Harran, Şanlıurfa, 364 m. asl, 36°52'1.66" N; 39°1'26.93" E), and M. brevirostris (2), (4) (Ceylanpınar, _Ş anlıurfa, 354 m asl, 36°49'36.43" N; 40°0'34.88" E; Akçakale, Şanlıurfa, 350 m. asl, 36°43'19.03" N; 38°58'52.02" E) (Fig. 1).

Fig. 1

In total, 15 adult A. harranensis (5 males, 10 females), 9 adult A schreiberi (7 males, 2 females), and 21 adult M. brevirostris (15 males, 6 females) samples were examined for helminth parasites.

The mean±SD snout-vent length (SVL) of specimens were A. harranensis 83.44±4.80 mm, with a range from 74.90 to 90.48 mm; A. schreiberi 58.78±11.03 mm, with a range from 46.94 to 77 mm, and M. brevirostris 54.97±2.49 mm, with a range from 49.30 to 58.94 mm, respectively.

The body cavities of the lizards were opened by a standard longitidutinal ventral incision. The alimentary canals were excised and separated into stomach, lungs, liver, small-large intestine and rectum. The contents of each part and other organs were poured into glass petri dishes for examination under a stereomicroscope with saline solution. Cestode samples were stained with acetocarmine, dehydrated, cleared in cedar oil; nematodes were also cleared in glycerol. Helminth samples were mounted in Canada Balsame or Entellan®. Acanthocephalan and cestode cyst samples were opened and larvae seperated with thin dissection needles and thin brushes under a stereomicroscope. Intensities are presented as mean values followed by the range. Voucher host specimens were deposited in Dokuz Eylül University, Faculty of Science Department of Biology, Zoology Museum, and parasite specimens were deposited in Pamukkale University, Faculty of Sciences and Arts, Department of Biology, Denizli, Turkey (PAU-HELM-1-5/2014).

The data collected from adult hosts (A. harranensis ) were analysed using Chi-square test with Minitab Version 14 (between two adult sexes and each observed helmint taxa individual numbers), M. brevirostris and A. schreiberi were not analysed due to insufficient observed helminth individual numbers in these lizard species. Also, simple linear regression analyses (Minitab Version 14) were performed (between host SVL and each observed helmint taxa individual numbers) for all studied lizards taxa.

A. harranensis harbored 1 species of nematode (Skrjabinodon sp.), 1 species of cestode (Oochoristica tuberculata), and 1 species of acantocephalan (Centrorhynchus sp., in cystacanth stage); A. schreiberi harbored only 1 unidentified cestode species (in cysticercoid stage) and M. brevirostris harbored 1 species of nematode (Spauligodon saxicolae).

Fifteen A. harranensis examined, 304 individuals of 3 helminth species were determined. Helminths were recorded the embedded in liver, mesenteries, the outer surface of stomach wall, small and large intestines of this species. No individual host was harbored more than 3 helminth species. Of the infected lizards, 5 (33.33 %) were harbored 2 species of helminth, 7 (46.66 %) were harbored 1 species of helminth, the remaining 3 (20 %) were uninfected. Atotal of 25.10±14.88 helminth individuals were found per infected host. Five individuals of 1 unidentified cysticercoid stage cestode species were found 9 A. schreiberi samples. Helminths were recorded embedded in the small intestine mucosa of this species, 1 (11.11 %) individuals of A. schreiberi was harbored only 1 helminth; the remaining 8 (88.89 %) were uninfected. There is 1 helminth individual per infected host.

Twenty-one M. brevirostris examined, 138 individuals of 1 helminth species were observed. Helminths were recorded in the large intestine and rectum of this species, 14 (66.67 %) individuals of M. brevirostris was harbored only 1 helminth; the remaining 7 (33.33 %) lizard samples were uninfected. There were 9.85±8.28 helminth individuals were found per infected host. No helminths were observed in body cavities and the other organs of these three lizard species. Data on helminth infections of A. harranensis, A schreiberi, and M. brevirostris are presented in Table 1.

There is a significant difference between adult sexes of A. harranensis and observed helmint taxa individual numbers (X²=34.113; d.f.=2; P<0.05). Skrjabinodon sp. and O. tuberculata individuals were observed in female lizards, Centrorhynchus sp. individuals is observed in male lizards. M. brevirostris and A. schreiberi were not analysed due to insufficient observed helminth individual numbers in these lizard species. According to results of the simple linear regression analyses: There is no significant correlation existing between SVL of A. harranensis and each observed individual numbers with Skrjabinodon sp. (f=0.03; d.f.= 13; R²= 0.2; P>0.05), O. tuberculata (f=1.78; d.f.= 13; R²=12.1; P>0.05) and Centrorhynchus sp. (f=0.41; d.f.= 13; R² = 3.1; P>0.05); there is no significant correlation was detected between SVL of A. schreiberi and each observed individual numbers with Unidentified cestode species (in cysticercoid stage) (f=0.00; d.f.= 7; R² = 0; P>0.05). Similiarly, there is no significant correlation reported between SVL of M. brevirostris and each observed individual numbers with S. saxicolae (f=0.94; d.f.= 19; R²=5; P>0.05).

The genus, Spauligodon includes a cosmopolitan group of nematode parasites of reptiles according to Bursey and Goldberg (2011a) comprising at least 47 described species, with 20 of them occurring in the Palearctic region (Jorge et al., 2012). Ikromov and Cho (2004) reported S. saxicolae from Eremias velox;Uhlířová (2005) recorded S. saxicolae from Darevskia caucasica;Murvanidze et al. (2008) reported Spauligodon saxicolae in Lacerta strigata, Darevskia saxicola (formerly known as Lacerta saxicola), D. rudis (formerly known as Lacerta rudis) and Dolichopis jugularis (formerly known as Coluber jugularis);Carretero et al. (2011) observed S. saxicolae from Podarcis vaucheri complex. In Turkey, Yıldırımhan (1999) reported S. saxicolae from Anatololacerta danfordi (formerly known as Lacerta danfordi), D. saxicola, Podarcis siculus and P. muralis (Northwestern part of Turkey); S. saxicolae was observed in Eremias strauchi and £ suphani collected from Eastern Part of Turkey (Dusen et al., 2013). Also, Roca et al. (2015) reported S. saxicolae in the samples of Darevskia rudis from northern part of Turkey. In this study, S. saxicolae was observed for first time from A. harranensis.

The genus SkrjabinodonInglis, 1968 has a widely distributed group of nematode parasites of reptile families. Inglis (1968) revised Parathelandros Diesing, 1861, retaining the genus for parasites of Australian amphibians and erecting Skrjabinodon as a new genus for parasites of reptiles (Bursey & Goldberg, 1999). There are several reptile family members infected by different Skrjabinodon species were recorded by various researchers: Gekkonidae (Moravec & Baruš, 1990; Bursey & Goldberg, 1999; Hering-Hagenbeck et al., 2002; Matsuo & Oku, 2002; Jones, 2013; Bursey & Brooks, 2010), Agamidae (Rezazadeh et al., 2012), Corytophanidae (Bursey & Brooks, 2010), Iguanidae (Bundy et al., 1987; Bursey & Brooks, 2010; Bursey & Goldberg, 2007), Phrynosomatidae (Bursey & Brooks, 2010), Polychrotidae (Bursey & Brooks, 2010), Gymnoph-thalmidae (Bursey & Goldberg, 2011b), Lacertidae (Roca & Ferragut, 1989; Hornero & Roca, 1992; Vicente et al., 2000; Yıldırımhan et al., 2011), Anguidae (Bursey & Goldberg, 2006), Teiidae (Bursey & Brooks, 2010), and Scincidae (Vicente et al., 2000; Hering-Hagenbeck et al., 2002; Vicente et al., 2002; Rocha et al., 2003; Bursey et al., 2008; Incedogan et al., 2014). In this study, we observed for the first time Skrjabinodon sp. from A. harranensis.

The genus Oochoristica contains medium sized of tapeworm species parasitic as adults in reptiles and mammals (Hughes et al., 1941; Yamaguthi, 1959). Hughes et al. (1941) published detailed report for O. tuberculata from different reptile species (Acanthodactylus pardalis, Agama agama, A. sanguinolenta, Chalcides ocellatus, Eumeces schneiderii, L. agilis, L. lepida, Podarcis muralis (formerly known as Lacerta muralis), L. ocellata, L. viridis, Pseudopus apodus (formerly known as Ophisaurus apodus), Uromastix acanthinurus, Varanus griseus, Cerastes vipera, Eryx jaculus, and Psammophis sibilans); also Yamaguthi, (1959) reported this cestode from Mabuya, Coelopeltis (synonim of Malpolon);Sharpilo et al. (2001) recorded O. tuberculata from L. agilis;Ibrahim et al. (2005) reported O. tuberculata from Chalcides ocellatus;Bakiev and Kirillov (2007) observed O. tuberculata from V. berus;Murvanidze et al. (2008) recorded O. tuberculata from A. caucasica, and L. strigata;Dugarov et al. (2012) recorded O. tuberculata from E. argus. In Turkey, Yıldırımhan (1999) reported O. tuberculata from L. viridis in Bursa Province; Yıldırımhan et al. (2006) observed O. tuberculata from Laudakia caucasica in Dogubayazıt (Ağrı Province); Yıldırımhan et al. (2011) observed O. tuberculata from L. trilineata in Bursa Province. Also, Dusen et al. (2013) reported O. tuberculata from E. suphani collected from Eastern Part of Turkey. Incedoğan et al. (2014) observed O. tuberculata from Chalcides ocellatus from middle and western parts of Mediterranean region of Turkey. In this study, we observed for the first time O. tuberculata from A. harranensis.

The adults of the acanthocephalan genus Centrorhynchus Lühe, 1911 (Polymorphida: Centrorhynchidae) are parasites mainly of birds of the orders Falconiformes and Strigiformes, but a few species are known from mammals and reptiles. With almost 90 species, this is the largest acanthocephalan genus occurring in birds of prey (Golvan, 1994; Richardson and Nickol, 1995). There are numerous amphibian, reptile, bird, and mammalian hosts records for Centrorhynchus species were presented by different researchers. Nickol (1969) observed cystacanths of C. conspectus from mesenteries in Desmognathus fuscus and Plethodon glutinosus;Marchand and Grita-Timoulali (1992) recorded a paratenic host Bufo regularis;Yıldırımhan et al. (2005) observed cystacanths of Centrorhynchus sp. in Pelophylax ridibundus (formerly known as Rana ridibunda);Dos Santos et al. (2010) observed cystacanths of Centrorhynchus sp. in Rhinella fernandezae (in amphibian hosts). Ward (1940) reported cystacanths of Centrorhynchus sp. in intestinal wall of Natrix sipedon;Schmidt and Kuntz, (1969) reported the paratenic reptile hosts of C. spilornae in Dinodon rufozonatum, Psammodynastes pulverulentis Agkistrodon acutus and Trimeresurus stejnegeri (in reptile hosts).

Vancleave (1918) recorded C. pinguis intestine of Pica pica;Ward (1956) observed C. milvus in Milvus migrans;Schmidt and Neiland (1966) reported C. kuntzi in Buteo magnirostris, C. nicaraguensis in Dromococcyx phasianellus, C. crotophagicola in Piaya cayana and Crotophaga sulcirostris, C. albidus in Ictinia plumbea, and 1 unidentified Centrorhynchus species from Tyto alba;Schmidt and Kuntz (1969) observed C. spilornae and C. amphibius in Spilornis cheela, Accipiter soloensis, A. virgatus affinis, and Hirundo rustica;Thatcher and Nickol, (1972) observed C. giganteum and C. tumidulus in Buteogallus urubitinga, Leucopternis semiplumbea Heterospizias meridionalis and also, unidentified Centrorhynchus sp. in Leucopternis princeps. Nickol (1983) reported C. kuntzi and C. spinosus in Bubo virginianus, Buteo jamaicensis, B. lineatus, B. platypterus, Melanerpes carolinus, and Strix varia: Ewald and Crompton (1993) reported C. aluconis in Strix aluco;Tezel et al. (2014) recorded C. amphibius in B. buteo (in bird hosts).

Cable and Quick (1954) reported cystacanths of Centrorhynchus sp. from Herpestes javanicus auropunctatus;Richardson (1993) cystacanths of C. wardae in Didelphis virginiana;Yabsley and Noblet, (1999) observed the cystacanths of C. conspectus in Procyon lotor;Kirillova and Kirillov (2007) reported cystacanths of C. aluconis in Sorex araneus (in mammalian hosts). In this study, we observed for the first time Centrorhynchus sp. from A. harranensis, in view of the results obtained, it can be concluded that Centrorhynchus sp. parasitised A. harranensis as a paratenic host in Turkey.

In summary: A. harranensis represents new host records for O. tuberculata, Skrjabinodon sp., and Centrorhynchus sp. (in cystacanth stage), A. schreiberi represents new host record for unidentified cestode species (in cysticercoid stage), and also, M. brevirostris represents new host records for S. saxicolae; from Turkey. In this investigation, we expanded the zoogeographical and host-range distribution of various helminth species of Turkish reptile helminth fauna.