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Review of the Helminth Parasites of Turkish Anurans (Amphibia)

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Review of the Helminth Parasites of Turkish Anurans (Amphibia) Sci Parasitol 13(1):1-16, March 2012 ISSN 1582-1366 REVIEW ARTICLE Review of the helminth parasites of Turkish anurans (Amphibia) Omar M. Amin 1, Serdar Düşen 2, Mehmet C. Oğuz 3 1 – Institute of Parasitic Diseases, 11445 E. Via Linda # 2-419, Scottsdale, Arizona 85259, USA. 2 – Department of Biology, Faculty of Science and Arts, Pamukkale University, Kinikli 20017, Denizli, Turkey. 3 – Department of Biology, Faculty of Science, Ataturk University, 25240 Erzurum, Turkey. Correspondence: Tel. 480-767-2522, Fax 480-767-5855, E-mail [email protected] Abstract. Of the 17 species of anurans (Amphibia) known from 6 families in Turkey, 12 species were reported infected with helminths including monogenean, digenean, cestode, nematode, and acanthocephalan parasites. The 17 species are Bufo bufo (Linnaeus, 1758), Bufo verrucosissimus (Pallas, 1814), Bufo (Pseudepidalea ) viridis Laurenti 1768 (Bufonidae), Bombina bombina (Linnaeus, 1761) (Discoglossidae), Hyla arborea (Linnaeus, 1758), Hyla savignyi Audoin, 1827 (Hylidae), Pelobates fuscus (Laurenti, 1768), Pelobates syriacus (Boettger, 1889) (Pelobatidae), Pelodytes caucasicus Boulenger (1896) (Pelodytidae), Pelophylax bedriagae (Camerano, 1882), Pelophylax ridibundus (Pallas, 1771) (formerly known as Rana ridibunda ), Pelophylax caralitanus (Arikan, 1988), Rana camerani (Boulanger, 1886), Rana dalmatina Bonaparte, 1838, Rana holtzi Werner, 1898, Rana macrocnemis Boulanger, 1885, Rana tavasensis Baran and atatür, 1986 (Ranidae). Helminths were not reported in B. verrucosissimus , H. savignyi , P. fuscus , P. bedriagae , and P. caralitanus . The most heavily infected host was P. ridibundus. This host is known to be an aggressive feeder and highly adaptable to a wide variety of habitats and diet. Host species with restricted distribution and limited diet show very light infections, if any. Some of the reported hosts extend their range of distribution outside of Turkey where they were found infected with the same and often with other populations of parasites reflecting the varied invertebrate fauna. The overall diversity of parasite populations per each host species is clearly markedy greater than what this report suggests if the host populations in their total range of distribution are taken into account. Parasites and hosts do not know political borders. Keywords: Helminth parasites; Anurans; Amphibia; Turkey. Received 27/12/2011. Accepted 20/01/2012. Introduction forwarded to the Institute of Parasitology for identification. No locality or collectors’ Perhaps one of the earliest reports on information were provided. A lapse of research amphibian parasites in Turkey is that of Schad on the topic prevailed over the following 35 et al. (1960) who examined nematodes from 35 years until the mid 1990s when few sporadic species of Turkish vertebrate including 5 publications made their appearance. The amphibian species collected in 1953-1954 and works of Baran and Atatür (1986, 1998) seem 1 Sci Parasitol 13(1):1-16, March 2012 ISSN 1582-1366 REVIEW ARTICLE to have ignited a surge of interest in Materials and methods amphibian, especially anuran, parasitology research. This review is based on study of published reports on helminth parasites from Turkish The first decade of the 21st century witnessed anurans from a wide variety of habitats (figure an avalanche of publications, primarily 1). We have decided to develop the present surveys, of the helminth parasites of anurans approach over regular review format that from different regions of Turkey with emphasis packs all information on hosts, parasites, and on areas readily accesible to research and references in one table. Our presentation educational facilities. This is the first attempt allows for comparing parasite populations of to put this information together in 1 report to the same host species in different locations as make some sense out of these unrelated well as comparing parasite populations from reports dealing with individual host species in different host species in the same location. As a separate geographical locations. result, one can examine (1) the impact of habitat and implicitly the intermediate host population in this habitat, and (2) the impact of host species and its feeding behavior on the final expression of parasitemia. Figure 1 . A map showing the major geographical locations from which reported collections were made Results Uğurtaş and Öz (1995), and Yiyit et al. (1999), among others,are also included. The 17 species Distribution and feeding behavior of Turkish are listed by family in alphabetical order. amphibians • Family I: BUFONIDAE The 17 species of amphibians in 6 families known from Turkey and their habitats are 1. Bufo bufo (Linnaeus, 1758) noted below according to Baran and Atatür, (1986, 1998), and Budak and Göçmen (2008), The European common toad lives in damp, among others. Special notes on the feeding rocky or pebbly areas with sparse vegetation behaviour conducive to the establishment of or in forest floors. It is fossorial and forages parasitic infections by Atatür et al. (1993), nocturnally, preying on insects, earthworms Çolak-Yılmaz and Kutrup (2006), Çiçek and and some molluscs. Mermer(2006, 2007), Uğurtaş et al. (2004), 2 Sci Parasitol 13(1):1-16, March 2012 ISSN 1582-1366 REVIEW ARTICLE Distribution: In Turkey, it is found in Middle • Family III: HYLIDAE Anatolia, Western Turkish Thrace, Western and Northeastern Anatolia. 1. Hyla arborea (Linnaeus, 1758) 2. Bufo verrucosissimus (Pallas, 1814) This tree frog is a small arboreal species. It is nocturnal and shelters under leaves in the The Caucasian toad lives in coniferous and daytime. It seeks water only in the breeding deciduous mountain forests upwards to the season, preferring clean, deep, heavily subalpine belt. It prefers wet shaded sites vegetated water. It feeds on various insects and where it feeds on beetles, ants and a wide spiders. variety of crawling terrestial invertebrates especially Myriapoda, caterpillars, Coleoptera, Distribution: In Turkey, this tree frog is known and Formicidae. in northwestern and southwestern Anatolia. Distribution: This species inhabits the 2. Hyla savignyi Audoin, 1827 Caucasus, the Caspian coast line of NW Iran, and northeastern Turkey where some records This tree frog is a nocturnal arboreal species may have been confused with those of B. bufo and shelters under leaves and ground cover which it was considered a subspecies of until during the day. It is normally terrestial except recently. during the breeding season when it seeks water preferably heavily vegetated clean 3. Bufo (Pseudepidalea ) viridis Laurenti water. It feeds on various insects and spiders. (1768) Distribution: In Turkey, this tree frog is found The European green toad is nocturnal but in the southeastern part of Anatolia. shelters in the daytime under stones or within subterranean burrows in gardens or open • Family IV: PELOBATIDAE areas. It is more tolerant to desiccation. Feeding is similiar to that of B. bufo . Yiyit et al. 1. Pelobates fuscus (Laurenti, 1768) (1999) stated that B. (P .) viridis predominantly fed on insectivorous (mosly Coleoptera) The common spade foot lives fossorially in (92.20%) as well as Oligochaeta, Crustacea, loose and soft soil of open plains close to Arachnida, Gastropoda, Diplopoda, Chilopoda ponds. It can descent to up to 1 m in the soil and anuran larvae. and is active nocturnally. Distribution: Widespread in Turkey. Distribution: The common spade foot is known only from Thrace, Turkey. • Family II: DISCOGLOSSIDAE 2. Pelobates syriacus (Boettger, 1889) 1. Bombina bombina (Linnaeus, 1761) The eastern spadefoot toad inhabits self- The fire-bellied toad is an aquatic species constructed burrows in loose and soft soil near occuring usually in shallow waters, temporary ponds and pools. Uğurtaş and Öz (1995) ponds, edges of streams, ditches, and ponds reported that Gastropoda (61.04%) were usually in lowland plains and marshes. It feeds preferred by P. syriacus than other foods mostly on various insects. (Insecta, Arachnida, Oligochaeta, Myriapoda and Crustacea). Distribution: This species is wide spread between Turkish Thrace region and Adapazarı. Distribution: Found in suitable habitats in both Anatolia and Turkish Thrace region. 3 Sci Parasitol 13(1):1-16, March 2012 ISSN 1582-1366 REVIEW ARTICLE • Family V: PELODYTIDAE 3. Pelophylax ridibundus (Pallas, 1771) (Formerly known Rana ridibunda ) 1. Pelodytes caucasicus Boulenger (1896) The Eurasian marsh frog, P. ridibundus (R. The Caucasian parsley frog prefers shady, ridibunda ) is a medium-sized aquatic anuran damp places close to water. It is a nocturnal species. It is diurnal and inhabits lakes, pools, species that shelters under stones in the or slowly flowing streams with much daytime. It feeds on various insects. vegetation. It stays close to water and prefers low plains or marshes. P. ridibundus forages Distribution: Only known from the eastern also at night and has an opportunistic feeding Turkish Black Sea region, with a vertical strategy. It is a highly adaptable species in its distribution of up to 2300 m. habitats and diet which includes dragonflies and other insects, earthworms, and slugs. The • Family VI: RANIDAE larger frogs also eat rodents, smaller amphibians, and fishes. The main diet of P. 1. Pelophylax bedriagae (Camerano, 1882) ridibundus (R. ridibunda ) is Arthropoda (Insecta, Arachnida, Crustacea, Chilopoda, The Levant water frog live most of the time in Diplopoda), Gastropoda, Annelida, Pisces water with rich aquatic vegetation
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