Pelophylax cf. bedriagae

Pictures

Picture	Title	Caption	Copyright
Title Water frogs Caption Water frogs from Silifke (southern Turkey), brownish and greenish specimens. From Plötner (2005). Copyright Jörg Plötner	Water frogs	Water frogs from Silifke (southern Turkey), brownish and greenish specimens. From Plötner (2005).	Jörg Plötner
Title Water frog male Caption Water frog male from Ceyhan (south-eastern Turkey). From Plötner (2005). Copyright Hansjürg Hotz	Water frog male	Water frog male from Ceyhan (south-eastern Turkey). From Plötner (2005).	Hansjürg Hotz
Title Water frog male Caption Male water frog from the Black Sea coast (north-eastern Anatolia). From Plötner (2005). Copyright Hansjürg Hotz	Water frog male	Male water frog from the Black Sea coast (north-eastern Anatolia). From Plötner (2005).	Hansjürg Hotz
Title Habitat Caption Stagnant water in south-western Turkey - habitat of the caralitanus lineage. Copyright Cigdem Akin	Habitat	Stagnant water in south-western Turkey - habitat of the caralitanus lineage.	Cigdem Akin
Title Habitat Caption Channel in Fethiye (southern coastal part of Turkey) inhabited by frogs of the cerigensis lineage. Copyright Cigdem Akin	Habitat	Channel in Fethiye (southern coastal part of Turkey) inhabited by frogs of the cerigensis lineage.	Cigdem Akin
Title Habitat Caption Vegetation-rich brook in Edirne (European part of Turkey) where P. cf. bedriagae and P. ridibundus co-occur. Copyright Cigdem Akin	Habitat	Vegetation-rich brook in Edirne (European part of Turkey) where P. cf. bedriagae and P. ridibundus co-occur.	Cigdem Akin
Title Habitat Caption Water frog habitat in south-eastern Turkey. Copyright Cigdem Akin	Habitat	Water frog habitat in south-eastern Turkey.	Cigdem Akin
Title Habitat Caption Flowing water in northern Anatolia - natural habitat of P. cf. bedriagae. Copyright Cigdem Akin	Habitat	Flowing water in northern Anatolia - natural habitat of P. cf. bedriagae.	Cigdem Akin
Title Habitat Caption Habitat of P. cf. bedriagae in Sanliurfa (eastern Turkey). Copyright Cigdem Akin	Habitat	Habitat of P. cf. bedriagae in Sanliurfa (eastern Turkey).	Cigdem Akin

Identity

Preferred Scientific Name

• Pelophylax cf. bedriagae

Other Scientific Names

• Pelophylax bedriagae (Camerano, 1882)
• Pelophylax caralitanus (Arikan, 1988)
• Pelophylax ridibundus (Pallas, 1771)

International Common Names

• English: Anatolian lake frog; Anatolian marsh frog; Anatolian water frog

Local Common Names

• Germany: Anatolischer Wasserfrosch
• Turkey: kurbag

Summary of Invasiveness

In the last three to four decades, Anatolian water frogs (Pelophylax cf. bedriagae) have been introduced into several western European countries mainly for culinary purposes but also as ornamental animals for garden ponds. P. cf. bedriagae comprises several distinct evolutionary lineages that exhibit a high genotypic and phenotypic variability. A clear differentiation of P. cf. bedriagae from closely related water frog species, for example P. ridibundus and P. bedriagae, requires molecular tools. P. cf. bedriagae may influence native water frog populations ecologically as predators and disease vectors, or genetically by transmitting allochthonous genes into the endemic gene pool. Rapid dispersion of P. cf. bedriagae is documented for Belgium, France, Switzerland, and south-western Germany. As a consequence fundamental genetic changes of the native gene pools and a decrease of autochthonous water frogs can be expected.

Taxonomic Tree

• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Chordata
•             Subphylum: Vertebrata
•                 Class: Amphibia
•                     Order: Anura
•                         Family: Ranidae
•                             Genus: Pelophylax
•                                 Species: Pelophylax cf. bedriagae

Notes on Taxonomy and Nomenclature

For many years it was thought that only a single water frog species, Pelophylax ridibundus (Pallas, 1771) (formerly Rana ridibunda), inhabited Turkey (e.g., Bodenheimer, 1944; Mertens, 1952; Basoglu and Özeti, 1973), even though large specimens with orange spotted venters had been reported in the Beysehir Lake (Bodenheimer, 1944; Basoglu and Özeti, 1973). Based on bioacoustic and morphometric data, it was also suggested that the single species inhabiting Anatolia was Pelophylaxbedriagae rather than P. ridibundus (e.g., Schneider et al., 1992; Schneider and Sinsch, 1999; Sinsch and Schneider, 1999; Schneider and Sinsch, 2001). P. bedriagae was originally described under the name Rana levantina by Schneider et al. (1992). As pointed out by Dubois and Ohler (1994), R. levantina is a junior synonym of Pelophylax (Rana) bedriagae (Camerano, 1882). DNA data (e.g. Plötner et al., 2001, 2009; Akin et al., 2010b; Ç. Akin, Middle East Technical University, Ankara, Turkey, unpublished data) clearly demonstrate, however, that Anatolian water frogs are not conspecific with either European lake frogs (P. ridibundus sensu stricto) or P. bedriagae from the Near East (western Syria, Jordan, probably Palestine) and northern Egypt. Instead, they probably represent several distinct species (Akin et al., 2010b; Plötner et al., 2010). Because the systematic status of Anatolian water frogs is not yet entirely clear we provisionally call these frogs Pelophylax cf. bedriagae.

On the Anatolian mainland three main mitochondrial (mt) haplogroups (named MHG4, 5, and 6) can be differentiated (Akin et al., 2010b; Plötner et al., 2010). MHG6 shows the highest diversity; it is distributed from western Anatolia to the northern shore of the Caspian Sea including the type locality of Pelophylax ridibundus (Atyrau, Kazakhstan). The two other Anatolian MHGs (4 and 5) are restricted to the south-eastern part of Turkey east and west of the Amanos mountains. MHG6 can be differentiated into four subgroups that comprise forms that were described as distinct species and subspecies. MHG6a, for example, is characteristic of a lineage that was described as P. ridibundus caralitanus by Arikan (1988). The separation of the caralitanus lineage was mainly based on the orange maculation of the belly, a characteristic feature of almost all frogs from the Lake District and the Konya plain. Compared to other Anatolian lineages, caralitanus individuals differ in karyological characters (Alpagut and Falakali, 1995; Alpagut Keskin and Falakali Mutaf, 2006), some body proportions, allele frequencies of protein coding loci (Jdeidi, 2000, Jdeidi et al., 2001), and mtDNA sequences (Plötner and Ohst, 2001; Plötner 2005, Akin et al., 2010b, Plötner et al., 2010). These findings, in concert with the syntopic occurrence of individuals that belong to different mtDNA lineages, led to the suggestion that caralitanus represents a distinct species (Jdeidi, 2000; Jdeidi et al., 2001, Plötner 2005). New mtDNA and nuclear DNA data, however, raise doubts about the species status of  P. caralitanus; the small genetic mtDNA divergence values observed among the four subgroups of MHG6 (uncorrected p distances <2.2%; Plötner et al., 2010) and genetic data obtained from three nuclear markers (ITS-2, SAI-1, RanaCR1; Plötner et. al., 2009; Ç. Akin (Middle East Technical University, Ankara, Turkey), T. Ohst (Humboldt-Universität zu Berlin, Germany), and J. Plötner (Museum für Naturkunde Berlin, Germany), unpublished data) do not support the existence of a separate species. Moreover, inconsistencies between morphology and mtDNA were observed in southwestern Anatolia. Here, individuals with caralitanus specific orange coloured venters had non-caralitanus haplotypes and individuals with black spotted or white coloured venters often had caralitanus specific haplotypes (Akin, 2007; Akin et al., 2010a). These findings clearly indicate extensive gene flow between distinct water frog lineages along transition zones.

In general, antihybridization mechanisms are only weakly developed in western Palaearctic water frogs and hybridization between distinct evolutionary lineages is common (e.g., Plötner et al., 2010). F1 hybrids often show a relatively high viability and fertility and may backcross with the parental lineages, an indication that genetically distinct (species-specific) genomes are still compatible. In areas where different mtDNA lineages overlap, considerable gene flow and horizontal transfer of mt genomes can be expected as a result of continuous primary hybridizations and backcrosses (e.g. Plötner et al. (2008); Holsbeek et al. (2008) found an example of a hybrid swarm of P. ridibundus and P. cf. bedriagae in Belgium). For these reasons, mitochondrial markers have only limited value for species identification in this group, and systematic conclusions cannot be drawn on the basis of single molecular data but require a holistic approach that includes molecular and bioacoustic investigations as well as ethological and biogeographic data.

Age estimates of Anatolian water frog (P. cf. bedriagae) lineages based on different models of DNA sequence evolution are in good agreement with the chronology of events in the history of crustal deformation and landscape development in Anatolia. The observed rates of divergence imply a time window of ca. 3 million years for the diversification of most Anatolian lineages, so the radiation of these lineages appears to have taken place around the Pliocene-Pleistocene boundary (Akin et al., 2010b; Plötner et al., 2010).

Description

Anatolian water frogs (P. cf. bedriagae) are members of the western Palaearctic water frog group, distinguished from the Palaearctic brown frog group by paired external lateral vocal sacs in males, extension of the webbing of the feet to the toe tips, absence of a black face mask from the eye to the tympanum, and presence of dark mottling on the inner thigh surfaces. The body size is lineage-specific; frogs of the caralitanus lineage (MHG6a) are on average larger than individuals of the other Anatolian lineages. Caralitanus females can reach snout-vent-lengths of about 13 cm (Arikan et al., 1998), and males about 11 cm (Ayaz et al., 2007). Individuals of non-caralitanus lineages are usually smaller; in the vicinity of Erzurum (NE Anatolia), for example, females had maximal snout-vent-lengths of about 10 cm and males about 10 cm (e.g. Ayaz et al., 2004).

The metatarsal tubercle is small and appears triangular or cylindrical. The dorsal coloration is highly variable from green, greenish-grey, or olive to light or dark brown with irregular green, brown or blackish spots that are also seen on parts of the hind legs. Some frogs, however, show totally homogenously coloured backs. In many populations, individuals may have a light green or yellowish vertebral stripe (e.g., Budak et al., 2000). The belly is white, greyish-white, or yellowish and usually black spotted or maculated; frogs from the Anatolian Lake District (the caralitanus lineage) exhibit an orange spotted belly. The vocal sacs of males are usually grey or blackish (e.g., Schneider and Sinsch, 2001).

The mating call of P. cf. bedriagae males is very similar to the calls of P. bedriagae from the Near East (e.g. Schneider and Sinsch, 2001). In western Turkish frogs, calls consisted on average of 5-12 pulse groups depending on water temperature (Joermann et al., 1988). Similarly, mating calls of water frogs from Ankara, Antakya, Bodrum, Hopa, and Mersin consisted of, on average, 5-14 pulse groups; calls of individuals from Beysehir (the caralitanus lineage) were composed of 6-12 pulse groups (Jdeidi, 2000). Local differences in several call parameters as described by Schneider and Sinsch (2001) may reflect specific characters of distinct genetic lineages; their taxonomic relevance, however, is not yet clear.

Distribution

The lineage-specificity of mtDNA provides an opportunity to localize the area of origin of allochthonous water frogs. P. cf. bedriagae specific haplotypes (MHG4-6) are distributed from western Turkey to central Russia; haplotypes of this group have also been found in Iran and Syria (Plötner et al. 2001; Akin et al., 2010b; Ç. Akin et al., Middle East Technical University, Ankara, Turkey, unpublished data). In north-eastern Greece and west of the Caspian Sea, MHG6 occurs syntopically with haplotypes characteristic of European P. ridibundus (Akin et al. 2010b; Plötner et al. 2010; J. Plötner (Museum für Naturkunde Berlin, Germany) and S. N. Litvinchuk, Institute of Cytology, Russian Academy of Sciences, St. Petersburg, Russia), unpublished data). Haplotypes of MHG4 are found in the Cilician plain west of the Amanos Mountains and haplotypes of MHG5 east of it (Akin et al., 2010b; Plötner et al., 2010).

MHG6 can be divided into four subgroups (6a-d). Haplotypes of subgroup 6a (cf. caralitanus) are mainly found in southwestern Turkey. They occur syntopically with haplotypes of subgroup 6c (cf. bedriagaesensu stricto), for example, in southwestern and central Anatolia, and with haplotypes of subgroup 6b (cf. cerigensis) in southern Anatolia (Akin, 2007; Akinet al., 2010a, b). In the Gökova plain (Silifke) MHG6a overlaps with MHG4. MHG6b is distributed west of Antalya; haplotypes of this group have been found in several populations of the coastal area and on the nearby Greek islands of Rhodos (Rhodes) and Karpathos. Haplotypes of MHG6c are distributed from western Anatolia to the northern shore of the Caspian Sea; this group occurs in the whole of Anatolia except the costal region east of Antalya, and west and east of the Amanos Mountains. Haplotypes of subgroup 6c were also detected on several Mediterranean islands along the Anatolian coast, for example Chios, Lesvos (Lesbos) and Samos. Haplotypes of subgroup 6d (Euphrates) have been found in the Tigris and Euphrates catchments of north-eastern Syria, eastern Anatolia, and western Iran (Akin et al., 2010b; J. Plötner, Museum für Naturkunde Berlin, Germany, unpublished data).

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

History of Introduction and Spread

Before appropriate molecular methods became available, allochthonous water frogs could not be differentiated from European lake frogs (P. ridibundus sensu stricto) in most cases. Therefore, the history of introduction is difficult to reconstruct. In Switzerland, for example, lake frogs of unknown origin are known to have been introduced between 1920 and 1950 (FOEN, 2006). In Belgium, lake frogs, probably introduced P. ridibundus, were first observed in the 1970s in the vicinity of Ghent (Bauwens and Claus, 1996). It is assumed, however, that Anatolian frogs (P. cf. bedriagae) have been introduced more recently in this country (Kok, 2001).

In a recent study of 87 water frog populations across northern Belgium, 54% of the sample sites contained non-native water frogs; in 26% of sites, individuals with P. cf. bedriagae (Anatolian) specific genetic markers were found (Holsbeek et al., 2008). Among 111 individuals from 15 French water frog populations, about 20% possessed mitochondrial genomes characteristic of P.cf. bedriagae (T. Ohst, Humboldt-Universität zu Berlin, Germany, unpublished data). Based on protein electrophoretic data obtained from 11 water frog populations along the Rhone River in France, about 55% of the populations were genetically influenced by allochthonous forms, including P. cf. bedriagae (Pagano et al., 2003). In a Swiss sample of 33 frogs, 6 individuals (18%) from four localities in close proximity to each other possessed Anatolian haplotypes (Ohst, 2008).

In south-western Germany an increase in lake frogs considered as P. ridibundus has been noticed since the 1970s (Sowig et al., 2007). The main cause of this development was probably continuing immigration of allochthonous individuals, including P. cf. bedriagae, from the neighboring countries Switzerland and France (Ohst, 2008). Besides migration, intentional introductions of allochthonous water frogs have been reported, for example in the Ruhr valley by employees of the university in Bochum (Kordges, 1988; Schröer, 1997). In a sample of 366 water frogs collected at 44 localities in western Germany, about 5% had mitochondrial genomes characteristic of P. cf. bedriagae; about 8% possessed P. cf. bedriagae-specific ITS-2 alleles (Ohst, 2008). Frogs with Anatolian alleles were recorded only south of Karlsruhe, clearly indicating northward migration of allochthonous frogs from Switzerland and France.

Introductions

Risk of Introduction

Allochthonous water frogs are still being imported and cultivated for culinary purposes, especially in France (Pagano et al., 2001; 2003; Schmeller et al., 2007) and Italy (C. C. Bilgin and Ç. Akin (Middle East Technical University, Ankara, Turkey), and J. Plötner (Museum für Naturkunde Berlin, Germany), unpublished data), and for pet shops and garden ponds, for example in Belgium (Holsbeek et al., 2008, 2010). In this country a growing demand for water frogs by ornamental pond owners is recognized. Although intended for garden ponds, these frogs often escape into natural biotopes. A successful establishment of Anatolian water frogs (P. cf. bedriagae) in western and Central Europe is probably linked with global warming; frogs are now able to hibernate in a more temperate climate. Further spread of P. cf. bedriagae is favoured by running waters (rivers, channels, ditches, etc.). Although there is no evidence for introductions with fish spawn, this possibility cannot be excluded completely. To prevent further spread of P. cf. bedriagae to "unpolluted" areas such as eastern Europe, the world-wide trade in living water frogs including eggs and tadpoles must be stopped by legislation.

Habitat

P. cf. bedriagae are semi-aquatic frogs, inhabiting (and breeding in) a wide variety of flowing and stagnant water habitats such as reservoirs, small ponds, banks of slowly flowing streams and rivers, irrigation channels, ditches, and even temporary water bodies (e.g. Beerli, 1994; Schneider and Sinsch, 2001; Akin et al., 2010a; J. Plötner, Museum für Naturkunde Berlin, Germany, unpublished data). P. cf. bedriagae, like closely related species of the P. ridibundus group, is probably tolerant of stagnant and fairly brackish water (e.g. Günther, 1990; Baier et al., 2009). Typical breeding waters are shallow (50-150 cm) and have a high sun exposure and a rich vegetation comprising plants such as Eleocharis palustris, Carex elata, Potamogeton spp., and Ceratophyllum submersum (e.g. Ayaz et al., 2007). On the other hand, water frogs have also been observed in small dirty ponds, streams, and rivers polluted with agricultural and industrial sewage, especially in western Anatolia (Ç. Akin, Middle East Technical University, Ankara, Turkey, personal communication, 2009). Because of their relatively broad ecological plasticity, P. cf. bedriagae can adapt easily to the ecological conditions of western Europe; here, they occur mainly along rivers and floodplains (e.g. Ohst, 2008; Holsbeek et al., 2008) but also in garden ponds (Holsbeek et al., 2008, 2010).

It is assumed that P. cf. bedriagae, like its close relative the European lake frog P. ridibundus, hibernates in the beds of water bodies (e.g. Berger, 1982). Hibernation under water potentially poses physiological problems because of the scanty amount of oxygen in the water (e.g. Lutschinger, 1988). Oxygen deficiency may occur during cold winters when the water is covered by ice; such conditions often cause a high mortality.

Habitat List

Biology and Ecology

Genetics

The diploid genome of Anatolian water frogs (P. cf. bedriagae) consists of 2N=26 chromosomes, five larger and eight smaller pairs (e.g. Alpagut and Falakali, 1995). Population-specific differences in the morphology of some chromosomes were described by Alpagut and Falakali (1995) and Alpagut Keskin and Falakali Mutaf (2006), these probably reflect lineage-specific characters of caralitanus and non-caralitanus frogs.

P. cf. bedriagae possesses several segregating protein-coding alleles (Beerli et al., 1996; Jdeidi, 2000; reviewed by Plötner and Ohst, 2001) that can be used as diagnostic markers to differentiate between allochthonous and autochthonous (European) water frog lineages (Pagano et al., 2003). Likewise, microsatellite markers can be used to assign individuals to parental species or to identify them as putative hybrids (Holsbeek et al., 2008). To date, however, no fixed  alleles have been found in Anatolian frogs. Among 20 Turkish populations represented by 378 specimens, five out of twelve enzyme-coding loci were polymorphic within or between populations; the highest genetic variability was detected in Lake District populations (cf. caralitanus), with an average heterozygosity of 0.12 (Jdeidi, 2000).

In their mitochondrial DNA, Turkish water frogs exhibit huge variability; among 612 sequences, 116 mitochondrial haplotypes were detected on the basis of the 340-bp NADH dehydrogenase subunit 3 (ND3) gene alone; 119 sequences of the ND2 gene yielded 80 haplotypes (Akin et al., 2010b). Because there are many lineage-specific substitutions, both genes are appropriate markers for reconstructing mitochondrial phylogenies (Plötner 2005, Akin et al. 2010b, Plötner et al. 2010). The non-coding nuclear internal transcribed spacer 2 (ITS-2) and the serum albumin intron 1 (SAI-1) possess sites specific for Anatolian water frogs (P. cf. bedriagae) and European water frogs (P. ridibundus), respectively (Ohst, 2008; Plötner et al., 2009). In all western Palaearctic water frogs investigated, the SAI-1 contains a 5' truncated chicken-repeat-like retroelement named RanaCR1 (Plötner et al., 2009). The 3’ end of RanaCR1 is defined by a perfect octameric repeat. Length variation in water frog SAI-1 sequences is caused by deletions at both the 5’ and 3’ ends of RanaCR1. Unlike other CR1 elements, RanaCR1 contains a CA microsatellite upstream of the octameric repeats in its 3’ UTR. Several sites of RanaCR1 are species-specific, so this retroelement can be used as a diagnostic marker. Length polymorphisms and specific nucleotide substitutions of RanaCR1 can be used as diagnostic characters for differentiation between distinct water frog lineages (Plötner et al., 2009), but introgression means that other markers must also be used -- a single marker is insufficient for species identification (J. Mergeay, Instituut voor Natuur- en Bosonderzoek, Geraardsbergen, Belgium, personal communication, 2014).

Reproductive biology

Little is known about reproductive biology of P. cf. bedriagae; it can be assumed, however, that they reproduce in a similar way to European lake frogs (P. ridibundus). Mating starts with the onset of spring, the particular date depending on the geographic region and the specific weather conditions. Generally, most matings occur in May and June (Basoglu and Özeti, 1973). In coastal areas of the Aegean region, the breeding season starts in early March and continues until the end of April (Çaydam, 1973 cited in Ayaz et al., 2007) while in regions with a continental climate or at higher altitudes the reproductive period can last through to the end of June.

Lake frog females (P. ridibundus) usually lay between 2,000 and 10,000 eggs in a few clutches among water plants (e.g., Günther 1990); the egg number correlates with body size (e.g. Berger and Uzzell, 1980). According to Basoglu and Özeti (1973), P. cf. bedriagae females lay 5000-10000 eggs in a few clutches in open water or among aquatic plants.

Larvae hatch approximately 7-10 days after eggs have been laid and complete metamorphosis two to three months later, depending on water temperature and food supply. Water temperatures below 11 °C and above 33 °C are unfavourable for normal embryonic development of central European lake frogs (Günther, 1974); embryogenesis of P. cf. bedriagae is thought to proceed in a similar range of water temperature values (13.3 °C to 33.5 °C) to that in which the adult males call (Schneider and Sinsch, 2001).

If the environmental conditions during larval development are not optimal, a few tadpoles may hibernate and complete metamorphosis in the year after hatching, especially in continental regions.

Nutrition

P. cf. bedriagae feeds mainly on terrestrial arthropods (especially insects and spiders), molluscs, nematodes, and annelids, but has also been observed to prey on small vertebrates, for example fish, bird nestlings, small mammals, and other amphibians including juveniles of their own species (e.g. Yilmaz and Kutrup, 2006, Çiçek and Mermer, 2006, 2007). Adult P. cf. bedriagae are generalist and opportunistic predators; their diet is strongly influenced by prey availability. In contrast to adults, tadpoles are herbivores and detritivores; they eat algae, dead organisms, and plants.

Associations

In its natural range, P. cf. bedriagae is commonly associated with the southern crested newt (Triturus karelini), the fire bellied toad (Bombina bombina), the common tree frog (Hyla arborea), and the green toad (Bufo viridis) (Ayaz et al., 2007). In Central Europe it co-occurs in the same habitats as the endemic water frog forms P. ridibundus and P. kl. esculentus (Ohst, 2008; Holsbeek et al., 2008). In Anatolia, it is typically associated with certain reptile species, for example grass snakes (Natrix natrix), dice snakes (Natrix tessellata), and the European pond turtle (Emys orbicularis), which all prey on water frogs. Larger water bodies, such as channels and lakes, are usually inhabited by different fish communities and aquatic birds that may prey on water frogs.

Climate

Latitude/Altitude Ranges

Water Tolerances

Natural enemies

Notes on Natural Enemies

Potential predators for adult water frogs include several mammals (e.g. racoon (Procyon lotor) and polecat (Mustela putorius)), bird species (especially egrets (Ardeidae) and storks (Ciconiidae)), water snakes (genus Natrix) and turtles (Emys spp., Mauremys spp.). Carnivorous water insects (e.g. dragonfly larvae (Odonata) and great diving beetles (Dytiscidae)), many fish species, and different aquatic birds (e.g. ducks (Anatidae)) feed on eggs and larvae; some carnivorous fish species (e.g., pike, Esox lucius) even prey on juvenile and adult frogs (Ayaz et al., 2007; reviewed by Günther, 1990).

Means of Movement and Dispersal

Natural dispersal (non-biotic)

Lake frogs (P. ridibundus) migrate over water and land, especially along floodplains and river systems (e.g. Heym, 1974). The migration behaviour of Anatolian frogs (P. cf. bedriagae) is unknown; they are probably capable of long-distance travel over land and will eventually disperse to suitable habitats, even if the water bodies are not connected.

Intentional introduction

In Belgium, P. cf. bedriagae are introduced intentionally as ornamental animals or pets for garden ponds (e.g., Holsbeek et al., 2008, 2010). It is likely that frogs from Anatolia have escaped from the food trade or been deliberately released into the wild in France, Switzerland, and probably Italy.

Pathway Causes

Impact Summary

Environmental Impact

Allochthonous water frogs prey on other amphibians including native water frogs (P. lessonae, P. ridibundus, P. esculentus). Therefore, high densities of allochthonous individuals may cause a substantial decrease in the population size of syntopic indigenous amphibian species. Furthermore, larvae of allochthonous forms compete with larvae of autochthonous species for food, which may cause food scarcity under special circumstances. Allochthonous water frogs may also transmit pathogens (for example Batrachochytrium dendrobatidis and Ranavirus, e.g. Jancovich et al., 2003; Ohst et al. 2005; Fischer and Garner, 2007; Federici et al., 2008) and parasites such as Digenea, Nematoda, Acanthocephala, and Hirudinea species (Yildirimhan et al., 2005) to indigenous populations.

Introgressive hybridisation may lead to a decrease of the indigenous water frog species P. ridibundus and P. lessonae. It may also influence the structure and dynamics of native water frog populations composed of P. lessonae and P. esculentus (the L-E system), those composed of P. ridibundus and P. esculentus (the R-E system), or diploid and triploid P. esculentus (pure hybrid populations) (Uzzell and Berger, 1975). P. esculentus usually excludes one parental genome from its germline prior to meiosis (in the L-E system the lessonae genome; in the R-E system either the ridibundus genome or less frequently the lessonae genome) and produces haploid gametes that contain an unrecombined genome of the allotopic parental species (reviewed by Plötner, 2005). This clonal mode of reproduction, called hybridogenesis (Schulz, 1969), enables the hybrid to reproduce by backcrosses with the syntopic parental species. It is not known whether and to what extent allochthonous forms have already influenced these unique population systems. Preliminary data from Belgium demonstrate that allochthonous water frogs can have a rapid and massive impact on the genetic structure of P. esculentus populations (G. Holsbeek, Katholiek Universiteit Leuven, Belgium, unpublished data); introgression with P. ridibundus is extensive where both it and P. cf. bedriagae occur; and hybridization with P. kl. esculentus has also been observed (Holsbeek et al. 2010). On the other hand it seems that P. cf. bedriagae, unlike other species, does not have the mechanism of meiotic drive to preferentially select for certain gamete types above other types, and that introgressed individuals (cf. bedriagae x ridibundus) do not always have it (J. Mergeay, Instituut voor Natuur- en Bosonderzoek, Geraardsbergen, Belgium, 2014).

Because genomes of ridibundus-like frogs are almost all compatible and antihybridization mechanisms are only weakly developed in western Palaearctic water frogs (e.g. Berger et al., 1982; 1994; Plötner et al., 2010), hybridisations between native and introduced individuals are common; about 41% of water frogs collected in south-west Germany possessed genetic characters of both allochthonous and autochthonous forms. Such hybridisation events are not restricted to the F1 generation; some hybrids even possessed genetic characters of different autochthonous forms (Ohst, 2008).

It is known from crossing experiments that interspecies crosses between Central European P. ridibundus and P. lessonae lead to hybridogenetic P. esculentus, whereas crosses between Balkan P. kurtmuelleri and P. lessonae result in non-hybridogenetic hybrids that are almost all sterile (Hotz et al., 1985; Berger et al., 1994). On the other hand, matings between P. esculentus which inherit the ridibundus genome and allochthonous lineages of the ridibundus group including Anatolian frogs (P. cf. bedriagae) may lead to viable ridibundus-like hybrid forms, as observed in Belgium by Holsbeek et al. (2010).

Because water frog males most probably prefer larger over smaller females, it can be expected that autochthonous P. lessonae and P. esculentus males will prefer larger P. cf. bedriagae females over females of their own species. Such mating preferences in concert with viable and fertile hybrids could explain the increase in lake frog densities in different regions of Europe (e.g., Sowig et al., 2007; Holsbeek et al., 2008).

Threatened Species

Risk and Impact Factors

• Proved invasive outside its native range
• Has a broad native range
• Abundant in its native range
• Highly adaptable to different environments
• Capable of securing and ingesting a wide range of food
• Highly mobile locally
• Fast growing
• Has high reproductive potential
• Gregarious
• Has high genetic variability

• Changed gene pool/ selective loss of genotypes
• Conflict
• Reduced native biodiversity
• Threat to/ loss of native species

• Competition (unspecified)
• Hybridization
• Predation

• Highly likely to be transported internationally deliberately
• Highly likely to be transported internationally illegally
• Difficult to identify/detect in the field
• Difficult/costly to control

Uses

In Turkey, huge numbers of water frogs are still collected for export (e.g. Ayaz et al., 2007), especially to France and Italy. In 1991, 1321 tonnes of ranid frogs were produced for human consumption in Turkey; in 1998 100 tonnes were still produced (Teixeira et al., 2001, cited in a CCM study (Daszak et al., 2006). In 2005, 507 tonnes of frog legs were exported by Turkish companies, mainly to France (Semercioglu, 2006). In 2009, a similar amount (478 tonnes), comprising living animals and frozen and fresh chilled meat, was exported (C. C. Bilgin and Ç. Akin (Middle East Technical University, Ankara, Turkey), and J. Plötner (Museum für Naturkunde Berlin, Germany), unpublished data). If a notional average price of 5 € per kg is assumed, the sales values were about 2.5 and 2.4 million € in 2005 and 2009, respectively. On a regional scale, the trade in frogs and frog products is therefore an important economic factor; Turkish frog producers contribute about 5% to the annual import of frogs and frog products into the EU. Such extensive and unlimited catching activities will almost certainly result in a significant population decline (Baran et al., 1992), with unforeseeable ecological and economic consequences.

Uses List

General

• Pet/aquarium trade

Human food and beverage

• Meat/fat/offal/blood/bone (whole, cut, fresh, frozen, canned, cured, processed or smoked)

Diagnosis

A clear identification of allochthonous water frogs and hybrids between allochthonous and autochthonous forms requires molecular tools. A combination of mitochondrial and nuclear markers is the best diagnostic procedure, as mitichondrial DNA sequences do not distinguish between species and species hybrids -- they only provide evidence for a maternal genetic impact of an allochthonous species or lineage on a native population. Appropriate mitochondrial markers are, for example, the ND1 gene (Holsbeek et al. 2008), the ND2 and ND3 genes (e.g. Plötner and Ohst, 2001, Akin et al., 2010b), and the Cytb gene (Lymberakis et al., 2007). Nucleotide sequences of the nuclear serum albumin intron-1 (SAI-1) containing a 5’ truncated non-long terminal repeat retrotransposon (RanaCR1) allow a clear differentiation between pure lineages of Central European P. ridibundus and Anatolian P. cf. bedriagae (Plötner et al., 2009; J. Plötner (Museum für Naturkunde Berlin, Germany) and Ç. Akin (Middle East Technical University, Ankara, Turkey), unpublished data); introgressed individuals or hybrids cannot be identified in this way, but Holsbeek et al. (2008) could distinguish among both pure matrilines and intrigressed individuals using clustering approaches on the basis of microsatellite markers. As well as the aforementioned publications, Plötner et al. (2001, 2008) provide details on PCR and DNA sequencing.

Similarities to Other Species/Conditions

Single morphological characters or character combinations do not allow a clear differentiation between Anatolian P. cf. bedriagae and European P. ridibundus (e.g., Jdeidi, 2000); there is a great overlap in many morphometric parameters, and hybrids between the two forms may reduce the discriminative power of statistical methods because they show intermediate values in many morphometric characters. Multivariate approaches can be used to distinguish allochthonous from autochthonous forms; for example, based on discriminant analysis, Sinsch and Schneider (1999) were able to assign about 89% of individuals correctly to P. cf. bedriagae or P. ridibundus.

In the field, specialists may identify P. cf. bedriagae on the basis of their mating calls. Compared to Central European P. ridibundus, the number of pulse groups per call is greater and the pulses per pulse group are fewer in P. cf. bedriagae (Schneider and Sinsch, 1999; reviewed by Plötner, 2005). For an exact species diagnosis, however, direct comparisons of mating calls can be done only if the calls are recorded at the same water temperature, because many call parameters are temperature-dependent (e.g. Schneider and Sinsch, 2001).

Precise identification of allochthonous water frogs and their differentiation from autochthonous forms requires molecular markers. Besides specific enzymes (Beerli et al., 1996; Jdeidi, 2000; reviewed by Plötner and Ohst, 2001), a combination of mitochondrial and nuclear DNA sequences allows a clear differentiation between allochthonous and autochthonous water frogs and their hybrids (Ohst, 2008). Serum albumin intron 1 (SAI-1) and the embedded retroelement RanaCR1, for example, are specific markers that can be used to distinguish between the nuclear genomes of Anatolian P. cf. bedriagae, European P. ridibundus, and Balkan P. kurtmuelleri (Plötner et al., 2009).

Prevention and Control

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Prevention

There is no practical way to prevent the further expansion of allochthonous water frogs, among them P. cf. bedriagae, in western Europe. Eradication of non-native water frogs seems to be impossible. To prevent additional introductions of allochthonous water frogs, the international trade and sale of water frogs has to be prohibited by legislation. In small areas with known recent introductions water frogs could be tested genetically and allochthonous forms or hybrids between allochthonous and autochthonous lineages could be removed.

Control

The occurrence of lake frogs, considered as P. ridibundus, in areas where such forms were never detected before, is a first indication that allochthonous water frogs may be present. In such cases, frogs should be screened genetically and individuals with allochthonous genes should be removed from the population. A complete eradication of allochthonous water frogs seems possible only in small populations that live in clearly structured ecosystems and at a very early stage of invasion. If introgression of allochthonous genes into the indigenous gene pool has already occurred, the allochthonous form should be accepted as an established (naturalized) element of the ecosystem. Populations with allochthonous forms should be monitored to gain more insights into the population dynamics of the invader and to detect factors linked with its invasiveness. The general public has to be informed via mass media of the detrimental consequences that invasive water frog species may have for ecosystems and native water frog populations.

Gaps in Knowledge/Research Needs

There is still a big gap in the ecological and physiological data necessary to estimate the fitness (and thus the invasive potential) of P. cf. bedriagae outside its natural distribution area. Additional genetic data from natural populations are required to evaluate the extent of genetic pollution caused by P. cf. bedriagae lineages and other allochthonous forms.

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Distribution References

Akın Ç, Bilgin M, Bilgin C C, 2010. Discordance between ventral colour and mtDNA haplotype in the water frog Rana (ridibunda) caralitana Arikan, 1988. Amphibia-Reptilia. 31 (1), 9-20.

CABI, Undated. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI

Holsbeek G, Mergeay J, Hotz H, Plötner J, Volckaert F A M, Meester L de, 2008. A cryptic invasion within an invasion and widespread introgression in the European water frog complex: consequences of uncontrolled commercial trade and weak international legislation. Molecular Ecology. 17 (23), 5023-5035. http://www.blackwell-synergy.com/loi/mec DOI:10.1111/j.1365-294X.2008.03984.x

Ohst T, 2008. Genetic influence of allochthonous water frogs on the endemic water frog population (R. kl. esculenta complex). (Genetische Einflüsse allochthoner Wasserfrösche auf endemische Wasserfroschpopulationen (R. kl. esculenta Komplex).). Berlin, Germany: Humboldt-Universität zu Berlin.

Pagano A, Dubois A, Lesbarrères D, Lodé T, 2003. Frog alien species: a way for genetic invasion. Comptes Rendus Biologies. 85-92.

Plötner J, 2005. Die westpaläarktischen Wasserfrösche. Von Märtyrern der Wissenschaft zur biologischen Sensation. Bielefeld, Germany: Larenti Verlag. 160 pp.

Plötner P, Uzzell T, Beerli P, Akın Ç, Bilgin C C, Haefeli C, Ohst T, Köhler F, Schreiber R, Guex G D, Litvinchuk S N, Westaway R, Reyer H U, Pruvist N, Hotz H, 2010. Genetic divergence and evolution of reproductive isolation in eastern Mediterranean water frogs. In: Evolution in action. Case studies in adaptive radiation and the origin of biodiversity. [ed. by Glaubrecht M]. Germany: Springer. 373-403.

Proess R, 2003. Distribution atlas of the Amphibia of Luxenbourg. More literatur on the Amphibia of Luxembourg. (Verbreitungsatlas der Amphibien des Groβherzogtums Luxemburg. Weitere in der Literatur für Luxemburg erwähnte Amphibienarten.). Ferrantia. 72-74.

Links to Websites

Organizations

Europe: SEH (Societas Europaea Herpetologica), Museum Natural History and Territory, University of Pisa, via Roma 79, 56011 Calci (Pisa), Italy, http://www.seh-herpetology.org/

Germany: DGHT (Deutsche Gesellschaft für Herpetologie u. Terrarienkunde), Postfach 14 21, 53351 Rheinbach, http://www.dght.de/

Switzerland: KARCH (Koordinationsstelle für Amphibien- und Reptilienschutz in der Schweiz), Passage Maximilien-de-Meuron 6, 2000 Neuchâtel, http://www.karch.ch

Contributors

03/11/09 Original text by:

Jörg Plötner, Museum für Naturkunde Berlin, Leibniz-Institut für, Evolutions- und Biodiversitätsforschung, an der Humboldt-Universität zu Berlin, Invalidenstrasse 43, D-10115 Berlin, Germany

Distribution Maps