ACTA ZOOLOGICA BULGARICA Acta zool. bulg., Suppl. 7, 2014: 51-56
Diet Composition of the Dice Snake (Natrix tessellata Laurenti, 1768) (Reptilia: Colubridae) in the Danube River Catchment Area
András Weiperth, Imre Potyó, Miklós Puky
MTA Centre for Ecological Research, Danube Research Institute, H-2131 Göd, Jávorka Sándor u. 14., Hungary; Email: puky. [email protected]
Abstract: Natrix tessellata (Laurenti, 1768) is a diurnal piscivorous Eurasian snake species with a large distribu- tion area. The Danube River is a main aquatic corridor and its floodplain is an important habitat for this species. Natrix tessellata lives in countries all along the river, owing to its good adaptability to different climate, altitude and even human activities, enabling it to live in human-dominated landscape as well. The aim of this paper is to give an overview on the feeding spectrum of N. tessellata in countries along the Danube River and to compare its feeding preferences in the different stretches of the river. The detailed analysis of the diet of N. tessellata is based on species level data from ten countries from the Danube River Basin (Austria, Bulgaria, Croatia, Czech Republic, Slovakia, Hungary, Romania, Serbia, Slovenia and Ukraine). On the basis of our own data and the special literature, we found that N. tessellata fed on 38 fish and six amphibian taxa in the region. The feeding spectrum changed characteristically along the Danube River with differences among the Lower Danubian (e.g. Bulgaria, Romania), Middle Danubian (e.g. Hungary) and Upper Danubian (e.g. Austria) countries.
Keywords: Natrix tessellata, Reptilia, feeding spectrum
Introduction Natrix tessellata is a Eurasian snake species strongly measures should still be undertaken for this species. bound to aquatic habitats (Ga s c et al. 1997). It in- Habitat destruction, pollution, road traffic, collection habits different water types along the Danube River, and persecution are listed as possible threats (e.g. such as different floodplain sections, tributaries and Ka m m e l , Me b e r t 2011). standing water bodies (Ga e b e l e et al. 2013). It is The dice snake has a large distribution and it listed in Annex II of the Bern Convention (1999) and occurs in different habitats, which would imply the it appears also in Annex IV of the Habitat Directive species can adapt well to local conditions, presum- of the European Union (92/43/ECC) but owing to ably by adopting a wide feeding spectrum. However, its wide distribution and presumably large popula- it is generally considered to be a diurnal piscivorous tion size, it is categorised as least concern by IUCN snake (Ga s c et al. 1997) despite the available infor- (2012). However, it is considered to be threatened mation showing that it also eats non-fish prey items in a number of Western and Central European (e.g. Be s h k o v , Du s h k o v 1981). states with low genetic variation in some popula- Natrix tessellata was found to live along the tions (Ga u t s c h i et al. 2002, Gu i c k i n g et al. 2004), Danube River and the connected habitats at sev- in addition its world population has been assessed eral stretches, and its diet was also investigated at as declining (IUCN 2012). As such, conservation several sites there. Due to its excellent swimming
51 Weiperth A., I. Potyó, M. Puky and diving abilities and association to freshwater Results and Discussion habitats, N. tessellata is generally considered to Species, and in some cases genus, level data on the be a strictly piscivorous fish species (La ň k a 1978, feeding spectrum of the dice snake were collected Kr e i n e r 2007), however, no comparative study has from ten countries in the Danube River catchment been conducted so far. In this paper we present the area. Altogether 44 animal taxa have been listed as first overview of the feeding spectrum of N. tessel- prey for the dice snake belonging to two classes: lata in the countries from the Danube River Basin Pisces and Amphibia. The ratio of classes among the and analyse the geographical differences among taxa is 14% Amphibia and 86% Pisces (Table 1). them. The highest number of prey taxa eaten was found in studies conducted in Hungary (19), Austria Material and Methods (15) and Serbia (13), while the lowest were from Information was gathered on the diet of the dice Croatia and Slovenia (six for both countries). Fish snake from its whole Danubian range. The coun- were recorded in the diet of the N. tessallata in all tries from the Danube River Basin with information countries in the Danube River catchment area (Fig. only from populations outside the Danube catch- 1.) and they comprised the highest number of taxa ment, i.e. the small German populations from the eaten in each of them. In spite of the high ratio Nahe River and Lahn River, as well as the Swiss of fishes among prey items, in 50% of the coun- populations from Geneva Lake were not included tries (Bulgaria, Czech Republic, Romania, Serbia, in the analysis. Information from papers only men- Slovenia) amphibians were also detected as prey of tioning large, collective groups such as „insects”, the dice snake. „fish” or „frogs” as food items, without giving spe- The detailed analysis of the diet of N. tessel- cies (or at least genus) level information, may be lata, based on species level data from ten count- discussed in the article but has not been included ries (Austria, Bulgaria, Croatia, Czech Republic, in the database, even if their addition would have Slovakia, Hungary, Romania, Serbia, Slovenia, added new items to the list such as insect, mice or Ukraine), proved that N. tessellata feeds on at least shrews (Ra d o v a n o v i c 1951, 1964). No time limit 44 prey taxa from two classes in the Danube River was applied and available reports from the first catchment (Table 1.). Earlier evaluations generally half of 20th century were used as well. Besides considered N. tessellata as a strictly piscivorous published records and our own observations, citi- snake species (Kr e i n e r 2007, La ň k a 1978), regard- zen science data were also collected by approach- less of the fact that it had been described to hunt ing international and national internet databases even in terrestrial habitats at night (Gr u s c h w i t z et for photographic evidence of dice snake predation al. 1999, La ň k a 1978). A key factor determining the on a given taxa (e.g. www.varangy.hu, www.her- actual species composition in the diet of N. tessel- petozoa.at, www.shdmr.org). Prey species were lata is that it remains in the immediate vicinity of determined according to Ar n o l d , Ov e n d e n (2002), surface waters at a distance of less than 20 metres to Ha r k a , Sa l l a i (2004), Ko t t e l a t , Fr e y h o f (2007), the water edge under normal conditions during the Pi n t é r (2002) and a public fish database in the in- active season (Ne u m a n n , Me b e r t 2011, Ve l e n s k y ternet (www.fishbase.us). et al. 2011). As a result, it predominantly feeds on Association analysis with the presence-absence aquatic and/or water-bound animals, with fish being data of the prey taxa of the dice snake was used in the most important prey organisms. non-metric cluster analysis (Go o d a ll 1953, Po d a n i There is a clear relationship between fish spe- 1997, 2001, Wi ll i a m s , La m b e r t 1960) to elucidate cies preyed upon and the size of the water bodies. zoogeographical differences among ten Danube In the main arm of the Danube River the dice snake River catchment countries, from where appropriate mostly eats benthic fish (Neogobius sp., Ponticola information could be collected. Statistical analysis sp.) and/or fish species hidden in aquatic vegetation was made using SYN-TAX 2000 (Po d a n i 2001). stands (Cyprinidae sp., Alburnus alburnus, juvenile Results were plotted using MS Office 2010 and Chondrostoma nasus and Leuciscus idus) (Ga e b e l e SYN-TAX 2000 (Po d a n i 2001). et al. 2013). Along tributaries, streams, densely ve-
52 Diet Composition of the Dice Snake (Natrix tessellata Laurenti, 1768) in the Danube River Catchment Area
Table 1. Prey spectrum of the dice snake (Natrix tessellata) in the Danube River catchment area. Country codes: AUT: Austria, BUL: Bulgaria, CRO: Croatia, CZE: Czech Republic, HUN: Hungary, ROU: Romania, SLO: Slovenia, SRB: Serbia, SVK: Slova- kia, UKR: Ukraine
Countries Classes Species/ Genus AUT CZE SVK HUN SLO CRO SRB ROU BUL UKR Alburnoides bipunctatus + Alburnus albidus + Alburnus alburnus + + + + + + + + + + Barbatula barbatula + Barbus barbus + Carassius auratus + + Carassius gibelio + + Chondrostoma nasus + + Cobitis taenia + + Cottus gobio + + Cyprinus carpio + Esox lucius + Gambusia affinis + + + Gobio gobio + + + Gymnocephalus schraetser + Knipowitschia caucasica + + + Knipowitschia sp. + + + + Lepomis gibbosus + + Leuciscus idus + + Pisces Leuciscus leuciscus + Leuciscus sp. + Neogobius fluviatilis + + + + + Neogobius melanostomus + + + + + Neogobius ratan + Neogobius sp. + + + + + Oncorhynchus mykiss + Perca fluviatilis + + + Ponticola eurycephalus + Ponticola kessleri + + + Ponticola syrman + Pseudorasbora parva + + + + + Rhodeus sericeus + + Rutilus rutilus + + + + + + + + Salmo trutta + + Sander volgensis + Scardinius erythrophthalmus + + + + Squalius cephalus + + + + + + + Thymallus thymallus + Bombina variegata + Pelophylax kl. esculentus + Pelophylax ridibundus + + + (tadpoles and juveniles) Amphibia Pseudepidalea viridis/variabilis + (tadpoles and juveniles) Rana sp. (tadpoles) + + Rana temporaria + +
53 Weiperth A., I. Potyó, M. Puky
A B
Fig. 1. Rare (A: Gymnocephalus schraetser) and common (B: Neogobius melanostomus) prey species of the dice snake along the Middle Danube River (Hungary). Larger fish or those that are difficult to handle, are carried on land and swallowed after the prey becomes weak due to oxygen shortage. (Photo: A: Ádám Selmeczi Kovács, B: Gábor Tirpák)
Fig. 2. Similarity of the feeding spectrum of the dice snake (N. tessellata) in ten countries in the Danube River catchment area. Country codes: AUT: Austria, BUL: Bulgaria, CRO: Croatia, CZE: Czech Republic, HUN: Hungary, ROU: Romania, SLO: Slove- nia, SRB: Serbia, SVK: Slovakia, UKR: Ukraine getated water courses, lakes and ponds, dice snake Other prey items were also present occasionally, hunts fish (mainlyCyprinidae sp., Gambusia affinis, which indicated the good adaptability of the species Lepomis gibbosus and Perca fluviatilis), as well as to different conditions. amphibian larvae and adults (mainly Pelophylax The feeding spectrum of the dice snake differs and Rana sp.) near the bank (Ga e b e l e et al. 2013, among different regions in the Danubian catchment. Sl o b o d a et al. 2010, Vl č e k et al. 2010, Zi m m e r m a n , The analysis of the results revealed three main groups Fa c h b a c h 1996). With decreasing water body size, (Fig. 2.). The first group in the cluster includes the the feeding spectrum of the dice snake changes Lower Danubian countries with the highest number considerably to include terrestrial species, besides of Ponto-Caspian gobiid species (e.g. Neogobius fish and amphibians (Ža g a r et al. 2011). Populations sp., Knipowitschia sp. and Ponticola sp.), common in high mountains (over 1000 m a.s.l.) may speciali- Cyprinidae species (Alburnus alburnus, Rutilus ru- se on eating larval and adult amphibians as predomi- tilus) and two non-native species (Lepomis gibbosus nant food (Ca f u t a , Kr o f e l 2007, Ža g a r et al. 2011). and Pseudorasbora parva). Amphibian predation
54 Diet Composition of the Dice Snake (Natrix tessellata Laurenti, 1768) in the Danube River Catchment Area was also recorded in all countries of the Ukrainian The Austrian – Slovenian – Croatian – Czech – Bulgarian – Romanian branch (Table 1) (Be s h k o v , branch includes countries with limited amphibi- Du s h k o v 1981, Ca r l s s o n et al. 2011, Ka r v e m o et an consumption (Ca f u t a , Kr o f e l 2007, Hu t i n e c , al. 2011, Ne k r a s o v a et al. 2013, Sc h ü l t e r 2006, Me b e r t 2011, Mu s i l o v á , Za v a d i l 2011, Re h a k 1992, Sl o b o d a et al. 2010, Ve l i k o v 2011). During extreme- Šv a b 2003, Vl č e k et al. 2010, Ža g a r et al. 2011) ly hot summers the dice snake was also observed to and (for Austria, Croatia, Slovenia) characteristic hunt at night in this area, as well as far away from local mountain fish species (Hu t i n e c , Me b e r t 2011, surface waters, which furthers the potential feeding Ža g a r et al. 2011, Zi m m e r m a n , Fa c h b a c h 1996) in spectrum of this snake (see e.g. Mö l l e r 1990, who the diet of the dice snake. Countries in which the observed over a period of several weeks a large dice dice snake also feeds on amphibians are on a sepa- snake which “unusually” hunted geckos at night in a rate sub-branch (Table 1). man-made environment). The analysis of the diet of the dice snake in the Countries from the Middle Danubian River Danube River catchment proved that the population Basin, except for Croatia, formed the next group of the snake in the Danube River Basin has got a (Serbia – Hungary – Slovakia). There were sev- diverse feeding spectrum. It feeds primarily on fish, eral fish with very large distribution areas among while amphibian larvae, juveniles and adults are of the prey species there, such as Alburnus alburnus, secondary importance at the catchment level. Some Leuciscus idus, Pseudorasbora parva, Rhodeus data also indicate occasional predation on reptiles sericeus, Rutilus rutilus, Squalius cephalus (Ga e b e l e and mammals. The large number of taxa in the diet et al. 2013, own data), (Table 1). Amphibian pre- indicates a good adaptability to different potential dation for the group is known only from a photo- prey species (Gh i r a et al. 2009) and the flexibility of graphic evidence from Serbia, while Ra d o v a n o v i ć the dice snake to reaching the appropriate resources (1951, 1964) also reported amphibian and small (Re s h e t n i k o v et al. 2013) also by switching its fo- mammal predation from the former Yugoslavia raging strategy from ambush to active search or back but without giving species-specific information. along the whole Danubian catchment.
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