Analele Științifice ale Universității Al. I. Cuza Iași, s. Biologie animală, Tom LVII, 2011 THE POTENTIAL RELATIONSHIPS BETWEEN PREDATORS AND MOLDAVIAN MEADOW VIPERS (VIPERA URSINII MOLDAVICA) IN EASTERN ROMANIA Constantin ION, Ștefan R. ZAMFIRESCU and Alexandru STRUGARIU Faculty of Biology, Alexandru Ioan Cuza University of Iași, 11 Carol I Bvd., No. 20A, 700505, Iași, Romania, costin_zoo@yahoo.com Abstract. The Moldavian Meadow Viper is a species, which eats mainly insects and lives in the steppe vegetation at low heights, where there are also predators that can hunt it or that are rivals for the food resources. In the period 2009-2011, we took an account of the presence of predators in the habitats with meadow viper populations. The day predators have a small influence on the meadow viper populations. We take into consideration the fact that the pheasants and storks among birds and wild boars among mammals also represent the main predators of the Moldavian Meadow Viper. The balance between the population of predators and the population of Moldavian Meadow Vipers can be kept only if the human impact does not lead to a division into fragments of the habitats and implicitly a superposition of food and space necessities for birds and snakes. Keywords: predators, Moldavian Meadow Viper Rezumat. Potențialele legături dintre prădători și vipera de stepă (Vipera ursinii moldavica) în estul României. Vipera de stepă este o specie preponderent insectivoră și trăiește în vegetația de stepă de la joase altitudini, unde apar în mod frecvent și prădători, care fie pot vâna exemplare de vipere sau cu care intră în concurență pentru resursele de hrană. În perioada 2009-2011 am inventariat prezența prădătorilor în habitatele în care există populații ale viperei de stepă. Răpitoarele de zi au o influentă scăzută asupra populațiilor de viperă. Considerăm că principalii prădători ai viperei de stepă sunt reprezentați de fazan, barză, dintre pasări și porcul mistreț, dintre mamifere. Starea de echilibru populațional între prădători și vipera de stepa poate fi menținută, numai daca impactul uman nu duce la o fragmentare a habitatelor și implicit la o suprapunere a necesităților de hrana și spațiu pentru păsări și vipere. Cuvinte cheie: prădatori, Vipera ursini moldavica Introduction The meadow viper (Vipera ursinii, Bonaparte, 1835) is a small-sized, mildly venomous snake which has a wide but fragmented range in Europe, covering parts of France, Italy, Hungary, Romania and the Balkan Peninsula while being considered extinct from Austria, Bulgaria and the Republic of Moldova (Nilson & Andren 2001, Edgar & Bird, 2006). The Moldavian Meadow Viper (Vipera ursinii moldavica, Nilson, Andren et Joger, 1993) has a limited range in Europe, its presence being confirmed only in Eastern Romania, in the following locations: Dealul lui Dumnezeu, Valea lui David, in the western part of Iasi County (Zamfirescu et al., 2007) and in the areas Cardon, Sfântu Gheorghe and Perișor from the Danube Delta (Krecsák & Zamfirescu, 2008). The subspecies prefers low-altitude grasslands like steppes (Zamfirescu et al., 2008) and westpontic salt meadows (Strugariu et al., 2011). V. ursinii is considered by some authors as the most threatened European snake species (e.g. Edgar & Bird 2006). The species is labelled as vulnerable in the IUCN Red List, included in Annex II of the European Habitat Directive and listed in CITES Appendix I. The Eastern Romanian subspecies (Vipera ursinii moldavica) is labelled as critically endangered in the IUCN Red List and in the Romanian Red Data Book of Vertebrates (Iftime 2005). The Moldavian Meadow Viper (Vipera ursinii moldavica) eats mainly insects (Fuhn & Vancea, 1961), but other populations of V. ursinii also forage for lizards and - 35 -
Constantin Ion et al. even nestling birds (Agrimi & Luiselli, 1992). On the other hand, birds of prey can eat vipers but accidentally (Convention on the conservation of European wildlife and natural habitats, 2006). The Moldavian meadow viper usually hibernates from October to March and mating usually takes place in April or May (Zamfirescu et al., in preparation). Offsprings of the Moldavian meadow vipers, counting from 1 to 10 are born in August- September-October and the frequency of reproduction is annual or less than annual (Strugariu et al., in preparation). The relationships established between the viper populations and the bird populations are based on the existence of large populations of insects (carbide, grasshoppers, locusts). Although both reptiles and birds eat insects, the competition for the ecological resources does not take place in a striking manner, the ecological relationship between them being frequently accidental (Convention on the conservation of European wildlife and natural habitats, 2006). The meadow viper has many natural enemies including birds of prey, mustelids, wild cats, and other snake species. For instance, an over-population of wild boar has caused significant damage to the viper habitats in Hungary and Italy (Péchy et al., 1996; Filippi & Luiselli, 2003), and the wild boars prey on snakes. Intensive rearing and release of pheasants for shooting may also be a problem. Pheasants can consume young snakes and they are a major threat for the species in the Danube Delta (Convention on the conservation of European wildlife and natural habitats, 2006). The intensive rearing and the release into the wild of artificially high numbers of pheasants (Phasianus colchicus) for shooting purposes have become more common in many parts of Europe. Pheasants have been recorded eating small reptiles in a number of countries and could consume young meadow vipers easily. The increasing numbers of this species are considered a threat for the Moldavian meadow vipers in the Danube Delta Biosphere Reserve (Fuhn 1976; Török, 2002). During a three years programme we estimated the ecological relationships that can be established between predators and the Moldavian Meadow Viper, in the East of Romania. The evaluation of the predators presence in the areas with Moldavian Meadow Vipers was realised with the purpose of establishing the degree of conserving the populations of birds and reptiles. Materials and methods During the period 2009-2011, we had a programme to estimate the presence of the potential predators in the areas with meadow vipers from the East of Romania. We investigated the following areas: Valea lui David and Dealul lui Dumnezeu, situated at 8 km distance of Iasi and the area of Sfântu Gheorghe (Danube Delta). The avifauna was observed through the transect method and the observation from a fixed point with binoculars of 8x40, and a fieldscope 20x60. We followed the qualitative and quantitative analysis of the bird species, but also the interactions established with the viper populations. During the monitoring programme, ecological observations were made, concerning the presence of the Moldavian Meadow Viper, but also the potential predators mentioned in literature (Meadow viper, Vipera ursinii factsheet EU Wildlife and Sustainable Farming project, 2009). We observed the birds general state of conservation, but also the way in which they use the same food resources and the same areas as the Moldavian Meadow Viper. In Important Habitat Areas - Natura 2000 sites: Valea lui David and Dealul lui Dumnezeu we estimated a general image concerning avifauna, as the dates can be used for the subsequent measures of area management. For the area Sfântu Gheorghe (Danube Delta) we focused only on the potential predators of the meadow viper or over the ones which can compete with the viper for food, also adding some quantitative - 36 -
Analele Științifice ale Universității Al. I. Cuza Iași, s. Biologie animală, Tom LVII, 2011 data about avifauna, useful in estimating the diversity in the area, but also about the protection measures against some invasive predators like the Pheasant (Phasianus colchicus). Results and Discussion In the Natura 2000 sites: Valea lui David and Dealul lui Dumnezeu (Iasi County) 82 bird species were identified included in 12 taxonomic orders. The birds we identified, find in these areas excellent feeding, nesting or passage places. The existing hills favour the development of xerophilous vegetation hosting plenty of food (fruits, insects) for birds. At the same time, the configuration of the field favours the development of some ascending thermal currents, making easy the flight of the big birds (the diurnal birds of prey) during the passage. Although we did not observe cases in which vipers were caught in these areas by other animals, the birds of prey use the meadows as a feeding place and we do not exclude the possibility of killing and eating young Moldavian meadow vipers. Many of the bird species use the same food resources, hunting big insects, but also small mammals. The birds we identified (Table 1) prefer open places but also the ponds around the reservations. Beside the birds of prey observed (17 species), most species are passerines (41 species). The birds use the areas especially as feeding places and no direct interactions with the meadow viper populations have been observed. The human impact is stronger in the scientific reservation Valea lui David and this produces lacks of balance in the existent habitats, and implicitly represents a possible danger for the viper populations and for the existence of food resources. The extension of the surrounding constructions, the presence of domestic animals in the area put more and more pressure on the habitats used by vipers and birds. At the same time, there is an obvious growth of the pheasant populations in the peripheral areas (7-8 brooding pairs), their diet often including snakes (Cramp, 1977). Most species, except most of the passerines, are rarely met in the studied areas. A higher abundance and a higher species frequency can be noticed during the passage and in winter. Birds find here large numbers of big insects during migration, but also many rodent populations constituting an important food source even in the winter period. We consider that, for the viper populations, the greatest threat is the Pheasant, a species introduced in Romania (Linția, 1955), in numerical expansion in the area. The Magpie (Pica pica), the Hooded Crow (Corvus cornix), but also the Rook (Corvus frugilegus) are potential predators for the viper populations, as it is known that these species are opportunist (Cramp & Perrins, 1994). In the areas Sfântu Gheorghe and Perișor-Periteașca, where the Moldavian meadow viper was studied (e.g. Strugariu et al., 2011), as a result of the faunistic research, we also saw vertebrate species, which represent potential predators. The most numerous group is represented by birds which can be grouped in: birds of prey, in whose diet can be included the Moldavian meadow viper; the Stork; the Pheasant; and species of Crow Family, which represent potential predators of Moldavian meadow vipers as is mentioned in Convention on the conservation of European wildlife and natural habitats, 2006. Among the birds of prey observed in the area, which can constitute competitors for the ecological resource of the Moldavian meadow viper and whose presence was confirmed in literature (International ringing Camp in Romania, 2007), there are: Circaetus gallicus (Short-toed Snake Eagle), which is rarely present during migration in the Sfântu Gheorghe area. Its presence could cause a diminution of the meadow populations, considering the fact that its food is constituted mainly of snakes (Gil & Pleguezuelos, 2001). The food necessary for this species is of 1-2 snakes per day (Cramp, 1980). The impact of this species on the viper population is reduced, being - 37 -
Constantin Ion et al. known that this species avoids small snakes (Bakaloudis & Vlachos, 2011), including the meadow vipers. The species was observed in small numbers, especially in migration, during autumn. Aquila pennata (Booted Eagle) was very rarely observed in the habitats with meadow viper. It eats especially big lizards, small birds and mammals (Veiga, 1986), presented in the same biotopes as the meadow viper. As additional food, it consumes insects in great quantity (Cramp, 1980), without being observed to eat snakes. Buteo rufinus (Long-legged Buzzard) is present especially in the autumn migration, when it hunts on the meadows in the north of Sfântu Gheorghe, where a large population of meadow viper can be found. Its diet sometimes includes vipers (Cramp, 1980), but also big insects (sometimes up to 25% of the food). The number of observed individuals is small, and thus, it probably does not have negative effects on the viper populations. Taking into account the fact that this species has been in a real numerical expansion in the last years (personal observations) and that it can consume a lot of food, we do not exclude its presence in a greater number in the habitats with meadow viper. Buteo buteo (Common Buzzard) is a constant presence both in the reproduction period and in the migration period. Large populations were identified especially around Sfântu Gheorghe, both in the reproduction period and in the passage one. In the area Sfântu Gheorghe at least two pairs of Common Buzzard nestle. Sometimes they consume vipers (Cramp, 1980), but also insects, in small quantities. They hunt especially locusts, grasshoppers (Orthoptera), beetles (Coleoptera), moth caterpillars (Lepidoptera), cockchafer (Melolontha melolontha), but also earthworms (Lumbricidae). Next to the already-mentioned species, present in large numbers, during migration it also appears the northern subspecies vulpinus. The subspecies buteo also eats snakes, especially when the rodent populations are smaller, in the periods with a lot of water, as in 2010. The subspecies vulpinus eats reptiles, but especially in the breeding period or the one in which the broods grow, but it is not the case in the area Sfântu Gheorghe Perișor-Periteașca, here being present only in the migration period. Pernis apivorus (Honey Buzzard), although can consume reptiles, including vipers, does not represent a danger for the viper populations, as the main food for this species is represented by wasps, hornets, bumble-bees, ground-insects (especially beetles) and small vertebrates, which can be found in abundance in these areas. In the beginning of the reproduction period, it can also consume earthly insects or reptiles. There were no observed cases in which the honey buzzard hunted vipers, but only snakes such as Natrix spp. (Cramp, 1980), often smaller than 40 cm. The Honey Buzzard was observed in the area only in the migration period, being rarely nestling in the Danube Delta (Munteanu et al., 2002). Of course that between the meadow viper and all the birds of prey that can also consume insects (eagles, falcons) can be established competing relationships for food. The Goshawks, Sparrowhawks and especially the Marsh Harrier (Circus aeruginosus), which breeds in the area (2-3 breeding pairs) hunts large numbers of insects as additional food (Cramp, 1980). During migration, other species of birds of prey were observed in the area: Hen Harrier (Cyrcus cyaneus), Montagu s Harrier (Circus pygargus) and more rarely Pallid Harrier (Circus macrourus), insects being very rarely included in their diet. Also during migration, but especially in the autumn one, the Black Kite (Milvus migrans) was observed; it can also consume insects, especially beetles (Cramp, 1980). Also present in the area, especially during the summer are Kestrels (Falco tinnunculus), 2-3 breeding pairs, Red-footed Falcons (Falco vespertinus), 2-4 breeding pairs and Hobby (Falco subbuteo), 1-2 breeding pairs. All these species use the area with meadow vipers as a hunting area, consuming also insects, especially in the case of the Red-footed Falcon. - 38 -
Analele Științifice ale Universității Al. I. Cuza Iași, s. Biologie animală, Tom LVII, 2011 The Pheasant (Phasianus colchicus) represents a threat for the populations of vipers, especially for the ones of young snakes, during spring, when the species needs more food, as they have to feed their broods (Cramp, 1977). In the north of Sfântu Gheorghe, we estimated a population of 10-15 breeding pairs, which use the meadows where the meadow vipers live, as feeding areas. Animal food consists mainly of small arthropods, larvae, beetles (Coleoptera), grasshoppers (Orthoptera), bugs (Heteroptera), flies (Diptera), spiders (Arachnida) and millipedes (Myriapoda) (Cramp, 1977). Taking into account the fact that the pheasant is a species invasively introduced for the Danube Delta (Linția, 1955, p. 459), it represents a great danger for the existence of the Moldavian Meadow Viper populations and can lead to, if its density grows, a serious lack of balance. The White Stork (Ciconia ciconia) is constantly present in the investigated areas both in the reproduction period and especially in the migration period. During the breeding period, the White Stork uses meadows to look for food. Near the village, there are four White Stork nests on the way, which connects Sfântu Gheorghe to Sulina. We often observed the species consuming larvae and insects, especially Coleoptera (beetles) and Orthoptera (grasshoppers, crickets and locusts), frogs, snakes and small mammals. We frequently saw in the Danube Delta, White Storks eating snakes (Natrix spp.). Snakes constitute one of the main sources of food (del Hoyo et al., 1992), especially because in the Danube Delta their abundance is great (Török, 2002). We also saw two cases in the northern area of the village Sfantu Gheorghe, where the White Stork ate small Meadow Vipers. We must pay special attention to the corvids (Jackdaw Corvus monedula, Rook Corvus frugilegus, Hooded Crow Corvus cornix, Raven Corvus corax) which often rummage for food near the galleries with vipers. The Hooded Crow and Raven populations are numerous. Near the garbage hollows and on the meadows where the Moldavian Meadow Viper can be found, dozens of Hooded Crows appear, looking for food. Also, in the breeding period, four breeding pairs of Raven were observed in the area we investigated. They can attack especially juveniles of vipers, being known the fact that they can eat snakes (Cramp & Perrins, 1994). Also among corvids, we have to mention the presence in a large number of the Magpie (Pica pica), known as possible consumer of vipers (Cramp & Perrins, 1994), among different food resources. The Red-backed Shrike (Lanius colurio) can eat snakes (Cramp & Perrins, 1994). In the investigated area the species is represented by a breeding population of 4-6 breeding pairs and was observed attacking near the galleries where the vipers shelter, probably catching juveniles. In general, shrikes (Lanius spp.) could eat juvenile vipers but probably only consume small numbers (Cramp & Perrins, 1994). The Wild Boar (Sus scrofa) can consume a big numbers of meadow vipers (Péchy et al., 1996; Filippi & Luiselli, 2003). In the research area, we rarely observed wild boars but numerous footmarks are present especially in the forest near the northern area of the village of Sfântu Gheorghe, where there is an important population of Moldavian Meadow Viper. According to the natives accounts and Doroșencu, in verbis, wild boars especially eat young vipers in large numbers. Although vipers, through certain morphological and chromatic characteristics might deter various potential avian predators to a certain degree (e.g. Wüster et al., 2004; Niskanen & Mappes, 2005; Valkonen et al., 2011; Strugariu & Zamfirescu, 2011), they are still probably highly vulnerable in front of large terrestrial predators such as the wild boar. Anthropic activities, either legal or illegal and especially through overgrazing or the extension of the industrial facilities contribute to a fragmentation of the habitats in the studied areas and to a greater competition for food resources, but also to a lack of potential refuges for the vipers, which make the viper populations more vulnerable in front of their potential predators. - 39 -
Constantin Ion et al. Tabel 1. Bird species present in Valea lui David and Dealul Dumnezeu. No. Species 1. Podiceps cristatus 2. Ciconia ciconia 3. Anas plathyrhyncos 4. Aquilla pomarina 5. Aquila pennata 6. Buteo buteo 7. Buteo lagopus 8. Circus cyaneus 9. Accipiter gentilis 10. Accipiter nissus 11. Milvus migrans 12. Pandion haliaetus 13. Circus aeruginosus 14. Circus cyaneus 15. Circus pygargus 16. Circus macrouros 17. Falco peregrinus 18. Falco subbuteo 19. Falco verspetinus 20. Falco tinnunculus 21. Perdix perdix 22. Phasianus colchicus 23. Coturnix coturnix 24. Crex crex 25. Gallinula chloropus 26. Fulica atra 27. Vanellus vanellus 28. Scolopax rusticola 29. Larus cachinnans 30. Chroicocephalus ridibundus 31. Chlidonias hybridus 32. Columba livia domestica 33. Streptopelia turtur 34. Streptopelia decaocto 35. Cuculus canorus 36. Athene noctua 37. Asio otus 38. Asio flammeus 39. Apus apus 40. Merops apiaster 41. Upupa epops No. Species 42. Galerida cristata 43. Alauda arvensis 44. Delichon urbica 45. Hirundo rustica 46. Anthus campestris 47. Motacilla flava 48. Motacilla alba 49. Lanius collurio 50. Lanius minor 51. Oriolus oriolus 52. Sturnus vulgaris 53. Garrulus glandarius 54. Pica pica 55. Corvus frugilegus 56. Corvus cornix 57. Corvus corax 58. Acrocephalus scipaceus 59. Acrocephalus arundinaceus 60. Sylvia borin 61. Sylvia communis 62. Sylvia curruca 63. Muscicapa striata 64. Oenanthe oenanthe 65. Saxicola rubetra 66. Saxicola torquata 67. Erithacus rubecula 68. Turdus merula 69. Turdus philomelos 70. Turdus pilaris 71. Turdus viscivorus 72. Parus major 73. Cyanistes caeruleus 74. Passer domesticus 75. Passer montanus 76. Fringilla coelebs 77. Carduelis chloris 78. Carduelis carduelis 79. Carduelis cannabina 80. Miliaria calandra 81. Emberiza schoeniculus 82. Emberiza citrinella - 40 -
Analele Științifice ale Universității Al. I. Cuza Iași, s. Biologie animală, Tom LVII, 2011 Conclusions We consider that the main predators of the meadow viper are the Pheasant, the Stork between birds and the Wild boar between mammals. The diurnal birds of prey probably have a small influence on the viper populations. The balance in number between predators and the meadow viper can be maintained only if the human impact does not lead to a division of the habitats and implicitly to a superposition of food necessities and space for birds and vipers. Acknowledgements: This research was financed through CNCSIS UEFISCSU, Project PNII IDEI 2098 No.1041/2009. We want to thank Mr. Alexandru Doroșencu for his valuable help in writing this work. References Agrimi, U., Luiselli, L., 1992. Feeding strategies of the viper Vipera ursinii ursinii (Reptilia, Viperidae) in the Apennines. Herpetol. J., 2: 37-42. Bakaloudis, D., E., Vlachos, C., G., 2011. Feeding habits and provisioning rate of breeding short-toed eagles Circaetus gallicus in northeastern Greece. Journal of Biological Research-Thessaloniki, 16: 166 176. Cramp, S., 1977. Handbook of the birds of Europe, the Middle East and North Africa: the birds of the Western Palaearctic. Stanley Cramp, chief editor. Oxford University Press, Oxford, New York. Cramp, S., 1980. Handbook of the birds of Europe, the Middle East and North Africa : the birds of the Western Palearctic. Stanley Cramp, chief editor. Oxford University Press, Oxford, New York Cramp, S., Perrins, C., M., 1994. Handbook of the Birds of Europe the Middle East and North Africa. The Birds of the Western Palearctic (ed. C.M. Perrins). vol. 8, Oxford University Press, Oxford, New York, p. 54 75. Del Hoyo, J., Elliott, A., Sargatal, J. (Eds.), 1992. Handbook of the Birds of the World, vol. 1. Lynx Edicions, Barcelona. Edgar, P., Bird, D.R., 2006. Action plan for the Conservation of the Meadow viper (Vipra ursinii) in Europe. Convention on the Conservation of European Wildlife and Natural Habitats Standing Committee, 26 th meeting, Strasbourg, 27-29 November, T-PVS/Inf (2006) 21. Filippi, E., Luiselli, L., 2003. Aspects of the ecology and conservation of the meadow viper Vipera ursinii in the Duchessa Mountains Natural Park (Latium, Central Italy). Herp. Bull., 86: 5-9. Fuhn, I.. E., Vancea, T., 1961. Fauna RPR. Reptilia. Vol. 14. Fac. 2, Ed. Academiei, București. Gil, J., M., Pleguezuelos, J. M., 2001. Prey and prey-size selection by the short-toed eagle (Circaetus gallicus) during the breeding season in Granada (south-eastern Spain), Journal of Zoology, 255: 131-137. Iftime, A., 2005. Reptile. In: Bodnarescu N. & Tatole V. (eds.), Cartea Roșie a Vertebratelor din România. Ed. Academiei, București, pp. 173-196. Krecsák, L., Zamfirescu, S., 2008. Vipera (Acridophaga) ursinii in Romania: historical and present distribution. Nort-Western Journal of Zoology, vol. 4, no.2, p. 339-359. Linția, D., 1955. Păsările din România. Vol al III-lea. Editura Ademia Republicii Populare Romîne, p. 459. Munteanu, D., Papadopol, A., Weber, P., 2002. Atlasul populatiilor clocitoare din România, Editia II, Cluj Napoca, p. 31-41. Nilson, G., Andren, C., 2001. The Meadow and Steppe Vipers of Europe and Asia The Vipera (Acridophaga) ursinii complex. Acta Zoologica Academia Scientarium Hungaricae, 47: 88-267. Niskanen, M., Mappes, J., 2005. Significance of the dorsal zigzag pattern of Vipera latastei gaditiana against avian predators. Journal of Animal Ecology, 74: 1091-1101. Péchy, T., Korsós, Z., Újvári, B., 1996. Recovery program for the Meadow Viper in Hungary. Magyar Madártani és Természetvédelmi Egyesület, Budapest. Strugariu, A., Zamfirescu, Ș.R., Gherghel, I., Sahlean, T.C., Moraru, V., Zamfirescu, O., 2011. A preliminary study on population characteristics and ecology of the critically endangered meadow viper Vipera ursinii in the Romanian Danube Delta. Biologia, 66 (1):175-180. Strugariu, A., Zamfirescu, Ș.R., 2011. Population characteristics of the adder (Vipera berus berus) in the Northern Romanian Carpathians with emphasis on colour polymorphism: is melanism always adaptive in vipers? Animal Biology, 61: 457-468. Török, Z., 2002. Potential management plan for conservation of Vipera ursinii from the Danube Delta Biosphere Reserve (Romania). Analele Știinșifice ale INDD, 9: 174-184. Valkonen, J.K., Nokelainen, O., Mappes, J., 2011. Antipredatory function of head shape for vipers and their mimics. PLoS One, 6 (7): e22272. doi: 10.1371/journal.pone.0022272. - 41 -
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