About diet of Vipera ursinii (Bonaparte, 1835) in a central Apennine grassland landscape: what do they eat when orthoptera are not present?

Gabriele Achille; Andrea Brusaferro; Csaba  Szabó; Nazzareno Polini

doi:10.30550/j.azl/2062

Authors

Gabriele Achille Laboratory of Protistology and Biology Education, University of Macerata, 62100 Macerata, Italy https://orcid.org/0009-0009-6925-2082
Andrea Brusaferro School of Biosciences and Veterinary Medicine, University of Camerino, via Gentile III da Varano, IT-62032, Camerino (Macerata), Italy https://orcid.org/0000-0001-5588-2360
Csaba Szabó epartment of Animal Nutrition and Physiology, Faculty of Agricultural and Food Sciences and Environmental Management, University of Debrecen, 4032 Debrecen, Hungary https://orcid.org/0000-0002-2234-204X
Nazzareno Polini Studio Naturalistico, 63900 Fermo, Italy https://orcid.org/0009-0000-0212-438X

DOI:

https://doi.org/10.30550/j.azl/2062

Keywords:

Vipera ursinii, predation strategy, feeding habits, niche breadth

Abstract

Abstract: In this ecological study, the researchers applied themselves to understanding the diet of Vipera ursinii. This viper has a very short period of activity and has a fragmented range; it frequents similar habitats but at different altitudes. In view of its Italian distribution, this study dealt with mountain populations that frequent primary pastures above the forest line, from 1600 to 1850 m a.s.l. At these altitudes and latitudes, the snake is known as a large consumer of meadow orthoptera. The present work was carried out in the Apennines (central Italy), the subjects studied were handled and divided between juveniles and adults. The diet of this snake has never been studied in the areas covered by the following population, so the metapopulation in question is new data. The aim of the research is to identify and analyze the diet of Vipera ursinii even in a period of non-population of orthoptera using methods already in use. Observation of regurgitated material or faecal droppings obtained by non-invasive ventral palpation were the components that led the researchers to unprecedented conclusions for both the species and the snake group: the presence in the diet of new taxa such as ants, slug and caterpillar. This new knowledge may give a new perspective on this taxon that is potentially vulnerable to environmental changes due to environmental thermal alteration phenomena.

Downloads

Download data is not yet available.

Author Biographies

Andrea Brusaferro, School of Biosciences and Veterinary Medicine, University of Camerino, via Gentile III da Varano, IT-62032, Camerino (Macerata), Italy

Nazzareno Polini, Studio Naturalistico, 63900 Fermo, Italy

References

Agrimi, U., Luiselli, L. (1992). Feeding strategies of the viper Ursinii ursinii (Reptilia: Viperidae) in the Apennines. Herpetological Journal, 2: 37 – 42.

Borgo, A. (2015). Abundance, Ecological and Trophical niche breadh and overlap in red fox (Vulpes vulpes) and martens (Martes sp.) in the friulian dolomites (Eastern Alps). Gortania, Botanica, Zoologia, 37: 105-122.

Bosso L., Rebelo H., Garonna A. P., Russo D., (2013) Modelling geographic distribution and detecting conservation gaps in Italy for the threatened beetle Rosalia alpina. Journal for Nature Conservation, 21(2); 72–80. DOI: 10.1016/j.jnc.2012.10.003 DOI: https://doi.org/10.1016/j.jnc.2012.10.003

Baron, J.P. (1980). Donnees sur l'ecologie de Vipera ursinii ursinii au Mont Ventoux. Bull.Soc. Herp.Fr. 14, 26-27.

Baron, J.P. (1989). Feeding of Vipera ursinii ursinii (Bonaparte 1835) in the Mont Ventoux (France): diet and feeding cycle. Abstracts of the First World Congress of Herpetology, Canterbury.

Baron, J.P. (1992). Régime er cycles alimentaires de la vipère d’orsini (Vipera ursinii Bonaparte, 1835) au mont Ventoux, France. Rev. Ecol. (Terre Vie) Vol. 47, pp 287-311. DOI: https://doi.org/10.3406/revec.1992.2408

Brusaferro, A., Iesari V., Tardella F.M., Catorci, A. (2019). Effect of grassland mosaic structure and dynamism on the reproductive habitat suitability for Alectoris graeca in central Apennines. Journal of Mountain Science 16 (12). https://doi.org/10.1007/s11629-019-5695-1 DOI: https://doi.org/10.1007/s11629-019-5695-1

Capula, M., Luiselli, L. (1990). Analysis of the gut contents of Vipera aspis (REPTILIA, VIPERIDAE) from an area of central Italy (TOLFA MOUNTAINS, LATIUM): a new method to study the terrestrial small mammals. Hystn*, (n.s.) 2: 101-107.

Carvalho, C.B., Freitas, E.B., Faria R.G., Batista, R.C., Batista, C.C., Coelho W.A., Bocchiglieri, A. (2008). Histórianatural de Leptodactylus mystacinus e Leptodactylus fuscus (Anura: Leptodactylidae) no Cerrado do Brasil Central Biota Neotropica 8: 105-115. https://doi.org/10.1590/S1676-06032008000300010. DOI: https://doi.org/10.1590/S1676-06032008000300010

Cerasoli, F. Besnard, A., Marchand, M.A., D'Alessandro, P., Iannella, M., Biondi, M. (2021). Determinants of habitat suitability models transferability across geographically disjunct populations: Insights from Vipera ursinii ursinii. Ecol Evol. 11(9): 3991-4011. doi: 10.1002/ece3.7294. PMID: 33976789; PMCID: PMC8093743. DOI: https://doi.org/10.1002/ece3.7294

Console, G., Iannella, M., Cerasoli, F., D'Alessandro, P., Biondi, M. (2020). A European perspective of the conservation status of the threatened meadow viper Vipera ursinii (BONAPARTE, 1835) (Reptilia, Viperidae). Wildlife Biology (2). 10.2981/wlb.00604 DOI: https://doi.org/10.2981/wlb.00604

Ferchaud, A.L., Ursenbacher, S., Cheylan, M., Luiselli, L., Jeli?, D., Halpern, B., Behrooz, R. (2012). Phylogeography of the Vipera ursinii complex (Viperidae): Mitochondrial markers reveal and east–west disjunction in the Palaearctic region. Journal of Biogeography, 39(10), 1836–1847. DOI: https://doi.org/10.1111/j.1365-2699.2012.02753.x

Dreux, P., Saint Girons, H. (1951). Ecologie des vipères : Vipera ursinii. Bull. Soc. Zoo/. France, 76: 47-54.

Feinsinger, P., Speers, E.E., Poole, R.W. (1981). A simple measure of niche breadth. Ecology, 62: 21-32. DOI: https://doi.org/10.2307/1936664

Ferrarini, A., Alatalo, J.M., Gustin, M. (2017). Climate change will seriously impact bird species dwelling above the treeline: A prospective study for the Italian Alps. Science of the total environment, 590: 686-694. DOI: https://doi.org/10.1016/j.scitotenv.2017.03.027

Filippi, E. Luiselli, L. (2002). Vipera ursinii ursinii nel Parco Nazionale del Gran Sasso-Monti della Laga. Unpublished Report, Gran Sasso-Monti della Laga National Park, Assergi (AQ), Italy.

Filippi, E., Rugiero, L., Capula, M., Capizzi, D., Luiselli, L. (2005). Comparative food and body size if five populations of Elaphe quatuorlineata the effects of habitat variation, and the consequences of intersexual body size dimorphism in diet divergence. Copeia: 517-525. DOI: https://doi.org/10.1643/CH-04-350R1

Glaudas, X., Glennon, K.L., Martins, M., Luiselli, L., Fearn, S., Trembath, D.F., Jeli?, D., Alexander, G.J. (2019). Foraging mode, relative prey size and diet breadth: A phylogenetically explicit analysis of snake feeding ecology. J Anim Ecol; 88: 757–767. DOI: https://doi.org/10.1111/1365-2656.12972

Hilpold, A., Seeber, J., Fontana, V., Niedrist, G., Rief, A., Steinwandter, M., Tasser, E., Tappeiner U. (2018). Decline of rare and specialist species across multiple taxonomic groups after grassland intensification and abandonment. Biodiversity and Conservation, 27, 3729–3744. https://doi.org/10.1007/s10531-018-1623-x DOI: https://doi.org/10.1007/s10531-018-1623-x

Joger, U., Crnobrnja-Isailovíc, J., Vogrin, M., Corti, C., Sterijovski, B., Westerström, A., Krecsák, Á., Pérez-Mellado, V., Sá-Sousa, P., Cheylan, M. (2009). Vipera ursinii: The IUCN Red List of Threatened Species. International Union for Conservation of Nature: Gland, Switzerland.

Kjaergaard, J. (1981). A method for examination of stomach content in live snakes and some information on feeding habits in common viper (Vipera berus) in Denmark. Natura Jutlandica, 19: 45-48.

Kofron, C.P. (1978). Foods and habits of aquatic snakes (Reptilia, Serpentes) in a Louisiana swamp. J. Herpetol., 12: 543-554. DOI: https://doi.org/10.2307/1563360

Kotenko, T.I. (1989). Vipera ursinii renardi (Reptilia, Serpentes) in Ukraine. Abstracts of the First World Congress Herpetology, Canterbury.

Kramer, E. (1961). Variation, sexual Dimorphismus, Wachstum und Taxinomie von Vipera ursinii (Bonaparte, 1835) und Vipera kaznakovi (Nikolskij, 1909). Revue Suisse Zoo/., 68: 627-725. DOI: https://doi.org/10.5962/bhl.part.75286

Krassawzeff, B.A. (1943). Zur Biologie der Steppenotter im Nord-Kaukasus. Zoo/. Anz., 142:141-144.

Luiselli, L. (1996). Food Habits of an Alpine Population of the Sand Viper (Vipera ammodytes). Journal of Herpetology, 30(1), 92–94. https://doi.org/10.2307/1564717 DOI: https://doi.org/10.2307/1564717

Luiselli, L., Filippi, E., Di Lena, E. (2007). Ecological Relationships between Sympatric Vipera aspis and Vipera ursinii in high-altitude Habitats of Central Italy. Journal of Herpetology 41 (3): 378-384. DOI: https://doi.org/10.1670/0022-1511(2007)41[378:ERBSVA]2.0.CO;2

Luiselli, L. (2004). Meadow viper, Vipera ursinii, in Italy: Aspects of conservation ecology (Reptilia, Viperidae). Bollettino Di Zoologia, 71(S1): 167–172. DOI: https://doi.org/10.1080/11250003.2004.9525554

Lyet, A., Thuiller W., Cheylan M., Besnard A. (2013). Fine?scale regional distribution modelling of rare and threatened species: Bridging GIS Tools and conservation in practice. Diversity and Distributions, 19 (7): 651–663. 10.1111/ddi.12037. DOI: https://doi.org/10.1111/ddi.12037

Makeyev, M. V. (1964). Biologie de la Vipère des steppes sur le plateau du Chu-IIi (en russe). Zoo/. Zh. SSSR, Moscou, 43:1726-1727.

Malatesta, L., Tardella, F.M., Tavoloni, M. (2019). Land use change in the high mountain belts of the central Apennines led to marked changes of the grassland mosaic. Applied Vegetation Science 22: 243-255. https://doi.org/10.1111/avsc.12416. DOI: https://doi.org/10.1111/avsc.12416

Méhely, L.V. (1911). Systematisch-phylogenetische studien an viperiden. IX Annales Musei Nationalis Hungarici: 186-243.

Méhely, L. (1984). Eine neue Giftschlange der ungarischen Fauna (Vipera rákosiensis My.). Mat.Természettud.Ért, 12(2–3): 87–92.

Mizsei, E., Jablonski, D., Roussos, S.A., Dimaki, M., Ioannidis, Y., Nilson, G.Ö.R.A.N., Nagy Z.T. (2017). Nuclear markers support the mitochondrial phylogeny of Vipera ursinii-renardi complex (Squamata: Viperidae) and species status for the Greek meadow viper. Zootaxa, 4227 (1): 75-88. DOI: https://doi.org/10.11646/zootaxa.4227.1.4

Mizsei, E., Zinenko, O., Sillero, N., Ferri, V., Roussos S.A., Szabolcs, M. (2018). The distribution of meadow and steppe vipers (Vipera graeca, V. renardi and V. ursinii): a revision of the New Atlas of Amphibians and Reptiles of Europe. Basic and Applied Herpetology, 32, pp.77-83. DOI: https://doi.org/10.11160/bah.94

Mizsei, E., Budai, M., Móré, A., Rák, G., Radovics, D., Bancsik, B., Wenner, B., Márton, S., Korsós, Z., Lengyel, S., Vadász, C. (2023). Management impacts on three reptile species (Vipera ursinii, Lacerta agilis, Lacerta viridis) in sandy grasslands in Hungary: Mowing should be avoided. Conservation Science and Practice, 5(12): 13048. https://doi.org/10.1111/csp2.13048. DOI: https://doi.org/10.1111/csp2.13048

Naulleau, G. (1973). Les Serpentes de France (Colubrides, Viperides Rev. Fr. Aquar. Herpet. No. special, hors serie, 9-24.

Naulleau, G. (1984). Les Serpentes de France. Rev. Fr. Aquar. Herpet. fasc. 3-4, 2nd edition.

Nilson, G., Andrén, C., Joger, U. (1993). A re-evaluation of the taxonomic status of the Moldavian steppe viper based on immunological investigations, with a discussion of the hypothesis of secondary intergradation between Vipera ursinii rakosiensis and Vipera (ursinii) renardi. Amphibia-Reptilia, 14(1), 45-57. https://doi.org/10.1163/156853893X00183. DOI: https://doi.org/10.1163/156853893X00183

Oliveira, M., Gottschalk M.S., Loebmann D., Santos M.B., Miranda S., Rosa C., Tozetti A.M. (2015). Diet composition and niche overlap in two sympatric species of Physalaemus (Anura, Leptodactylidae, Leiuperinae) in coastal subtemperate wetlands. Herpetology Notes 8: 173-177.

Ozol, M.K. (1941). Beitriige zur Biologie von Vipera renardi. Arb. Woroschilowsk Pedag. Inst., 3, Woroschilowsk.

Pianka, E.R. (1974). Niche overlap and diffuse competition. Proc. Nat. Acad. Sci. USA, 71: 2141-2145. DOI: https://doi.org/10.1073/pnas.71.5.2141

Pearson, K. (1900). On the criterion that a given system of deviations fro the probable in the case of a correlated system of variables is such that it can be reasonably supposed to have arisen from random sapling. Philosophical Magazine. Series 5, 50 (302): 157-175. doi:10.1080/14786440009463897. DOI: https://doi.org/10.1080/14786440009463897

Pedrotti, F. (1969). Introduzione alla vegetazione dell'Appennino Centrale. Mitt. ostalp. -din. pflanzensoz. Arbeitsgem. Camerino, 9: 21-57.

Prigioni, C. (1991). The study of the diet of the fox (Vulpes vulpes). Hystrix, 3: 51-62.

R Core Team. (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org.

Rebelo, H., Tarroso, P., Jones, G. (2010). Predicted impact of climate change on European bats in relation to their biogeographic patterns. Global Change Biology, 16 (2): 561–576. 10.1111/j.1365-2486.2009.02021. DOI: https://doi.org/10.1111/j.1365-2486.2009.02021.x

Rivas-Martínez, S., Rivas-Sáenz, S. (2016). Worldwide bioclimatic classification system, Phytosociological Research Center, Spain. http://www.globalbioclimatics.org.

Rolando, A. (1986). La teoria della nicchia: prospettive e problemi in ornitologia. Avocetta, 10: 1-36.

Saint Girons, H. (1975). Observations preliminaires sur la thermoregulation des Viperes d'Europe. Vie et Milieu 25, Fasc. I, Serie C (1) : 37-168.

Saint Girons, H. (1978). Thermoregulation comparee des Viperes d'Europe. Etude biotelemetrique. Terre et Vie 32, 4 (1): 7-440. DOI: https://doi.org/10.3406/revec.1978.5017

Saint Girons, H. (1979). Les cycles alimentaires des Viperes europeennes dans des conditions seminaturelles. Ann. Biol. Anim. Bioc. Biophys. 1 9, 125- 1 34. DOI: https://doi.org/10.1051/rnd:19790111

Saint Girons, H., Naulleau, G. (1981). Poids des nouveaunes et strategies reproductives des Viperes europeenes. Rev. Ecol (Terre et Vie). 35: 597-616. DOI: https://doi.org/10.3406/revec.1981.4129

Simpson, E.H. (1949). Measurements of Diversity. Nature, 163: 688. http://dx.Doi.org/10-1038/163688a0 DOI: https://doi.org/10.1038/163688a0

Soberón, J. Nakamura, M. (2009). Niches and distributional areas: Concepts, methods, and assumptions. Proceedings of the National Academy of Sciences of the United States of America, 106 (Supplement 2): 19644–19650. 10.1073/pnas.0901637106. DOI: https://doi.org/10.1073/pnas.0901637106

Sutherland, W.J. (2006). Ecological Census Techniques: A handbook. Second Edition. Cambridge University Press.: 432 pp. DOI: https://doi.org/10.1017/CBO9780511790508

Temple, H.J. Cox, N. (2009). European red list of reptiles.

Terentiev, P.V., Chernov, S.A. (1949). Key to Amphibians and Reptiles. Moscou (Israel Programm for Scientific Translations, Jerusalem, 1965).

Zinenko, O., Stümpel, N., Mazanaeva, L., Bakiev, A., Shiryaev, K., Pavlov, A., Kotenko, T., Kukushkin O., Chikin, Y., Duisebayeva, T., Nilson, G., Orlov, N.L., Tuniyev, S., Ananjeva, N.B., Murphy R.W., Joger ,U. (2015). Mitochondrial phylogeny shows multiple independent ecological transitions and northern dispersion despite of Pleistocene glaciations in meadow and steppe vipers (Vipera ursinii and Vipera renardi). Molecular Phylogenetics and Evolution, 84: 85–100. 10.1016/j.ympev.2014.12.005. DOI: https://doi.org/10.1016/j.ympev.2014.12.005