Vol. 76 (1) 2024
ARTICLES
Importance of Agricultural Areas for the Distribution of Protected Amphibian Species in Bulgaria
Georgi Popgeorgiev1, Simeon Lukanov2,*, Blagovesta Dimitrova2 & Borislav Naumov2
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1National Museum of Natural History, Bulgarian Academy of Sciences, blvd. Tzar Osvoboditel 1, 1000 Sofia, Bulgaria
*2Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria; simeon_lukanov@abv.bg
Abstract
We mapped the distribution for the past 18 years (2004–2022) of five protected amphibian species across Bulgaria using a spatial resolution of 100 m2 in CORINE Land Cover 2018 (CLC). Since the altitudinal distribution and habitat preferences of these species in the country make them potentially vulnerable to agricultural activities, the primary aim was to establish what part of the known records of each species falls within agricultural lands. Results indicated that all five studied species inhabit CLC types falling within the general type “Agricultural areas” (CLC Level 1: 2), with four species predominantly occurring in such regions. In total, three species (Bombina bombina, Triturus cristatus and T. ivanbureschi) had more than 50% of their distribution records in agricultural areas. In another species, Triturus dobrogicus, the percentage was above 40%. The lowest number (under 36%) was for B. variegata. For T. dobrogicus, nearly 32% of all records were concentrated in the CLC Level 3 category “Non-irrigated arable lands”. This data suggests that a large percentage of the populations of these protected species across Bulgaria are potentially exposed to agricultural practices such as pesticide use, or crop land aggregation and highlight the need for regional approach for species protection.
Key words
conservation, CORINE Land Cover, occurrence records, Bombina, Triturus
How to Cite
Popgeorgiev G., Lukanov S., Dimitrova B. & Naumov B. 2024. Importance of Agricultural Areas for the Distribution of Protected Amphibian Species in Bulgaria. Acta zoologica bulgarica 76 (1) 87-96.
References
- Adams E., Leeb C. & Brühl C. A. 2021. Pesticide exposure affects reproductive capacity of common toads (Bufo bufo) in a viticultural landscape. Ecotoxicology 30: 213–223.
- Agostini M. A., Roesler I., Bonetto C., Ronco A. E. & Bilenca D. 2020. Pesticides in the real world: The consequences of GMO-based intensive agriculture on Native Amphibians. Biological Conservation 241: 108355. doi:10.1016/j.biocon.2019.108355.
- Acquaroni M., Svartz G. & Pérez C. 2022. Acute, chronic and neurotoxic effects of dimethoate pesticide on rhinella arenarum throughout the development. Journal of Environmental Science and Health Part B 57(2): 142–152. doi:10.1080/03601234.2022.2034459.
- Arntzen J. & Wallis G. 1999. Geographic variation and taxonomy of crested newts (Triturus cristatus superspecies): morphological and mitochondrial DNA data. Contributions to Zoology 68(3): 181–203.
- Bancila R. I., Lattuada M. & Sillero N. 2023. Distribution of amphibians and reptiles in agricultural landscape across Europe. Landscape Ecology 38(3): 861–874. doi:10.1007/s10980-022-01583-w.
- Barral M. P., Villarino S., Levers C., Baumann M., Kuemmerle T. & Mastrangelo M. 2020. Widespread and major losses in multiple ecosystem services as a result of agricultural expansion in the Argentine Chaco. Journal of Applied Ecology 57(12): 2485–2498. doi:10.1111/1365-2664.13740.
- Berger G., Pfeffer H., Kachele H., Andreas S. & Hoffmann J. 2003. Nature protection in agricultural landscapes by setting aside unproductive areas and ecotones within arable fields (“Infield Nature Protection Spots”). Journal for Nature Conservation 11(3): 221–233.
- Berger G., Graef F., Pallut B., Hoffmann J., Brühl C. A. & Wagner N. A. 2018. How does changing pesticide usage over time affect migrating amphibians: a case study on the use of glyphosate-based herbicides in German agriculture over 20 years. Frontiers in Environmental Sciences 6:6. doi: 10.3389/fenvs.2018.00006
- Carpio A. J., Oteros J., Tortosa F. S. & Guerrero-Casado J. 2016. Land use and biodiversity patterns of the herpetofauna: the role of olive groves. Acta Oecologica 70: 103–111.
- Chagnon M., Kreutzweiser D., Mitchell E. A., Morrissey C. A., Noome D. A. & van der Sluijs P. J. 2014. Risks of large-scale use of systemic insecticides to ecosystem functioning and services. Environmental Science and Pollution Research 22(1): 119–134. doi:10.1007/s11356-014-3277-x.
- Fahrig L., Baudry J., Brotons L., Burel G., Crist T. O., Fuller R. J., Sirami C., Siriwardena G. M. & Martin J. M. 2010. Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecology Letters 14(2): 101–112. doi:10.1111/j.1461-0248.2010.01559.x.
- Gibbons J. W., Scott D. E., Ryan T. E., Buhlmann K. A., Tuberville T. D., Metts B. S., Greene J. L., Mills T., Leiden Y., Poppy S. & Winne C. T. 2000. The global decline of reptiles, déjà vu amphibians: reptile species are declining on a global scale. Six significant threats to reptile populations are habitat loss and degradation, introduced invasive species, environmental pollution, disease, unsustainable use, and global climate change. Bioscience 50: 653–666.
- Gherghel I. & Iftime A. 2009. On the presence of the Danube crested newt, Triturus dobrogicus, at Durankulak Lake, Bulgaria. North-Western Journal of Zoology 5(1): 209–213.
- Greulich K. & Pflugmacher S. 2004. Uptake and effects on detoxication enzymes of Cypermethrin in embryos and tadpoles of Amphibians. Archives of Environmental Contamination and Toxicology 47(4): 489–495. doi:10.1007/s00244-004-2302-3.
- Guerkan M., Serbest S. & Hayretdağ S. S. 2016. Acute toxicity of the synthetic pyrethroid alpha-cypermethrin on the tadpoles of variable green toad, Bufotes variabilis (Amphibia:Anura). Ege Journal of Fisheries and Aquatic Sciences 33(4): 367–371. doi:10.12714/egejfas.2016.33.4.10.
- Guiller G., Legentilhomme J., Boissinot A., Blouin-Demers G., Barbraud C. & Lourdais O. 2022. Response of farmland reptiles to agricultural intensification: Collapse of the common adder Vipera berus and the western green lizard Lacerta bilineata in a hedgerow landscape. Animal Conservation 25(6): 849–864. doi:10.1111/acv.12790.
- Hammer Ø., Harper D. A. T. & Ryan P. D. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1): 1–9.
- Jayawardena U. A., Navaratne A. N., Amerasinghe P. H. & Rajakaruna R. S. 2011. Acute and chronic toxicity of four commonly used agricultural pesticides on the Asian common toad, Bufo melanostictus Schneider. Journal of the National Science Foundation of Sri Lanka 39(3): 267–276.
- Jehle R. & Arntzen J. 2000. Post-breeding migrations of newts (Triturus cristatus and T. marmoratus) with contrasting ecological requirements. Journal of Zoology 251(3): 297–306.
- Jones D. K., Hammond J. I. & Relyea R. A. 2010. Roundup and amphibians: the importance of concentration, application time, and stratification. Environmental Toxicology Chemistry 29(9): 2016–2025. doi: 10.1002/etc.240. PMID: 20821659.
- Kovar R., Brabec M., Vita R. & Bocek R. 2009. Spring migration distances of some Central European amphibian species. Amphibia Reptilia 30(3): 367–378.
- Lenhardt P. P., Brühl C. A. & Berger G. 2015. Temporal coincidence of amphibian migration and pesticide applications on arable fields in spring. Basic & Applied Ecology 16: 54–63.
- Litvinchuk S. & Borkin L. 2009. Evolution, systematics and distribution of Crested newts (Triturus cristatus complex) in Russia and adjacent countries. Evropeisky Dom Press, St. Petersburg, 592 pp. (In Russian, English summary)
- Ministry of Agriculture, Department “Agrostatistics” Results and analyses, No. 419 – October 2022
- Naumov B. & Biserkov V. 2013. On the distribution and subspecies affiliation of Triturus dobrogicus (Amphibia: Salamandridae) in Bulgaria. Acta Zoologica Bulgarica 65(3): 307–313.
- Naumov B., Lukanov S., Vacheva E. & Slavchev M. 2023. Distribution and ecology of Triturus cristatus (Laurenti, 1768) (Amphibia: Salamandridae) in Bulgaria. Acta Zoologica Bulgarica 75(1): 113–122.
- Newbold T., Hudson L. N., Phillips H. R. P., Hill S. L. L., Contu S., Lysenko I., Blandon A., Butchart S. H. M., Booth H. L., Day J., de Palma A., Harrison M. L. K., Kirkpatrick L., Pynegar E., Robinson A., Simpson J., Mace G. M., Scharlemann J. P. & Purvis A. 2014. A global model of the response of tropical and sub-tropical forest biodiversity to anthropogenic pressures. Proceedings of the Royal Society of London. Series B 281: 20141371.
- Ockleford C., Adriaanse P., Berny P., Brock T., Duquesne S., Grilli S., Hernandez-Jerez A. F., Bennekou S. H., Klein M., Kuhl T., Laskowski R., Machera K., Pelkonen O., Pieper S., Stemmer M., Sundh I., Teodorovic I., Tiktak A., Topping C. J., Wolterink G., Aldrich A., Berg C., Ortiz-Santaliestra M., Weir S., Streissl F. & Smith R. H. 2018. Scientific opinion on the state of the science on pesticide risk assessment for amphibians and reptiles. EFSA Journal 16(2): 5125 doi: 10.2903/j.efsa.2018.5125
- Pope S.E., Fahrig L. & Merriam H.G. 2000. Landscape complementation and metapopulation effects on leopard frog populations. Ecology 81: 2498–2508.
- Popgeorgiev G., Naumov B., Kornilev Y., Vergilov V., Slavchev M., Lukanov S., Dyugmedzhiev A., Stoyanov A., Dobrev D. & Tzankov N. 2019. Diversity and distribution of amphibians and reptiles in the Bulgarian part of the Lower Danube. In: Shurulinkov P., Hubenov Z., Beshkov S. & Popgeorgiev G. (Eds): Biodiversity of the Bulgarian–Romanian section of the Lower Danube. New York: Nova Science Publishers, pp. 283–314.
- Sayim F. 2010. Toxicity of trifluralin on the embryos and larvae of the red-bellied toad, Bombina bombina. Turkish Journal of Zoology 34(4): Article 6. doi: 10.3906/zoo-0811-21
- Scales B. R. & Marsden S. J. 2008. Biodiversity in small-scale tropical agroforests: a review of species richness and abundance shifts and the factors influencing them. Environmental Conservation 35: 160–172.
- Sillero N., Campos J., Bonardi A., Corti A., Creemers R., Crochet P., Crnobrnja-Isailović J., Denoël M., Ficetola G. F., Gonçalves J., Kuzmin S., Lymberakis P., de Pous P., Rodríguez A., Sindaco R., Speybroeck J., Toxopeus B., Vieites D. R. & Vences M. 2014. Updated distribution and biogeography of amphibians and reptiles of Europe. Amphibia–Reptilia 35(1): 1–31. doi: 10.1163/15685381-00002935
- Speybroeck J., Beukema W., Bok B. & van der Voort J. 2016. Field guide to the amphibians and reptiles of Britain and Europe. London: Bloomsbury. 423 p.
- Speybroeck J., Beukema W., Dufresnes C., Fritz U., Jablonski D., Lymberakis P., Martínez-Solano I., Razzetti E., Vamberger M., Vences M., Vörös J. & Crochet P. 2020. Species list of the European herpetofauna – 2020 update by the Taxonomic Committee of the Societas Europaea Herpetologica. Amphibia–Reptilia 41(2): 139–189.
- Stojanov A., Tzankov N. & Naumov B. 2011. Die Amphibien und Reptilien Bulgariens. Frankfurt am Main: Chimaira. 588 p.
- Thanomsit C., Saowakoon S., Wattanakornsiri A., Nanuam J., Prasatkaew W., Nanthanawat P., Mongkolvai P. & Chalorcharoenying W. 2020. The glyphosate (Roundup): fate in aquatic environment. Naresuan University Journal: Science and Technology 21(1): 65–81.
- Todd B. D., Willson J. D., Gibbons J. W. 2010. The global status of reptiles and causes of their decline. In: Sparling D. W., Linder G., Bishop C. A. & Krest S. (Eds): Ecotoxicology of amphibians and reptiles, 2nd edn. Boca Raton: CRC Press, pp. 47–67.
- Tscharntke T., Clough Y., Wanger T. C., Jackson L., Motzke I., Perfecto I., Vandermeer J. & Whitbread A. 2012. Global food security, biodiversity conservation and the future of agricultural intensification. Biological Conservation 151: 53–59.
- Vitt L. J. & Caldwell J. P. 2009. Spacing, movements, and orientation. In: Vitt L. J. & Caldwell J. P. (Eds): Herpetology: an introductory biology of amphibians and reptiles. San Diego: Academic Press, pp. 217–238.
- Wielstra B., Litvinchuk S., Naumov B., Tzankov N. & Arntzen J. 2013. A revised taxonomy of crested newts in the Triturus karelinii group (Amphibia: Caudata: Salamandridae), with the description of a new species. Zootaxa 3682(3): 441–453.
- Wielstra B., Sillero N., Vörös J. & Arntzen J. 2014. The distribution of the crested and marbled newt species (Amphibia: Salamandridae: Triturus) – an addition to the New Atlas of Amphibians and Reptiles of Europe. Amphibia–Reptilia 35: 376–381.
- Zaffaroni N., Zavanella T. & Arias E. 1979. Peripheral blood cells in the crested newt after long-term exposure to the fungicide manganese ethylenebisdithiocarbamate (Maneb). Bulletin of environmental contamination and toxicology 23: 587–591.


