Comparison of wild bee communities of three semi-natural meadow habitats at Harghita–Covasna Region, Transylvania, Romania
Abstract
In the temperate climate wild bees are the most important pollinator organisms. Pollination is essential for the communities of semi-natural habitats since this ecosystem service directly affects plant reproduction. The diversity of wild bees living in such areas is remarkably high, but they are susceptible to various anthropogenic influences.
In our study, the composition and structure of wild bee communities were examined in Romania (Transylvania) at three semi-natural areas near Filia, Merești and Vârghiș. The surveyed areas were used as extensive meadows under relatively low but slightly different anthropogenic influence levels. We collected bees in these areas at several places (9 sampling points/area) by individual netting four times during the season. In the studied areas, 129 bee species were found, which makes up about 18% of the approximately 726 wild bee species registered in Romania. In addition to the high number of species, we also observed high diversity values. Our results showed that, even at our sampling site closest to the human settlements, the extensive use of the surveyed areas as meadows allows the development of diverse, species-rich bee communities.
References
Andersson, G. K., Rundlöf, M. & Smith, H. G. (2012): Organic farming improves pollination success in strawberries. – PloS One 7(2). https://doi.org/10.1371/journal.pone.0031599
Ashman, T. L., Knight, T. M., Steets, J. A., Amarasekare, P., Burd, M., Campbell, D. R., Dudash, M. R., Johnston, M. O., Mazer, S. J., Mitchell, R. J., Morgan, M. T. & Wilson, W. G. (2004): Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. – Ecology 85(9): 2408–2421. https://doi.org/10.1890/03-8024
Babai, D. & Molnár, Z. (2014): Small-scale traditional management of highly species-rich grasslands in the Carpathians. – Agriculture, Ecosystems & Environment 182: 123–130. https://doi.org/10.1016/j.agee.2013.08.018
Babai, D. & Molnár, Z. (2016): Species-rich mountain grasslands through the eyes of the farmer: Flora, species composition, and extensive grassland management. – Martor 21: 146–149.
Babai, D., Tóth, A., Szentirmai, I., Biró, M., Máté, A., Demeter, L., Szépligeti, M., Varga, A., Molnár, Á., Kun, R. & Molnár, Z. (2015): Do conservation and agri-environmental regulations effectively support traditional small-scale farming in East-Central European cultural landscapes? – Biodiversity and Conservation 24(13): 3305–3327. https://doi.org/10.1007/s10531-015-0971-z
Ban-Calefariu, C. & Sárospataki, M. (2007): Contributions to the knowledge of Bombus and Psithyrus genera (Apoidea: Apidae) in Romania. – Travaux du Muséum National d’Histoire Naturelle “Grigore Antipa” 1: 239–258.
Ban, C. M. (2005): Contributions to the knowledge of apoid hymenopterans (Hymenoptera: Megachilidae, Anthophoridae, Apidae) from Maramures (Romania). Part I. – Travaux du Muséum National d’Histoire Naturelle “Grigore Antipa” 48: 289–301.
Ban, C. M. &Tomozei, B. (2006): New data on the Apoid hymenopterans (Hymenoptera: Andrenidae, Anthophoridae, Apidae) from Dobrogea (Romania). – Travaux du Muséum National d’Histoire Naturelle ”Grigore Antipa” 49: 307–318.
Batáry, P., Dicks, L. V., Kleijn, D. & Sutherland, W. J. (2015): The role of agri-environment schemes in conservation and environmental management. – Conservation Biology 29(4): 1006–1016. https://doi.org/10.1111/cobi.12536
Baude, M., Kunin, W. E., Boatman, N. D., Conyers, S., Davies, N., Gillespie, M. A., Morton, R. D, Smart, S. M. & Memmott, J. (2016): Historical nectar assessment reveals the fall and rise of floral resources in Britain. – Nature 530(7588): 85–88. https://doi.org/10.1038/nature16532
Bawa, K. S. (1990): Plant-pollinator interactions in tropical rain forests. – Annual Review of Ecology and Systematics 21: 399–422. https://doi.org/10.1146/annurev.es.21.110190.002151
Biesmeijer, J. C., Roberts, S. P., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T., Schaffers, A. P., Potts, S. G., Kleukers, R., Thomas, C. D, Settele, J. & Kunin, W. E. (2006): Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. – Science 313(5785): 351–354. https://doi.org/10.1126/science.1127863
Brittain, C., Williams, N., Kremen, C. & Klein, A. M. (2013): Synergistic effects of non-Apis bees and honey bees for pollination services. – Proceedings of the Royal Society B: Biological Sciences 280(1754): 20122767. https://doi.org/10.1098/rspb.2012.2767
Dahlström, A., Iuga, A. M. & Lennartsson, T. (2013): Managing biodiversity rich hay meadows in the EU: a comparison of Swedish and Romanian grasslands. – Environmental Conservation 40(2): 194–205. https://doi.org/10.1017/S0376892912000458
Darvill, B., O’Connor, S., Lye, G. C., Waters, J., Lepais, O. & Goulson, D. (2010): Cryptic differences in dispersal lead to differential sensitivity to habitat fragmentation in two bumblebee species. – Molecular Ecology 19(1): 53–63. https://doi.org/10.1111/j.1365-294X.2009.04423.x
De Heer, M., Kapos, V. & Ten Brink, B. J. E. (2005): Biodiversity trends in Europe: development and testing of a species trend indicator for evaluating progress towards the 2010 target. – Philosophical Transactions of the Royal Society B: Biological Sciences 360(1454): 297–308. https://doi.org/10.1098/rstb.2004.1587
Doré, M., Fontaine, C. & Thébault, E. (2021): Relative effects of anthropogenic pressures, climate, and sampling design on the structure of pollination networks at the global scale. – Global Change Biology 27(6): 1266–1280. https://doi.org/10.1111/gcb.15474
Dorresteijn, I., Loos, J., Hanspach, J. & Fischer, J. (2015): Socioecological drivers facilitating biodiversity conservation in traditional farming landscapes. – Ecosystem Health and Sustainability 1(9): 1–9. https://doi.org/10.1890/EHS15-0021.1
Eeraerts, M., Vanderhaegen, R., Smagghe, G. & Meeus, I. (2020): Pollination efficiency and foraging behaviour of honey bees and non-Apis bees to sweet cherry. – Agricultural and Forest Entomology 22(1): 75–82. https://doi.org/10.1111/afe.12363
Ellis, A. M., Myers, S. S. & Ricketts, T. H. (2015): Do pollinators contribute to nutritional health? – PLoS One 10(1). https://doi.org/10.1371/journal.pone.0114805
Evans, D. (2006): The habitats of the European Union Habitats Directive. – Biology and Environment: Proceedings of the Royal Irish Academy 106: 167–173. https://doi.org/10.3318/BIOE.2006.106.3.167
Gallai, N., Salles, J. M., Settele, J. & Vaissière, B. E. (2009): Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. – Ecological Economics 68(3): 810–821. https://doi.org/10.1016/j.ecolecon.2008.06.014
Gathmann, A. & Tscharntke, T. (2002): Foraging ranges of solitary bees. – Journal of Animal Ecology 71(5): 757–764. https://doi.org/10.1046/j.1365-2656.2002.00641.x
Goulson, D. (2003): Bumblebees: their behaviour and ecology. – Oxford University Press, USA.
Goulson, D., Hanley, M. E., Darvill, B., Ellis, J. S. & Knight, M. E. (2005): Causes of rarity in bumblebees. – Biological Conservation 122(1): 1–8. https://doi.org/10.1016/j.biocon.2004.06.017
Goulson, D., Lye, G. C. & Darvill, B. (2008): Decline and conservation of bumble bees. – Annual Review of Entomology 53: 191–208. https://doi.org/10.1146/annurev.ento.53.103106.093454
Havas, E., Sárospataki, M. & Józan, Zs. (2008): Új adatok a Tihanyi-félsziget vadméhfaunájával kapcsolatban. [New data on Apoid fauna of Tihany Peninsula.] – Állattani Közlemények 93: 17–24. [in Hungarian]
Hill, M. O. (1973): Diversity and evenness: a unifying notation and its consequences. – Ecology 54(2): 427–432. https://doi.org/10.2307/1934352
Hoehn, P., Tscharntke, T., Tylianakis, J. M. & Steffan-Dewenter, I. (2008): Functional group diversity of bee pollinators increases crop yield. – Proceedings of the Royal Society B: Biological Sciences 275(1648): 2283–2291. https://doi.org/10.1098/rspb.2008.0405
Hooke, R. L., Martín-Duque, J. F. & Pedraza, J. (2012): Land transformation by humans: a review. – GSA Today 22(12): 4–10. https://doi.org/10.1130/GSAT151A.1
Huband, S., McCracken, D. I. & Mertens, A. (2010): Long and short-distance transhumant pastoralism in Romania: past and present drivers of change. – Practical Action Publishing. https://doi.org/doi:10.3362/2041-7136.2010.004
Klein, A. M., Vaissiere, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C. & Tscharntke, T. (2007): Importance of pollinators in changing landscapes for world crops. – Proceedings of the Royal Society, B 274(1608): 303–313. https://doi.org/10.1098/rspb.2006.3721
Kovács-Hostyánszki, A., Földesi, R., Mózes, E., Szirák, Á., Fischer, J., Hanspach, J. & Báldi, A. (2016): Conservation of pollinators in traditional agricultural landscapes–new challenges in Transylvania (Romania) posed by EU accession and recommendations for future research. – PloS One 11(6): e0151650. https://doi.org/10.1371/journal.pone.0151650
Kremen, C., Williams, N. M., Aizen, M. A., Gemmill-Herren, B., LeBuhn, G., Minckley, R., Packer, L., Potts, S. G., Roulston, T., Steffan-Dewenter, I., Vázquez, D. P., Winfree, R., Adams, L., Crone, E. E., Greenleaf, S. S., Keitt, T. H., Klein, A-M., Regetz, J., Ricketts, T. H. (2007): Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. – Ecology Letters 10(4): 299–314. https://doi.org/10.1111/j.1461-0248.2007.01018.x
Kremen, C., Williams, N. M. & Thorp, R. W. (2002): Crop pollination from native bees at risk from agricultural intensification. – Proceedings of the National Academy of Sciences 99(26): 16812–16816. https://doi.org/10.1073/pnas.262413599
Kun, R., Bartha, S., Malatinszky, Á., Molnár, Z., Lengyel, A. & Babai, D. (2019): “Everyone does it a bit differently!”: Evidence for a positive relationship between micro-scale land-use diversity and plant diversity in hay meadows. – Agriculture, Ecosystems & Environment 283: 106556. https://doi.org/10.1016/j.agee.2019.05.015
MacInnis, G. & Forrest, J. R. (2020): Field design can affect cross-pollination and crop yield in strawberry (Fragaria × ananassa D.). – Agriculture, Ecosystems & Environment 289: 106738. https://doi.org/10.1016/j.agee.2019.106738
Marini, L., Fontana, P., Klimek, S., Battisti, A. & Gaston, K. J. (2009): Impact of farm size and topography on plant and insect diversity of managed grasslands in the Alps. – Biological Conservation 142(2): 394–403. https://doi.org/10.1016/j.biocon.2008.10.034
Matache, I. & Ban, C. M. (2006): Family Megachilidae (Hymenoptera: Apoidea) in Dobrogea (Romania). – Travaux du Muséum National d’Histoire Naturelle “Grigore Antipa” 49: 297–306.
Michener, C. D. (2000): The bees of the world. Vol. 1. – Johns Hopkins University Press, Baltimore.
Myklestad, Å. & Sætersdal, M. (2003): Effects of reforestation and intensified land use on vascular plant species richness in traditionally managed hay meadows. – Annales Botanici Fennici 40(6): 423–441.
Newbold, T., Hudson, L. N., Hill, S. L., Contu, S., Lysenko, I., Senior, R. A., Börger, L., Bennett, D.J., Choimes, A., Collen, B. & Day, J. (2015): Global effects of land use on local terrestrial biodiversity. – Nature 520(7545): 45–50. https://doi.org/10.1038/nature14324
Nieto, A., Roberts, S. P. M., Kemp, J., Rasmont, P., Kuhlmann, M., García Criado, M., Biesmeijer, J. C., Bogusch, P., Dathe, H. H., De la Rúa, P., De Meulemeester, T., Dehon, M., Dewulf, A., Ortiz-Sánchez, F. J., Lhomme, P., Pauly, A., Potts, S. G., Praz, C., Quaranta, M., Radchenko, V. G., Scheuchl, E., Smit, J., Straka, J., Terzo, M., Tomozii, B., Window, J. & Michez, D. (2014): European Red List of bees. – Publication Office of the European Union, Luxembourg.
Poschlod, P., Bakker, J. P. & Kahmen, S. (2005): Changing land use and its impact on biodiversity. – Basic and Applied Ecology 6(2): 93–98. https://doi.org/10.1016/j.baae.2004.12.001
Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O. & Kunin, W. E. (2010): Global pollinator declines: trends, impacts and drivers. – Trends in Ecology and Evolution 25(6): 345–353. https://doi.org/10.1016/j.tree.2010.01.007
Potts, S. G., Imperatriz-Fonseca, V., Ngo, H. T., Aizen, M. A., Biesmeijer, J. C., Breeze, T. D., Dicks, L. V., Garibaldi, L. A., Hill, R., Settele, J. & Vanbergen, A. J. (2016): Safeguarding pollinators and their values to human well-being. – Nature 540(7632): 220–229. https://doi.org/10.1038/nature20588
Potts, S. G., Vulliamy, B., Roberts, S., O’Toole, C., Dafni, A., Ne’eman, G. & Willmer, P. (2005): Role of nesting resources in organising diverse bee communities in a Mediterranean landscape. – Ecological Entomology 30(1): 78–85. https://doi.org/10.1111/j.0307-6946.2005.00662.x
Quintero, C., Morales, C. L. & Aizen, M. A. (2010): Effects of anthropogenic habitat disturbance on local pollinator diversity and species turnover across a precipitation gradient. – Biodiversity and Conservation 19(1): 257–274. https://doi.org/10.1007/s10531-009-9720-5
Samu, F., Neidert, D., Szita, É., Fetykó, K., Botta-Dukát, Z. & Horváth, A. (2010): The role of ‘low-input’ agri-environmental schemes in the enhancement of functional biodiversity of Hungarian arable fields. – IOBC/WPRS Bulletin 56: 105–108.
Sárospataki, M. G., Bakos, R., Horváth, A., Neidert, D. & Horváth, V. (2016): The role of local and landscape level factors in determining bumblebee abundance and richness. – Acta Zoologica Academiae Scientiarum Hungaricae 62(4): 387–407. https://doi.org/10.17109/AZH.62.4.387.2016
Sárospataki, M., Báldi, A., Batáry, P., Józan, Z., Erdős, S. & Rédei, T. (2009): Factors affecting the structure of bee assemblages in extensively and intensively grazed grasslands in Hungary. – Community Ecology 10(2): 182–188. https://doi.org/10.1556/ComEc.10.2009.2.7
Sárospataki, M. & Fazekas, J. P. (1995): Ecological characteristics of bee communities on a sandy grassland. – Tiscia 29: 41–46.
Senapathi, D., Carvalheiro, L. G., Biesmeijer, J. C., Dodson, C. A., Evans, R. L., McKerchar, M., Morton R. D., Moss, E. D., Roberts S. P. M., Kunin, W. E & Potts, S. G. (2015): The impact of over 80 years of land cover changes on bee and wasp pollinator communities in England. – Proceedings of the Royal Society B: Biological Sciences 282(1806): 20150294. https://doi.org/10.1098/rspb.2015.0294
Tilman, D., Fargione, J., Wolff, B., D’Antonio, C., Dobson, A., Howarth, R., Schindler, D., Schlesinger, W. H., Simberloff, D. & Swackhamer, D. (2001): Forecasting agriculturally driven global environmental change. – Science 292(5515): 281–284. https://doi.org/10.1126/science.1057544
Tomozii, B. & Toma, V. C. (2011): New records of megachilid bees (Hymenoptera: Apiformes: Megachilidae) from Romania. – Studii şi Comunicări, Complexul Muzeal de Ştiintele Naturii “Ion Borcea” Bacău 24: 61–68.
Tomozii, B. (2020): Bees of Romania. http://www.beesofromania.ro [accessed: 11/07/2020]
Veen, P., Jefferson, R., de Smidt, J. & van der Straaten, J. (2009): Grasslands in Europe of high nature value. – KNNV Publishing, Zeist, 320 pp. https://doi.org/10.1163/9789004278103
Winfree, R., Aguilar, R., Vázquez, D. P., LeBuhn, G. & Aizen, M. A. (2009): A meta-analysis of bees’ responses to anthropogenic disturbance. – Ecology 90(8): 2068–2076. https://doi.org/10.1890/08-1245.1
Winfree, R., Bartomeus, I. & Cariveau, D. P. (2011): Native pollinators in anthropogenic habitats. – Annual Review of Ecology, Evolution, and Systematics 42: 1–22. https://doi.org/10.1146/annurev-ecolsys-102710-145042
Woodcock, B. A., Edwards, M., Redhead, J., Meek, W. R., Nuttall, P., Falk, S., Nowakowski, M. & Pywell, R. F. (2013): Crop flower visitation by honeybees, bumblebees and solitary bees: Behavioural differences and diversity responses to landscape. – Agriculture, Ecosystems & Environment 171: 1–8. https://doi.org/10.1016/j.agee.2013.03.005
http1: Tomozii, B.: Bees of Romania. http://www.beesofromania.ro [accessed: 11/07/2020]
http2: Elveszett Világ Természetvédelmi-, Turista és Barlangász Egyesület, Barót. http://www.vargyasszoros.org/ [accessed: 11/07/2020]
Copyright (c) 2021 Imre Demeter, Adalbert Balog, Zsolt Józan, Miklós Sárospataki
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Manuscripts must be solely the work of the author(s) stated, must not have been previously published elsewhere, and must not be under consideration by another journal. This journal provides immediate open access to its content on the principle that making research freely available to the public supports a greater global exchange of knowledge. The authors retain copyright and publishing rights without restrictions of papers published in Acta Zoologica Academiae Scientiarum Hungaricae.
