Abstract
Climate change presents a serious threat to global biodiversity. Loss of pollinators in particular has major implications, with extirpation of these species potentially leading to severe losses in agriculture and, thus, economic losses. In this study, we forecast the effects of climate change on the distribution of hoverflies in Southeast Europe using species distribution modelling and climate change scenarios for two time-periods. For 2041–2060, 19 analysed species were predicted to increase their areas of occupancy, with the other 25 losing some of their ranges. For 2061–2080, 55% of species were predicted to increase their area of occupancy, while 45% were predicted to experience range decline. In general, range size changes for most species were below 20%, indicating a relatively high resilience of hoverflies to climate change when only environmental variables are considered. Additionally, range-restricted species are not predicted to lose more area proportionally to widespread species. Based on our results, two distributional trends can be established: the predicted gain of species in alpine regions, and future loss of species from lowland areas. Considering that the loss of pollinators from present lowland agricultural areas is predicted and that habitat degradation presents a threat to possible range expansion of hoverflies in the future, developing conservation management strategy for the preservation of these species is crucial. This study represents an important step towards the assessment of the effects of climate changes on hoverflies and can be a valuable asset in creating future conservation plan, thus helping in mitigating potential consequences.
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References
Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J Appl Ecol 43:1223–1232. https://doi.org/10.1111/j.1365-2664.2006.01214.x
Araújo MB, Whittaker RJ, Ladle RJ, Erhard M (2005) Reducing uncertainty in projections of extinction risk from climate change. Glob Ecol Biogeogr 14:529–538. https://doi.org/10.1111/j.1466-822X.2005.00182.x
Beniston M (2006) Mountain weather and climate: a general overview and a focus on climatic change in the Alps. Hydrobiologia 562:3–16. https://doi.org/10.1007/s10750-005-1802-0
Benton TG, Vickery JA, Wilson JD (2003) Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol Evol 18:182–188. https://doi.org/10.1016/S0169-5347(03)
Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect–pollinated plants in Britain and the Netherlands. Science 313:351–354. https://doi.org/10.1126/science.1127863
Bradshaw WE, Holzapfel CM (2006) Evolutionary response to rapid climate change. Science 312:1477–1478. https://doi.org/10.1126/science.1127000/science.1127000
Costion CM, Simpson L, Pert PL, Carlsen MM, Kress WJ, Crayn D (2015) Will tropical mountaintop plant species survive climate change? Identifying key knowledge gaps using species distribution modelling in Australia. Biol Conserv 191:322–330. https://doi.org/10.1016/j.biocon.2015.07.022
Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci USA 106:12788–12793. https://doi.org/10.1073/pnas.0902080106
Donnelly A, Caffarra A, O’Neill BF (2011) A review of climate-driven mismatches between interdependent phenophases in terrestrial and aquatic ecosystems. Int J Biometeorol 55:805–817. https://doi.org/10.1007/s00484-011-0426-5
Dormann CF, Schweiger O, Arens P, Augenstein I, Aviron ST, Bailey D, Baudry J, Billeter R, Bugter R, Bukacek R, Burel F, Cerny M, De Cock R, De Blust G, DeFilippi R, Diekotter T, Dirksen J, Durka W, Edwards PJ, Frenzel M, Hamersky R, Hendrickx F, Herzog F, Klotz S, Koolstra B, Lausch A, Le Coeur D, Liira J, Maelfait JP, Opdam P, Roubalova M, Schermann-Legionnet A, Schermann N, Schmidt T, Smulders MJM, Speelmans M, Simova P, Verboom J, van Wingerden W, Zobel M, Burel F (2008) Prediction uncertainty of environmental change effects on temperate European biodiversity. Ecol Lett 11:235–244. https://doi.org/10.1111/j.1461-0248.2007.01142.x
Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40:677–697. https://doi.org/10.1146/annurev.ecolsys.110308.120159
Elith J, Graham CH, Anderson RP, Dudik M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G, Moritz C, Nakamura M, Nakazawa Y, Overton JM, Peterson AT, Phillips SJ, Richardson K, Scachetti-Pereira R, Schapire RE, Soberon J, Williams S, Wisz MS, Zimmermann NE (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151. https://doi.org/10.1111/j.2006.0906-7590.04596.x
Ferreira MT, Cardoso P, Borges PA, Gabriel R, de Azevedo EB, Reis F, Araújo M, Elias RB (2016) Effects of climate change on the distribution of indigenous species in oceanic islands (Azores). Clim Change 138:603–615. https://doi.org/10.1007/s10584-016-1754-6
Fontaine C, Dajoz I, Meriguet J, Loreau M (2005) Functional diversity of plant-pollinator interaction webs enhances the persistence of plant communities. PLoS Biol 4:e1. https://doi.org/10.1371/journal.pbio.0040001
Franklin J (2009) Mapping species distributions: spatial inference and prediction. Cambridge University Press, Cambridge
García-Robledo C, Kuprewicz EK, Staines CL, Erwin TL, Kress WJ (2016) Limited tolerance by insects to high temperatures across tropical elevational gradients and the implications of global warming for extinction. Proc Natl Acad Sci USA 113:680–685. https://doi.org/10.1073/pnas.1507681113
Gardner JL, Peters A, Kearney MR, Joseph L, Heinsohn R (2011) Declining body size: a third universal response to warming? Trends Ecol Evol 26:285–291. https://doi.org/10.1016/j.tree.2011.03.005
Gibson L, McNeill A, de Tores P, Wayne A, Yates C (2010) Will future climate change threaten a range restricted endemic species, the quokka (Setonix brachyurus), in south west Australia? Biol Conserv 143:2453–2461. https://doi.org/10.1016/j.biocon.2010.06.011
Google Inc. (2013) Google Earth. Mountain View, California, USA. https://www.google.com/earth. Accessed 15 January, 2016
Griffiths HI, Kryštufek B, Reed JM (2004) Balkan biodiversity pattern and process in the European hotspot. Kluwer Academic Press, Dordrect
Hannah L, Midgley GF, Millar D (2002) Climate change-integrated conservation strategies. Glob Ecol Biogeogr 11:485–495. https://doi.org/10.1046/j.1466-822X.2002.00306.x
Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø (2009) How does climate warming affect plant-pollinator interactions? Ecol Lett 12:184–195. https://doi.org/10.1111/j.1461-0248.2008.01269.x
Hendrickx F, Maelfait JP, Van Wingerden W, Schweiger O, Speelmans M, Aviron S, Augenstein I, Billeter R, Bailey D, Bukacek R, Burel F, Diekötter T, Dirksen J, Herzog F, Liira J, Roubalova M, Vandomme V, Bugter R (2007) How landscape structure, land-use intensity and habitat diversity affect components of total arthropod diversity in agricultural landscapes. J Appl Ecol 44:340–351. https://doi.org/10.1111/j.1365-2664.2006.01270.x
Hickling R, Roy DB, Hill JK, Fox R, Thomas CD (2006) The distributions of a wide range of taxonomic groups are expanding polewards. Glob Change Biol 12:450–455. https://doi.org/10.1111/j.1365-2486.2006.01116.x
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. https://doi.org/10.1002/joc.1276
Hijmans RJ, Guarino L, Mathur P (2012) DIVA-GIS, version 7.5. A geographic information system for the analysis of species distribution data. Manual
Hijmans RJ, Phillips S, Leathwick J, Elith J (2016) dismo: species distribution modeling. R package version 1.1–1
Hill JK, Thomas CD, Fox R, Telfer MG, Willis SG, Asher J, Huntley B (2002) Responses of butterflies to twentieth century climate warming: implications for future ranges. Proc Roy Soc Lond B 269:2163–2171. https://doi.org/10.1098/rspb.2002.2134
Hill J, Stellmes M, Udelhoven T, Röder A, Sommer S (2008) Mediterranean desertification and land degradation: mapping related land use change syndromes based on satellite observations. Glob Planet Change 64:146–157. https://doi.org/10.1016/j.gloplacha.2008.10.005
Hughes L (2000) Biological consequences of global warming: is the signal already apparent? Trends Ecol Evol 15:56–61. https://doi.org/10.1016/S0169-5347(99)
IPCC (2014) Fifth assessment report (AR5). Cambridge University Press, Cambridge
Isaac JL, Vanderwal J, Johnson CN, Williams SE (2009) Resistance and resilience: quantifying relative extinction risk in a diverse assemblage of Australian tropical rainforest vertebrates. Divers Distrib 15:280–288. https://doi.org/10.1111/j.1472-4642.2008.00531.x
Jauker F, Bondarenko B, Becker HC, Steffan-Dewenter I (2012) Pollination efficiency of wild bees and hoverflies provided to oilseed rape. Agric For Entomol 14:81–87. https://doi.org/10.1111/j.1461-9563.2011.00541.x
Jovičić S, Burgio G, Diti I, Krašić D, Markov Z, Radenković S, Vujić A (2017) Influence of landscape structure and land use on Merodon and Cheilosia (Diptera: Syrphidae): contrasting responses of two genera. J Insect Conserv. https://doi.org/10.1007/s10841-016-9951-1
Kaloveloni A, Tscheulin T, Vujić A, Radenković S, Petanidou T (2015) Winners and losers of climate change for the genus Merodon (Diptera: Syrphidae) across the Balkan Peninsula. Ecol Model 313:201–211. https://doi.org/10.1016/j.ecolmodel.2015.06.032
Krause CM, Cobb NS, Pennington DD (2015) Range shifts under future scenarios of climate change: dispersal ability matters for Colorado Plateau endemic plants. Nat Areas J 35:428–438. https://doi.org/10.3375/043.035.0306
Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci USA 99:16812–16816. https://doi.org/10.1073/pnas.262413599
Kumar S, Stohlgren TJ (2009) Maxent modeling for predicting suitable habitat for threatened and endangered tree Canacomyrica monticola in New Caledonia. J Ecol Nat Environ 1:094–098
Lenoir J, Gégout JC, Marquet PA, De Ruffray P, Brisse H (2008) A significant upward shift in plant species optimum elevation during the 20th century. Science 320:1768–1771. https://doi.org/10.1126/science.1156831
Liu C, Berry PM, Dawson TP, Pearson RG (2005) Selecting thresholds of occurrence in the prediction of species distributions. Ecography 28:385–393. https://doi.org/10.1111/j.0906-7590.2005.03957.x
Liu C, White M, Newell G (2013) Selecting thresholds for the prediction of species occurrence with presence-only data. J Biogeogr 40:778–789. https://doi.org/10.1111/jbi.12058
Lurgi M, Lopez B, Montoya J (2012) Climate change impacts on body size and food web structure on mountain ecosystems. Philos Trans Roy Soc Lond B 367:3050–3057. https://doi.org/10.1098/rstb.2012.0239
Maggini R, Lehmann A, Kéry M, Schmid H, Beniston M, Jenni L, Zbinden N (2011) Are Swiss birds tracking climate change? Detecting elevational shifts using response curve shapes. Ecol Model 222:21–32. https://doi.org/10.1016/j.ecolmodel.2010.09.010
Matson PA, Parton WJ, Power AG, Swift MJ (1997) Agricultural intensification and ecosystem properties. Science 277:504–509. https://doi.org/10.1126/science.277.5325.504
Merow C, Smith MJ, Silander JA (2013) A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36:1058–1069. https://doi.org/10.1111/j.1600-0587.2013.07872.x
Midgley GF, Hannah L, Millar D, Rutherford MC, Powrie LW (2002) Assessing the vulnerability of species richness to anthropogenic climate change in a biodiversity hotspot. Glob Ecol Biogeogr 11:445–451. https://doi.org/10.1046/j.1466-822X.2002.00307.x
Miličić M, Vujić A, Jurca T, Cardoso P (2017) Designating conservation priorities for Southeast European hoverflies (Diptera: Syrphidae) based on species distribution models and species vulnerability. Insect Conserv Divers 10:354–366. https://doi.org/10.1111/icad.12232
Ortega-Huerta MA, Peterson AT (2008) Modeling ecological niches and predicting geographic distributions: a test of six presence–only methods. Rev Mex Biodiv 79:205–216
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Pearson RG, Raxworthy CJ, Nakamura M, Peterson TA (2007) Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J Biogeogr 34:102–117. https://doi.org/10.1111/j.1365-2699.2006.01594.x
Peñuelas J, Boada M (2003) A global change-induced biome shift in the Montseny Mountains (NE Spain). Glob Change Biol 9:131–140. https://doi.org/10.1046/j.1365-2486.2003.00566.x
Petanidou T, Vokou D, Margaris NS (1991) Panaxia quadripunctaria in the highly touristic Valley of Butterflies (Rhodes, Greece): conservation problems and remedies. Ambio 20:124–128
Petanidou T, Vujić A, Ellis WN (2011) Hoverfly diversity (Diptera: Syrphidae) in a Mediterranean scrub community near Athens, Greece. Ann Soc Entomol 47:168–175. https://doi.org/10.1080/00379271.2011.10697709
Peters GP, Andrew RM, Boden T, Canadell JG, Ciais P, Le Quere C, Marland G, Raupach MR, Wilson C (2013) The challenge to keep global warming below 2 °C. Nat Clim Chang 3:4–6. https://doi.org/10.1038/nclimate1783
Peterson AT (2006) Uses and requirements of ecological niche models and related distributional models. Biodivers Inform 3:59–72. https://doi.org/10.17161/bi.v3i0.29
Peterson AT, Papes M, Eaton M (2007) Transferability and model evaluation in ecological niche modeling: a comparison of GARP and Maxent. Ecography 30:550–560. https://doi.org/10.1111/j.0906-7590.2007.05102.x
Phillips SJ, Dudik M (2008) Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31:161–175. https://doi.org/10.1111/j.0906-7590.2008.5203.x
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Previšić A, Walton C, Kučinić M, Mitrikeski PT, Kerovec M (2009) Pleistocene divergence of Dinaric Drusus endemics (Trichoptera, Limnephilidae) in multiple microrefugia within the Balkan Peninsula. Mol Ecol 18:634–647. https://doi.org/10.1111/j.1365-294X.2008.04046.x
Radenković S, Vujić A, Stahls G, Perez-Banon C, Petanidou T, Šimić S (2011) Three new cryptic species of the genus Merodon Meigen (Diptera: Syrphidae) from the island of Lesvos (Greece). Zootaxa 2735:35–56
Radenković S, Schweiger O, Milić D, Harpke A, Vujić A (2017) Living on the edge: Forecasting the trends in abundance and distribution of the largest hoverfly genus (Diptera: Syrphidae) on the Balkan Peninsula under future climate change. Biol Conserv 212:216–229. https://doi.org/10.1016/j.biocon.2017.06.026
Ristić R, Kašanin-Grubin M, Radić B, Nikić Z, Vasiljević N (2012) Land degradation at the Stara Planina ski resort. Environ Manage 49:580–592. https://doi.org/10.1007/s00267-012-9812-y
Sotherton NW (1998) Land–use changes and the decline of farmland wildlife: an appraisal of the set–aside approach. Biol Conserv 83:259–268. https://doi.org/10.1016/S0006-3207(97)
Stanley DA, Gunning D, Stout JC (2013) Pollinators and pollination of oilseed rape crops (Brassica napus L.) in Ireland: ecological and economic incentives for pollinator conservation. J Insect Conserv 17:1181–1189. https://doi.org/10.1007/s10841-013-9599-z
Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BF, De Siqueira MF, Grainger A, Hannah L, Hughes L (2004) Extinction risk from climate change. Nature 427:145–148
Thompson FC (2013) Family Syrphidae. Systema Dipterorum, version 1.5. http://www.diptera.org. Accessed 28 Sept 2016
Thuiller W, Albert C, Araújo M, Berry P, Cabeza M, Guisan A, Hickler T, Midgley G, Paterson J, Schurr F, Sykes M, Zimmermann N (2008) Predicting global change impacts on plant species’ distributions: future challenges. Perspect Plant Ecol Evol Syst 9:137–152. https://doi.org/10.1016/j.ppees.2007.09.004
Tilman D, Fargione J, Wolff B, D’Antonio C, Dobson A, Howarth R, Schindler D, Schlesinger WH, Simberloff D, Swackhamer D (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284. https://doi.org/10.1126/science.1057544
Turner BL II (1974) Prehistoric intensive agriculture in the Mayan lowlands. Science 185:118–124
Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc Roy Soc Lond B 275:649–659. https://doi.org/10.1098/rspb.2007.0997
Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc Roy Soc Lond B 272:2561–2569. https://doi.org/10.1098/rspb.2005.3356
Vujić A, Šimić S, Radenković S (2001) Endangered species of hoverflies (Diptera: Syrphidae) on the Balkan Peninsula. Acta Entomol Serbica 5:93–105
Vujić A, Radenković S, Stahls G, Ačanski J, Stefanović A, Veselić S, Andrić A, Hayat R (2012) Systematics and taxonomy of the ruficornis group of genus Merodon Meigen (Diptera: Syrphidae). Syst Entomol 37:578–602. https://doi.org/10.1111/j.1365-3113.2012.00631.x
Vujić A, Petanidou T, Tscheulin T, Cardoso P, Radenković S, Stahls G, Baturan Ž, Mijatović G, Rojo S, Perez-Banon C, Devalez J, Andrić A, Jovičić S, Krašić D, Markov Z, Radišić D, Tataris G (2016a) Biogeographical patterns of the genus Merodon Meigen, 1803 (Diptera: Syrphidae) in islands of the eastern Mediterranean and adjacent mainland. Insect Conserv Divers 9:181–191. https://doi.org/10.1111/icad.12156
Vujić A, Radenković S, Nikolić T, Radišić D, Trifunov S, Andrić A, Markov Z, Jovičić S, Mudri Stojnić S, Janković M, Lugonja P (2016b) Prime Hoverfly (Insecta: Diptera: Syrphidae) Areas (PHA) as a conservation tool in Serbia. Biol Conserv 198:22–32. https://doi.org/10.1016/j.biocon.2016.03.032
White AJ, Wratten SD, Berry NA, Weigmann U (1995) Habitat manipulation to enhance biological control of brassica pests by hover flies (Diptera: Syrphidae). J Econ Entomol 88:1171–1176. https://doi.org/10.1093/jee/88.5.1171
Wickramasinghe LP, Harris S, Jones G, Jennings VN (2004) Abundance and species richness of nocturnal insects on organic and conventional farms: effects of agricultural intensification on bat foraging. Conserv Biol 18:1283–1292. https://doi.org/10.1111/j.1523-1739.2004.00152.x
Williams SE, Shoo LP, Isaac JL, Hoffmann AA, Langham G (2008) Towards an integrated framework for assessing the vulnerability of species to climate change. PLoS Biol 6:2621–2626. https://doi.org/10.1371/journal.pbio.0060325
Wilson RJ, Gutiérrez D, Gutiérrez J, Martínez D, Agudo R, Monserrat VJ (2005) Changes to the elevational limits and extent of species ranges associated with climate change. Ecol Lett 8:1138–1146. https://doi.org/10.1111/j.1461-0248.2005.00824.x
Wulff AS, Hollingsworth PM, Ahrends A, Jaffré T, Veillon JM, L’Huillier L, Fogliani B (2013) Conservation priorities in a biodiversity hotspot: analysis of narrow endemic plant species in New Caledonia. PLoS ONE 8:e73371. https://doi.org/10.1371/journal.pone.0073371
Yates CJ, McNeill A, Elith J, Midgley GF (2010) Assessing the impacts of climate change and land transformation on Banksia in the South West Australian Floristic Region. Divers Distrib 16:187–201. https://doi.org/10.1111/j.1472-4642.2009.00623.x
Acknowledgements
We kindly thank John O’Brien for English proofreading and Dr Tamara Jurca for useful comments regarding this paper.
Funding
This work was supported by the Ministry of Education, Science and Technological Development, Republic of Serbia, under Grant Nos. 173002, 43002, Provincial Secretariat for Science and Technological Development under Grant No. 114–457–2173/2011–01 and H2020 Project ANTARES under Grant No. 664387. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Miličić, M., Vujić, A. & Cardoso, P. Effects of climate change on the distribution of hoverfly species (Diptera: Syrphidae) in Southeast Europe. Biodivers Conserv 27, 1173–1187 (2018). https://doi.org/10.1007/s10531-017-1486-6
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DOI: https://doi.org/10.1007/s10531-017-1486-6
Keywords
- Conservation
- Global warming
- Insects
- Endemism
- Species distribution modelling