Abstract
Flower-feeding insects are declining due to the loss of floral resources. The EU Grassland Butterfly Index underlined a decrease in abundance of 39% between 1990 and 2017. In Northwest Europe, land use intensification is the main driver of grassland butterflies' decline. Among the agri-environment schemes in Wallonia (Belgium), wildflower strips are implemented along crops in order to prevent further loss. They provide nectar sources and host plants to butterflies. For more than ten years, butterflies have been monitored in the Walloon flower strips. The strips vegetation was also surveyed to evaluate the larval food potential. In addition, flower visits for nectar were studied in 2020. Between 2010 and 2020, 56 butterfly species (more than 84,000 individuals) were recorded inside the strips and their population showed an overall increase of 82%. We suggest that this increase was due to the strips temporal continuity, combined with a local climate change. Most recorded butterflies belonged to common generalist species but species that are rare, threatened or protected in the region were also observed. Most species had at least one potential host plant inside the strips and we hypothesize that some of the abundant food generalists used them as breeding sites. In 2020, butterflies mainly visited Centaurea jacea, Lotus corniculatus and Medicago sativa for nectar collection. Before the flowering of C. jacea in June, few nectar was available and only a few flower visits were recorded. Thus, flower strips mostly benefit butterflies in summer in terms of nectar supply.
Implications for insect conservation
Our results highlight that the long term application of wildflower strips can be a good instrument to contribute to butterfly conservation in Wallonia. The study of the potential host plants and effective nectar sources provide additional understanding on how butterflies interact with the flower strips.
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Notes
Since 2018, the annual species (Centaurea cyanus, Papaver rhoeas, Papaver dubium) are not in the mix anymore. Heracleum sphondylium, Origanum vulgare, Plantago lanceolata and Prunella vulgaris have been added (Natagriwal 2018).
References
Abrahamczyk S, Wohlgemuth T, Nobis M et al (2020) Shifts in food plant abundance for flower-visiting insects between 1900 and 2017 in the canton of Zurich, Switzerland. Ecol Appl 30:1–11. https://doi.org/10.1002/eap.2138
Aviron S, Herzog F, Klaus I et al (2011) Effects of wildflower strip quality, quantity, and connectivity on butterfly diversity in a Swiss arable landscape. Restor Ecol 19:500–508. https://doi.org/10.1111/j.1526-100X.2010.00649.x
Bakowski M, Boron M (2005) Flower visitation patterns of some species of Lycaenidae (Lepidoptera). Biol Lett 42:13–19
Batáry P, Dicks LV, Kleijn D, Sutherland WJ (2015) The role of agri-environment schemes in conservation and environmental management. Conserv Biol 29:1006–1016. https://doi.org/10.1111/cobi.12536
Baude M, Kunin WE, Boatman ND et al (2016) Historical nectar assessment reveals the fall and rise of floral resources in Britain. Nature 530:85–88. https://doi.org/10.1038/nature16532
Bignal EM (1998) Using an ecological understanding of farmland to reconcile nature conservation requirements, EU agriculture policy and world trade agreements. J Appl Ecol 35:949–954. https://doi.org/10.1111/j.1365-2664.1998.tb00013.x
Boetzl FA, Krauss J, Heinze J et al (2021) A multitaxa assessment of the effectiveness of agri-environmental schemes for biodiversity management. Proc Natl Acad Sci USA 118:e2016038118. https://doi.org/10.1073/pnas.2016038118
Börschig C, Klein AM, von Wehrden H, Krauss J (2013) Traits of butterfly communities change from specialist to generalist characteristics with increasing land-use intensity. Basic Appl Ecol 14:547–554. https://doi.org/10.1016/j.baae.2013.09.002
Bruppacher L, Pellet J, Arlettaz R, Humbert J-Y (2016) Simple modifications of mowing regime promote butterflies in extensively managed meadows: Evidence from field-scale experiments. Biol Conserv 196:196–202. https://doi.org/10.1016/j.biocon.2016.02.018
Buhk C, Oppermann R, Schanowski A et al (2018) Flower strip networks offer promising long term effects on pollinator species richness in intensively cultivated agricultural areas. BMC Ecol 18:1–13. https://doi.org/10.1186/s12898-018-0210-z
Cardoso P, Barton PS, Birkhofer K et al (2020) Scientists’ warning to humanity on insect extinctions. Biol Conserv 242:1–12. https://doi.org/10.1016/j.biocon.2020.108426
Dormann CF, Fruend J, Bluethgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol J 2:7–24
Dover J (2019) The ecology of butterflies and moths in hedgerows and field margins. In: Dover JW (ed) The ecology of hedgerows and field margins. Routledge, Oxford, pp 186–193
Ekroos J, Heliölä J, Kuussaari M (2010) Homogenization of lepidopteran communities in intensively cultivated agricultural landscapes. J Appl Ecol 47:459–467. https://doi.org/10.1111/j.1365-2664.2009.01767.x
Feber RE, Smith H, MacDonald DW (1996) The effects on butterfly abundance of the management of uncropped edges of arable fields. J Appl Ecol 33:1191–1205. https://doi.org/10.2307/2404698
Fichefet V, Barbier Y, Baugnée J-Y et al (2008) Papillons de jour de Wallonie (1985–2007). Service—Public de Wallonie, Direction Générale de l’Agriculture, des Ressources Naturelles et de l’Environnement, Série «Faune-Flore-Habitat», no. 4, Gembloux
Fox R (2012) The decline of moths in Great Britain: a review of possible causes. Insect Conserv Divers 6:5–19. https://doi.org/10.1111/j.1752-4598.2012.00186.x
GBIF.org (2021) GBIF Home Page. https://www.gbif.org. Accessed 18 Feb 2021
Goulson D (2019) The insect apocalypse, and why it matters. Curr Biol 29:R967–R971. https://doi.org/10.1016/j.cub.2019.06.069
Gutiérrez D, León-Cortés JL, Menéndez R et al (2001) Metapopulations of four lepidopteran herbivores on a single host plant, Lotus corniculatus. Ecology 82:1371–1386. https://doi.org/10.1890/0012-9658(2001)082[1371:moflho]2.0.co;2
Haaland C, Bersier L-F (2011) What can sown wildflower strips contribute to butterfly conservation? An example from a Swiss lowland agricultural landscape. J Insect Conserv 15:301–309. https://doi.org/10.1007/s10841-010-9353-8
Haaland C, Gyllin M (2010) Butterflies and bumblebees in greenways and sown wildflower strips in southern Sweden. J Insect Conserv 14:125–132. https://doi.org/10.1007/s10841-009-9232-3
Haaland C, Naisbit RE, Bersier LF (2011) Sown wildflower strips for insect conservation: a review. Insect Conserv Divers 4:60–80. https://doi.org/10.1111/j.1752-4598.2010.00098.x
Habel JC, Segerer A, Ulrich W et al (2016) Butterfly community shifts over two centuries. Conserv Biol 30:754–762. https://doi.org/10.1111/cobi.12656
Habel JC, Ulrich W, Biburger N et al (2019) Agricultural intensification drives butterfly decline. Insect Conserv Divers 12:289–295. https://doi.org/10.1111/icad.12343
Henle K, Alard D, Clitherow J et al (2008) Identifying and managing the conflicts between agriculture and biodiversity conservation in Europe—a review. Agric Ecosyst Environ 124:60–71. https://doi.org/10.1016/j.agee.2007.09.005
Hicks DM, Ouvrard P, Baldock KCR et al (2016) Food for pollinators: quantifying the nectar and pollen resources of urban flower meadows. PLoS ONE 11:1–37. https://doi.org/10.1371/journal.pone.0158117
IEEP (2008) Funding for farmland biodiversity in the EU: Gaining evidence for the EU budget review. IEEP, London
Janz N, Nylin S (1998) Butterflies and plants: a phylogenetic study. Evolution (NY) 52:486–502. https://doi.org/10.1111/j.1558-5646.1998.tb01648.x
Jennersten O (1984) Flower visitation and pollination efficiency of some North European butterflies. Oecologia 63:80–89
Korpela EL, Hyvönen T, Lindgren S, Kuussaari M (2013) Can pollination services, species diversity and conservation be simultaneously promoted by sown wildflower strips on farmland? Agric Ecosyst Environ 179:18–24. https://doi.org/10.1016/j.agee.2013.07.001
Krauss J, Schmitt T, Seitz A et al (2004a) Effects of habitat fragmentation on the genetic structure of the monophagous butterfly Polyommatus coridon along its northern range margin. Mol Ecol 13:311–320. https://doi.org/10.1046/j.1365-294X.2003.02072.x
Krauss J, Steffan-Dewenter I, Tscharntke T (2004b) Landscape occupancy and local population size depends on host plant distribution in the butterfly Cupido minimus. Biol Conserv 120:355–361. https://doi.org/10.1016/j.biocon.2004.03.007
Kuussaari M, Heliölä J, Luoto M, Pöyry J (2007) Determinants of local species richness of diurnal Lepidoptera in boreal agricultural landscapes. Agric Ecosyst Environ 122:366–376. https://doi.org/10.1016/j.agee.2007.02.008
Lafranchis T (2000) Les papillons de jour de France, Belgique et Luxembourg et leurs chenilles. Collection Parthénope, Éditions Biotope, Mèze
Langlois A, Jacquemart AL, Piqueray J (2020) Contribution of extensive farming practices to the supply of floral resources for pollinators. Insects 11:1–19. https://doi.org/10.3390/insects11110818
Leal Filho W, Mandel M, Al-Amin AQ et al (2017) An assessment of the causes and consequences of agricultural land abandonment in Europe. Int J Sustain Dev World Ecol 24:554–560. https://doi.org/10.1080/13504509.2016.1240113
Lebeau J (2015) Nectar resource limitation in agricultural landscapes : effects on behaviour and life-history traits in the meadow brown butterfly (Maniola jurtina). Université catholique de Louvain, Ottignies-Louvain-la-Neuve
Lebeau J, Wesselingh RA, Van Dyck H (2017) Flower use of the butterfly Maniola jurtina in nectar- rich and nectar-poor grasslands: a nectar generalist with a strong preference? Insect Conserv Divers 10:258–270. https://doi.org/10.1111/icad.12222
McCracken ME, Woodcock BA, Lobley M et al (2015) Social and ecological drivers of success in agri-environment schemes: the roles of farmers and environmental context. J Appl Ecol 52:696–705. https://doi.org/10.1111/1365-2664.12412
Merckx T, Pereira HM (2015) Reshaping agri-environmental subsidies: From marginal farming to large-scale rewilding. Basic Appl Ecol 16:95–103. https://doi.org/10.1016/j.baae.2014.12.003
Mevi-Schütz J, Erhardt A (2005) Amino acids in nectar enhance butterfly fecundity: a long-awaited link. Am Nat 165:411–419. https://doi.org/10.1086/429150
Montgomery GA, Dunn RR, Fox R et al (2020) Is the insect apocalypse upon us? How to find out. Biol Conserv 241:1–6. https://doi.org/10.1016/j.biocon.2019.108327
Natagriwal (2018) Vade-mecum relatif à l’avis d’expert dans le cadre des Méthodes Agro-Environnementales et Climatiques (MAEC): Bandes et parcelles aménagées. Méthodes ciblées 7 et 8
Noordijk J, Delille K, Schaffers AP, Sýkora KV (2009) Optimizing grassland management for flower-visiting insects in roadside verges. Biol Conserv 142:2097–2103. https://doi.org/10.1016/j.biocon.2009.04.009
Öckinger E, Bergman KO, Franzén M et al (2012) The landscape matrix modifies the effect of habitat fragmentation in grassland butterflies. Landsc Ecol 27:121–131. https://doi.org/10.1007/s10980-011-9686-z
Ouvrard P, Jacquemart A (2018) Agri-environment schemes targeting farmland bird populations also provide food for pollinating insects. Agric for Entomol 20:558–574. https://doi.org/10.1111/afe.12289
Ouvrard P, Jacquemart A-L, Transon J (2018) Flower-strip agri-environment schemes provide diverse and valuable summer flower resources for pollinating insects. Biodivers Conserv 27:2193–2216. https://doi.org/10.1007/s10531-018-1531-0
Piqueray J, Gilliaux V, Decruyenaere V et al (2019) Management of grassland-like wildflower strips sown on nutrient-rich arable soils: the role of grass density and mowing regime. Environ Manage 63:647–657. https://doi.org/10.1007/s00267-019-01153-y
Pollard E (1988) Temperature, rainfall and butterfly numbers. J Appl Ecol 25:819–828
Pollard E, Yates TJ (1993) Monitoring butterflies for ecology and conservation: the British butterfly monitoring scheme. Chapman & Hall, London
Pollard E, Greatorex-Davies JN, Thomas JA (1997) Drought reduces breeding success of the butterfly Aglais urticae. Ecol Entomol 22:315–318. https://doi.org/10.1046/j.1365-2311.1997.00064.x
Pywell RF, Meek WR, Hulmes L et al (2011) Management to enhance pollen and nectar resources for bumblebees and butterflies within intensively farmed landscapes. J Insect Conserv 15:853–864. https://doi.org/10.1007/s10841-011-9383-x
RMI (2021) Weather in Belgium—RMI. https://www.meteo.be/en/belgium. Accessed 22 Dec 2020
Roy DB, Rothery P, Moss D et al (2001) Butterfly numbers and weather: predicting historical trends in abundance and the future effects of climate change. J Anim Ecol 70:201–217. https://doi.org/10.1046/j.1365-2656.2001.00480.x
RStudio Team (2019) RStudio: Integrated Development for R. RStudio Inc, Boston
Rusterholz HP, Erhardt A (1997) Preferences for nectar sugars in the peacock butterfly, Inachis io. Ecol Entomol 22:220–224. https://doi.org/10.1046/j.1365-2311.1997.t01-1-00047.x
Rusterholz HP, Erhardt A (2000) Can nectar properties explain sex-specific flower preferences in the Adonis Blue butterfly Lysandra bellargus? Ecol Entomol 25:81–90. https://doi.org/10.1046/j.1365-2311.2000.00233.x
Scheper J, Holzschuh A, Kuussaari M et al (2013) Environmental factors driving the effectiveness of European agri-environmental measures in mitigating pollinator loss - a meta-analysis. Ecol Lett 16:912–920. https://doi.org/10.1111/ele.12128
Settele J, Kudrna O, Harpke A et al (2008) Climatic risk atlas of European butterflies. Pensoft Publishers, Sofia
Sevilleja CG, van Swaay CAM, Bourn N et al (2019) Butterfly transect counts: manual to monitor butterflies. Report VS2019.016, Butterfly Conservation Europe & De Vlinderstichting/Dutch Butterfly Conservation, Wageningen
Sparks TH, Roy DB, Dennis RLH (2005) The influence of temperature on migration of Lepidoptera into Britain. Glob Chang Biol 11:507–514. https://doi.org/10.1111/j.1365-2486.2005.00910.x
Stoate C, Báldi A, Beja P et al (2009) Ecological impacts of early 21st century agricultural change in Europe—a review. J Environ Manage 91:22–46. https://doi.org/10.1016/j.jenvman.2009.07.005
Sutter L, Jeanneret P, Bartual AM et al (2017) Enhancing plant diversity in agricultural landscapes promotes both rare bees and dominant crop-pollinating bees through complementary increase in key floral resources. J Appl Ecol 54:1856–1864. https://doi.org/10.1111/1365-2664.12907
Szigeti V, Vajna F, Kőrösi Á, Kis J (2020) Are all butterflies equal? Population-wise proboscis length variation predicts flower choice in a butterfly. Anim Behav 163:135–143. https://doi.org/10.1016/j.anbehav.2020.03.008
Thomas JA (2005) Monitoring change in the abundance and distribution of insects using butterflies and other indicator groups. Philos Trans R Soc B Biol Sci 360:339–357. https://doi.org/10.1098/rstb.2004.1585
Thomas JA (2016) Butterfly communities under threat. Science (80–) 353:216–218. https://doi.org/10.1126/science.aaf8838
Thomas JA, Simcox DJ, Hovestadt T (2011) Evidence based conservation of butterflies. J Insect Conserv 15:241–258. https://doi.org/10.1007/s10841-010-9341-z
Tiple AD, Khurad AM, Dennis RLH (2009) Adult butterfly feeding-nectar flower associations: constraints of taxonomic affiliation, butterfly, and nectar flower morphology. J Nat Hist 43:855–884. https://doi.org/10.1080/00222930802610568
Tudor O, Dennis RLH, Greatorex-Davies JN, Sparks TH (2004) Flower preferences of woodland butterflies in the UK: nectaring specialists are species of conservation concern. Biol Conserv 119:397–403. https://doi.org/10.1016/j.biocon.2004.01.002
Van Dyck H, Van Strien AJ, Maes D, Van Swaay CAM (2009) Declines in common, widespread butterflies in a landscape under intense human use. Conserv Biol 23:957–965. https://doi.org/10.1111/j.1523-1739.2009.01175.x
Van Swaay CAM, Van Strien A (2005) Using butterfly monitoring data to develop a European grassland butterfly indicator. In: Kühn E, Feldmann R, Thomas JA, Settele J (eds) Studies on the ecology and conservation of butterflies in Europe, vol 1. General concepts and case studies. Pensoft Publishers, Sofia (Bulgaria), pp 106–108
Van Swaay CAM, Warren M (1999) Red data book of European butterflies (Rhopalocera), Nature and Environment No. 99. Council of Europe, Strasbourg
Van Swaay CAM, Warren M, Loïs G (2006) Biotope use and trends of European butterflies. J Insect Conserv 10:189–209. https://doi.org/10.1007/s10841-006-6293-4
Van Swaay CAM, Van Strien A, Aghababyan K et al (2016) The European Butterfly Indicator for Grassland species: 1990–2015. De Vlinderstichting, Wageningen
Van Swaay CAM, Dennis EB, Schmucki R et al (2019) The EU Butterfly Indicator for Grassland species: 1990–2017. Technical Report
Van Swaay CAM, Bos G, van Grunsven R et al (2020) Vlinders, libellen en hommels geteld. Jaarverslag 2019. Technical Report
Warren MS, Maes D, van Swaay CAM et al (2021) The decline of butterflies in Europe: problems, significance, and possible solutions. Proc Natl Acad Sci USA 118:1–10. https://doi.org/10.1073/pnas.2002551117
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York
Wiklund C (1984) Egg-laying patterns in butterflies in relation to their phenology and the visual apparency and abundance of their host plants. Oecologia 63:23–29
Wiklund C (1982) Generalist versus specialist utilization of host plants among butterflies. In: Visser JH, Minks AK (eds) Proceedings of the 5th international symposium on insect–plant relationships, Wageningen, Netherlands, pp 181–191
Wix N, Reich M, Schaarschmidt F (2019) Butterfly richness and abundance in flower strips and field margins: the role of local habitat quality and landscape context. Heliyon 5:1–12. https://doi.org/10.1016/j.heliyon.2019.e01636
Yang LH, Gratton C (2014) Insects as drivers of ecosystem processes. Curr Opin Insect Sci 2:26–32. https://doi.org/10.1016/j.cois.2014.06.004
Zingg S, Ritschard E, Arlettaz R, Humbert J-Y (2019) Increasing the proportion and quality of land under agri-environment schemes promotes birds and butterflies at the landscape scale. Biol Conserv 231:39–48. https://doi.org/10.1016/j.biocon.2018.12.022
Acknowledgements
We thank Marie Legast and Valentin Gilliaux for their contribution to the vegetation data collection. We also acknowledge the Belgian Royal Meteorological Institute for allowing us to use their data.
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Natagriwal is a non-profit association funded by the Walloon Government.
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Julien Piqueray and Claude Dopagne conceived the ideas and designed the methodology. All authors contributed to the field investigation (vegetation survey: J. Piqueray; butterfly annual monitoring: C. Dopagne; butterfly foraging observations: Alyssa Kolkman). A. Kolkman analysed the data and wrote the draft with the noticable help of the two other autors. All authors read and approved the final manuscript.
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10841_2021_347_MOESM3_ESM.xlsx
Supplementary data S3 List of plants species recorded in the flower strips (2010-2020), sorted by family. For each species, we specified the percentage of strips where the species has been observed and if it is a potential nectar source and/or host plant for recorded butterfly species. Species in bold are included in the sown mix (XLSX 20 kb)
10841_2021_347_MOESM4_ESM.pdf
Supplementary data S4 Trends of some of the most abundant species (note: y-axis scale differs between plots) (PDF 347 kb)
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Kolkman, A., Dopagne, C. & Piqueray, J. Sown wildflower strips offer promising long term results for butterfly conservation. J Insect Conserv 26, 387–400 (2022). https://doi.org/10.1007/s10841-021-00347-2
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DOI: https://doi.org/10.1007/s10841-021-00347-2