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Biodiversity and Conservation

, Volume 28, Issue 6, pp 1343–1360 | Cite as

Mitigating the precipitous decline of terrestrial European insects: Requirements for a new strategy

  • Jan Christian HabelEmail author
  • Michael J. Samways
  • Thomas Schmitt
Review Paper

Abstract

Severe decline in terrestrial insect species richness, abundance, flying biomass, and local extinctions across Europe are cause for alarm. Here, we summarize this decline, and identify species affected most. We then focus on the species that might respond best to mitigation measures relative to their traits. We review apparent drivers of decline, and critically reflect on strengths and weaknesses of existing studies, while emphasising their general significance. Generality of recent scientific findings on insect decline have shortcomings, as results have been based on irregular time series of insect inventories, and have been carried out on restricted species sets, or have been undertaken only in a particular geographical area. Agricultural intensification is the main driver of recent terrestrial insect decline, through habitat loss, reduced functional connectivity, overly intense management, nitrogen influx, and use of other fertilisers, as well as application of harmful pesticides. However, there are also supplementary and adversely synergistic factors especially climate change, increasingly intense urbanisation, and associated increase in traffic volume, artificial lighting and environmental pollution. Despite these various synergistic impacts, there are mitigating factors that can be implemented to stem the precipitous insect decline. Science can provide the fundamental information on potential synergistic and antagonistic mechanisms of multiple drivers of insect decline, while implementation research can help develop alternative approaches to agriculture and forestry to mitigate impacts on insects. We argue for more nature-friendly land-use practices to re-establish Europe’s insect diversity.

Keywords

Biodiversity crisis Insect decline Species richness Abundance Agricultural intensification Habitat fragmentation Habitat degradation Pesticides Climate change Insect conservation 

Notes

Acknowledgements

We thank two anonymous referees for helpful comments to improve our article.

References

  1. Augenstein B, Ulrich W, Habel JC (2012) Directional temporal shifts in community structure of butterflies and ground beetles in fragmented oligotrophic grasslands of Central Europe. Basic Appl Ecol 13:715–724Google Scholar
  2. Baur B, Cremene C, Groza G, Rakosy L, Schileyko AA, Baur A, Stoll P, Erhardt A (2006) Effects of abandonment of subalpine hay meadows on plant and invertebrate diversity in Transylvania, Romania. Biol Conserv 132:261–273Google Scholar
  3. Bianchi FJJA, Booij CJH, Tscharntke T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc Roy Soc B 273:1715–1727Google Scholar
  4. Biesmeijer JC, Roberts SPM, Reemer M, Ohlemuller 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 313:351–354Google Scholar
  5. Birkhofer K, Smith HG, Weisser WW, Wolters V, Gossner MM (2015) Land-use effects on the functional distinctness of arthropod communities. Ecography 38:889–900Google Scholar
  6. Brittain CA, Vighi M, Bommarco R, Settele J, Potts SG (2010) Impacts of a pesticide on pollinator species richness at different spatial scales. Basic Appl Ecol 11:106–115Google Scholar
  7. Brooks DR, Bater JE, Clark SJ, Montoth DJ, Andrews C, Corbett SJ, Beaumont DA, Chapman JW (2012) Large carabid beetle declines in a United Kingdom monitoring network increases evidence for a widespread loss of insect biodiversity. J Appl Ecol 49:1009–1019Google Scholar
  8. Cleary DFR, Boyle TJB, Setyawati T, Anggraeni CD, Van Loon EE, Menken SBJ (2007) Bird species and traits associated with logged and unlogged forest in Borneo. Ecol Appl 17:1184–1197Google Scholar
  9. Conrad KF, Woiwod IP, Parsons M, Fox R, Warren MS (2004) Long-term population trends in widespread British moths. J Insect Conserv 8:119–136Google Scholar
  10. Conrad KF, Warren MS, Fox R, Parsons MS, Woiwod IP (2006) Rapid declines of common, widespread British moths provide evidence of an insect biodiversity crisis. Biol Cons 132:279–291Google Scholar
  11. Crowder DW, Northfield TD, Gomulkiewicz R, Snyder WE (2012) Conserving and promoting evenness: organic farming and fire-based wildland management case studies. Ecology 93:2001–2007Google Scholar
  12. Cunningham SA, Attwood SJ, Bawa KS, Benton TG, Broadhurst LM, Didham RK, McIntyre S, Perfecto I, Samways MJ, Tscharntke T, Vandermeer J, Villard M-A, Young AG, Lindenmayer DB (2013) To close the yield-gap while saving biodiversity will require multiple locally relevant strategies. Agri Ecosyst Environ 173:20–27Google Scholar
  13. De Jong FMW, De Snoo GR, Van de Zande JC (2008) Estimated nationwide effects of pesticide spray drift on terrestrial habitats in the Netherlands. J Env Manag 87:721–730Google Scholar
  14. Dempster JP (1975) Animal population ecology. Academic Press, LondonGoogle Scholar
  15. Den Boer PJ (1985) Fluctuations of density and survival of carabid populations. Oecologia 67:22–330Google Scholar
  16. Dennis RLH, Eales HT (1997) Patch occupancy in Coenonympha tullia (Muller, 1764) (Lepidoptera: Satyrinae): habitat quality matters as much as patch size and isolation. J Insect Conserv 1:167–176Google Scholar
  17. Desender K, Dekoninck W, Dufrêne M, Maes D (2010) Changes in the distribution of carabid beetles in Belgium revisited: have we halted the diversity loss? Biol Conserv 143:1549–1557Google Scholar
  18. Desneux N, Decourtye A, Delpuech J-M (2007) The sub-lethal effects of pesticides on beneficial arthropods. Ann Rev Entomol 52:81–106Google Scholar
  19. Ebert G, Rennwald E (1991) Die Schmetterlinge Baden-Württembergs. Band 1 and 2. Ulmer, StuttgartGoogle Scholar
  20. Eskildsen A, Carvalheiro LG, Kissling WD, Biesmeijer JC, Schweiger O, Høye TT (2015) Ecological specialization matters: long-term trends in butterfly species richness and assemblage composition depend on multiple functional traits. Div. Distrib 21:792–802Google Scholar
  21. European Community (2015) Natura 2000 Barometer. Natura 2000 Newsletter, 37, 8–9Google Scholar
  22. European Economic Community (1992) Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. Off J L206:7–50Google Scholar
  23. Filz KJ, Engler JO, Stoffels J, Weitzel M, Schmitt T (2013) Missing the target? A critical view on butterfly conservation efforts on calcareous grasslands in south-western Germany. Biodiv Conserv 22:2223–2241Google Scholar
  24. Fox R (2013) The decline of moths in great Britain: a review of possible causes. Insect Conserv Divers 6:5–19Google Scholar
  25. Freemark K, Boutin C (1995) Impacts of agricultural herbicide use on terrestrial wildlife in temperate landscapes: review with special reference to North America. Agric Ecosyst Environ 52:67–91Google Scholar
  26. Frost KR, Ware GW (1970) Pesticide drift from aerial and ground applications. Agric Eng 51:460–464Google Scholar
  27. Gabriel D, Sait SM, Kunin WE, Benton TG (2013) Food production vs. biodiversity: comparing organic and conventional agriculture. J Appl Ecol 50:355–364Google Scholar
  28. Gangwani K, Landin J (2018) The decline of insect representation in biology textbooks over time. Am Entomol 64:252–257Google Scholar
  29. Garibaldi LA, Pérez-Méndez N, Garratt MPD, Gemmill-Herren B, Miguez FE, Dicks LV (2019) Policies for ecological intensification of crop production. Trends Ecol Evol.  https://doi.org/10.1016/j.tree.2019.01.003 Google Scholar
  30. Geiger F, Bengtsson J, Berendse F, Weisser WW, Emmerson M, Morales MB, Ceryngier P, Liira J, Tscharntke T, Winqvist C, Eggers S, Bommarco R, Pärt T, Bretagnolle V, Plantegenest M, Clement LW, Dennis C, Palmer C, Oñate JJ, Guerrero I, Hawro V, Aavik T, Thies C, Flohre A, Hänke S, Fischer C, Goedhart PW, Inchausti P (2010) Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl Ecol 11:97–105Google Scholar
  31. Gelbrecht J, Clemens F, Kretschmer H, Landeck I, Reinhardt R, Richert A, Schmitz O, Rämisch F (2016) Die Tagfalter von Brandenburg und Berlin (Lepidoptera: Rhopalocera und Hesperiidae). N&L 3/4Google Scholar
  32. Gómez-Rodriguez C, Baselga A (2018) Variation among European beetle taxa in pattern of distance decay of similarity suggests a major role of dispersal processes. Ecography 14:1825–1834Google Scholar
  33. Gossner MM, Müller J (2011) The influence of species traits and q-metrics on scale-specific β-diversity components of arthropod communities of temperate forests. Landscape Ecol 26:411–424Google Scholar
  34. Gossner MM, Lachat T, Brunet J, Isacsson G, Bouget C, Brustel H, Brandl R, Weisser WW, Müller J (2013) Current near-to-nature forest management effects on functional trait composition of saproxylic beetles in beech forests. Conserv Biol 27:605–614Google Scholar
  35. Gossner MM, Lewinsohn TM, Kahl T, Grassein F, Boch S, Prati D, Birkhofer K, Renner SC, Sikorski J, Wubet T, Arndt H, Baumgartner V, Blaser S, Blüthgen N, Börschig C, Buscot F, Diekötter T, Jorge LR, Jung K, Keyel AC, Klein A-M, Klemmer S, Krauss J, Lange M, Müller J, Overmann J, Pašalić E, Penone C, Perović DJ, Purschke O, Schall P, Socher SA, Sonnemann I, Tschapka M, Tscharntke T, Türke M, Venter PC, Weiner CN, Werner M, Wolters V, Wurst S, Westphal C, Fischer M, Weisser WW, Allen E (2016) Land-use intensification causes multitrophic homogenization of grassland communities. Nature 540:266–269Google Scholar
  36. Guenat S, Kunin WE, Dougill AJ, Dallimer M (2019) Effects of urbanisation and management practices on pollinators in tropical Africa. J Appl Ecol 56:214–224Google Scholar
  37. Habel JC, Schmitt T (2018) Vanishing of the common species: empty habitats and the role of genetic diversity. Biol Conserv 218:211–216Google Scholar
  38. Habel JC, Rödder D, Schmitt T, Nève G (2011) Global warming will affect the genetic diversity and uniqueness of Lycaena helle populations. Glob Change Biol 17:194–205Google Scholar
  39. Habel JC, Braun J, Fischer C, Weisser WW, Gossner MM (2015) Population restoration of the nocturnal bird Athene noctua in Western Europe: an example of evidence based species conservation. Biodiv Conserv 24:1743–1753Google Scholar
  40. Habel JC, Segerer A, Ulrich W, Torchyk O, Weisser WW, Schmitt T (2016) Butterfly community shifts over 2 centuries. Conserv Biol 30:754–762Google Scholar
  41. Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N, Schwan H, Stenmans W, Müller A, Sumser H, Hörren T, Goulson D, Kroon H (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12:e0185809Google Scholar
  42. Hanski I (1999) Habitat connectivity, habitat continuity, and metapopulations in dynamic landscapes. Oikos 87:209–219Google Scholar
  43. Hanski I, Kuussaari M, Nieminen M (1994) Metapopulation structure and migration in the butterfly Melitaea cinxia. Ecology 75:747–762Google Scholar
  44. Haslberger A, Segerer AH (2016) Systematische, revidierte und kommentierte Checkliste der Schmetterlinge Bayerns (Insecta: Lepidoptera). Mitteilungen der Münchner Entomologischen GesellschaftGoogle Scholar
  45. Henry M, Béguin M, Requier F, Rollin O, Odoux J-F, Aupinel P, Aptel J, Tchamitchian S, Decourtye A (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336:348–350Google Scholar
  46. Hewitt JE, Thrush SF, Ellingsen KE (2016) The role of rare species identities in spatial patterns of species richness and conservation. Conserv Biol 30:10180–11088Google Scholar
  47. Hochkirch A, Schmitt T, Beninde J, Hiery M, Kinitz T, Kirschey J, Matenaar D, Rohde K, Stoefen A, Wagner N, Zink A, Lötters S, Veith M, Proelss A (2013) Europe needs a new vision for a Natura 2020 network. Conserv Lett 6:462–467Google Scholar
  48. Isaac NJ, Strien AJ, August TA, Zeeuw MP, Roy DB (2014) Statistics for citizen science: extracting signals of change from noisy ecological data. Methods Ecol Evol 5:1052–1060Google Scholar
  49. Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS, Reich PB, Scherer-Lorenzen M, Schmid B, Tilman D, van Ruijven J et al (2011) High plant diversity is needed to maintain ecosystem services. Nature 477:199–202Google Scholar
  50. Iserhard CA, Duarte L, Seraphim N, Freitas AVL (2019) How urbanization affects multiple dimensions of biodiversity in tropical butterfly assemblages. Biodiv Conserv 28:621–638Google Scholar
  51. IUCN (2018) The IUCN red list of threatened species. IUCN, CambridgeGoogle Scholar
  52. Johnston A, Fink D, Hochachka WM, Kelling S (2018) Estimates of observer expertise improve species distributions from citizen science data. Methods Ecol Evol 9:88–97Google Scholar
  53. Kadlec T, Vrba P, Kepka P, Schmitt T, Konvicka M (2010) Tracking the decline of the once-common butterfly: delayed oviposition, demography and population genetics in the hermit Chazara briseis. Anim Conserv 13:172–183Google Scholar
  54. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc Roy Soc B 274:303–313Google Scholar
  55. Knowler JT, Flint PWH, Flint S (2016) Trichoptera (Caddisflies) caught by the Rothamsted light trap at Rowardennan, loch Lomondside throughout 2009. Glasg Nat 26:35–42Google Scholar
  56. Kremen C, Miles A (2012) Ecosystem services in biologically diversified versus conventional farming systems: benefits, externalities, and trade-offs. Ecol Soc 17:40Google Scholar
  57. Kunin WE, Harte J, He F, Hui C, Jobe RT, Ostling A, Polce C, Šizling A, Smith AB, Smith K, Smart SM, Storch D, Tjørve E, Ugland K-I, Ulrich W, Varma V (2018) Upscaling biodiversity: estimating the species-area relationship from small samples. Ecol Monogr 9:95Google Scholar
  58. Kuussaari M, Heliölä J, Pöyry J, Saarinen K (2007) Contrasting trends of butterfly species preferring semi-natural grasslands, field margins and forest edges in northern Europe. J Insect Conserv 11:351–366Google Scholar
  59. Lichtenberg EM, Kennedy CM, Kremen C, Batáry P et al (2017) A global synthesis of the effects of diversified farming systems on arthropod diversity within fields and across agricultural landscapes. Glob Change Biol 23:4946–4957Google Scholar
  60. Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323Google Scholar
  61. Lyons SK, Amatangelo KL, Behrensmeyer AK, Bercovici A, Blois JL, Davis M, DiMichele WA, Du A, Eronen JT, Faith JT, Graves GR, Jud N, Labandeira C, Looy CV, McGill B, Miller JH, Patterson D, Pineda-Munoz S, Potts R, Riddle B, Terry R, Tóth A, Ulrich W, Villaseñor A, Wing S, Anderson H, Anderson J, Waller D, Gotelli NJ (2016) Holocene shifts in the assembly of plant and animal communities implicate human impacts. Nature 529:80–83Google Scholar
  62. Martin AE, Graham SL, Henry M, Pervin E, Fahrig L (2018) Flying insect abundance declines with increasing road traffic. Insect Conserv Divers 11:608–613Google Scholar
  63. Mayfield MM, Bonser SP, Morgan JW, Aubin I, McNamara S, Vesk PA (2010) What does species richness tell us about functional trait diversity? Predictions and evidence for responses of species and functional trait diversity to land-use change. Glob Ecol Biogeogr 19:423–431Google Scholar
  64. McGill BJ, Dornelas M, Gotelli NJ, Magurran AE (2015) Fifteen forms of biodiversity trend in the Anthropocene. Trends Ecol Evol 30:104–113Google Scholar
  65. McLaughlin JF, Hellmann JJ, Boggs CL, Ehrlich PR (2002) Climate change hastens population extinctions. PNAS 30:6070–6074Google Scholar
  66. Mehr M, Brandl R, Hothorn T, Dziock F, Förster B, Müller J (2011) Land use is more important than climate for species richness and composition of bat assemblages on a regional scale. Mamm Biol 76:451–460Google Scholar
  67. Morris MG, Clarke RT, Rispin WE (2005) The success of a rotational grazing system in conserving the diversity of chalk grassland Auchenorrhyncha. J Insect Conserv 9:363–374Google Scholar
  68. Mouchet MA, Villeger S, Mason NWH, Mouillot D (2010) Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct Ecol 24:867–876Google Scholar
  69. Müller J, Brunet J, Brin A, Bouget C, Brustel H, Bussler H, Förster B, Gunnar I, Köhler F, Thibault L, Gossner MM (2012) Implications from large-scale spatial diversity patterns of saproxylic beetles for the conservation of European Beech forests. Insect Conserv Div 6:162–169Google Scholar
  70. Myers JH (2018) Population cycles: generalities, exceptions and remaining mysteries. Proc R Soc B 285:20172841Google Scholar
  71. Noordijk J, Schaffers AP, Heijerman T, Boer P, Gleichman M, Sýkora KV (2010) Effects of vegetation management by mowing on ground-dwelling arthropods. Ecol Eng 36:740–750Google Scholar
  72. Paniatowski D, Hertenstein F, Raude N, Rottbehüt K, Nickel H, Fartmann T (2018) The invasion of Bromus erectus alters species diversity of vascular plants and leafhoppers in calcareous grasslands. Insect Conserv Div 11:578–586Google Scholar
  73. Perović D, Gámez-Virués S, Börschig C, Klein A-M, Krauss J, Steckel J, Rothenwöhrer C, Erasmi S, Erasmi S, Tscharntke T, Westphal C (2015) Configurational landscape heterogeneity shapes functional community composition of grassland butterflies. J Appl Ecol 52:505–513Google Scholar
  74. Ponisio LC, M’Gonigle LK, Mace KC, Palomino J, de Valpine P, Kremen C (2015) Diversification practices reduce organic to conventional yield gap. Proc R Soc B 282(1799):20141396Google Scholar
  75. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353Google Scholar
  76. Puech C, Baudry J, Joannon A, Poggi S, Aviron S (2014) Organic vs. conventional farming dichotomy: does it make sense for natural enemies? Agricult Ecosys Env 194:48–57Google Scholar
  77. Rada S, Schweiger O, Harpke A, Kühn E, Kuras T, Settele J, Musche M (2019) Protected areas do not mitigate biodiversity declines: A case study on butterflies. Div Distrib.  https://doi.org/10.1111/ddi.12854 Google Scholar
  78. Ranjha MH, Irmler U (2014) Movement of carabids from grassy strips to crop land in organic agriculture. J Insect Conserv 18:457–467Google Scholar
  79. Reichholf JH (2005) Zweimal zwei Brennnesselfalter: unterschiedliche Bestandsentwicklungen von Inachis io (Linnaeus, 1758), Aglais urticae (Linnaeus, 1758), Eurrhypara hortulata (Linnaeus, 1758) und Pleurotypa ruralis (Scopoli, 1763) bei gleichen Raupenfutterpflanzen (Lepidoptera, Nymphalidae et Pyralidae). Atlanta 36:449–456Google Scholar
  80. Reichholf JH (2006) Starker Rückgang der Auenwald-Winkeleule Mesogona oxalina Hübner, 1803, im niederbayerischen Inntal (Lepidoptera, Noctuidae). Entomologische Nachrichten und Berichte 225–228Google Scholar
  81. Reichholf JH (2008) Starker Rückgang des Rotrandspanners Calothysanis amata L. am unteren Inn. Mitteilungen der Zoologischen Gesellschaft Braunau 283–287Google Scholar
  82. Reidsma P, Tekelenburg T, van den Berg M, Alkemade R (2006) Impacts of land-use change on biodiversity: an assessment of agricultural biodiversity in the European Union. Agric Ecosyst Environ 114:86–102Google Scholar
  83. Rundlöf M, Nilsson H, Smith HG (2008) Interacting effects of farming practice and landscape context on bumble bees. Biol Conserv 141:417–426Google Scholar
  84. Rundlöf M, Andersson GKS, Bommarco R, Fries I, Hederström V, Herbertsson L, Jonsson O, Klatt BK, Pedersen TR, Yourstone J, Smith HG (2015) Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521:77–80Google Scholar
  85. Samways MJ (2007) Rescuing the extinction of experience. Biodiv Conserv 16:1995–1997Google Scholar
  86. Samways MJ (2018) Insect conservation for the twenty-first century. In: Shah MM, Sharif U (eds) Insect science-diversity, conservation and nutrition. IntechOpen.  https://doi.org/10.5772/intechopen.73864
  87. Samways MJ (2019) Insect conservation: a global synthesis. CABI, WallingfordGoogle Scholar
  88. Samways MJ, McGeoch MA, New TR (2010) Insect conservation: approaches and methods. Oxford University Press, OxfordGoogle Scholar
  89. Sánchez-Bayo F, Wyckhuys KAG (2019) Worldwide decline of the entomofauna: a review of its drivers. Biol Conserv 232:8–27Google Scholar
  90. Saunders M (2017) Insects in decline: why we need more studies like this. https://ecologyisnotadirtyword.com/2017/10/20/insects-in-decline-why-we-need-more-studies-like-this/. Accessed 31 8, 2018
  91. Saunders ME, Roger E, Geary WL, Meredith F, Welbourne DJ et al (2018) Citizen science in schools: engaging students in research on urban habitat for pollinators. Austral Ecol 43:635–642Google Scholar
  92. Schneider MK, Lüscher G, Jeanneret P, Arndorfer M, Ammari Y et al (2014) Gains to species diversity in organically farmed fields are not propagated at the farm level. Nat Commun 5:4151–4158Google Scholar
  93. Schowalter TD (2011) Insect ecology: an ecosystem approach. Academic Press, San DiegoGoogle Scholar
  94. Segerer A, Neumayr L, Neuner A (1987) Interessante „Makrolepidopteren“-Funde aus Regensburg und Umgebung (1). Galathea 33:2–23Google Scholar
  95. Settele J, Kudrna O, Harpke A, Kuhn I, van Swaay C, Vervonik R, Warren M, Wiemers M, Hanspach J, Hickler T, Kuhn E, van Halder I, Veling K, Vliegenthart A, Wynhoff I, Schweiger O (2008) Climatic risk atlas of European butterflies. BioRisk 1:1–710Google Scholar
  96. Seufert V, Ramankutty N, Foley J (2012) Comparing the yields of organic and conventional agriculture. Nature 485:22–232Google Scholar
  97. Shortall CR, Moore A, Smith E, Hall MJ, Woiwod IP, Harrington R (2009) Long-term changes in the abundance of flying insects. Insect Cons Div 2:251–260Google Scholar
  98. Simaika JP, Samways MJ (2018) Insect conservation psychology. J Insect Conserv 22:1133–1143Google Scholar
  99. Simons NK, Weisser WW, Gossner MM (2016) Multi-taxa approach shows consistent shifts in arthropod functional traits along grassland land-use intensity gradient. Ecology 97:754–764Google Scholar
  100. Simons NK, Lewinsohn T, Blüthgen N, Buscot F, Boch S, Daniel R, Gossner MM, Jung K, Kaiser K, Müller J, Prati D, Renner SC, Socher SA, Sonnemann I, Weiner CN, Werner M, Wubet T, Wurst S, Weisser WW (2017) Contrasting effects of grassland management modes on species-abundance distributions of multiple groups. Agric Ecosyst Environ 237:143–153Google Scholar
  101. Siviter H, Brown MJF, Leadbeater E (2018) Sulfoxaflor exposure reduces bumblebee reproductive success. Nature 561:109–112Google Scholar
  102. Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1878Google Scholar
  103. Storkey J, MacDonald AJ, Bell JR, Clark IM, Gregory AS, Hawkin NJ, Hirsch PR, Todman LC, Whitmore AP (2016) Chapter one—the unique contribution of Rothamsted to ecological research at large temporal scales. Adv Ecol Res 55:3–42Google Scholar
  104. Swinton AH (1880) Insect variety: its propagation and distribution. Cassell Petter and Galpin, LondonGoogle Scholar
  105. Szabo JK, Vesk PA, Baxter PW, Possingham HP (2010) Regional avian species declines estimated from volunteer-collected long-term data using list length analysis. Ecol Appl 20:2157–2169Google Scholar
  106. Theiling KM, Croft BA (1988) Pesticide side-effects on arthropod natural enemies: a database summary. Agric Ecosyst Environ 21:191–218Google Scholar
  107. Thomas JA (2005) Monitoring change in the abundance and distribution of insects using butterflies and other indicator groups. Philos Trans R Soc B 360:229–257Google Scholar
  108. Thomas JA (2016) Butterfly communities under threat. Science 353:216–218Google Scholar
  109. Thomas JA, Bourn NAD, Clarke RT, Stewart KE, Simcox DJ, Pearman GS, Curtis R, Goodger B (2001) The quality and isolation of habitat patches both determine where butterflies persist in fragmented landscapes. Proc R Soc B 268:1791–1796Google Scholar
  110. Thomas AG, Telfer MG, Roy DB, Preston CD, Greenwood JJD, Asher J, Fox R, Clarke RT, Lawton JH (2004) Comparative losses of British butterflies, birds, and plants and global extinction crisis. Science 303:1879–1881Google Scholar
  111. Thomas JA, Simcox DJ, Clarke RT (2009) Successful conservation of a threatened Maculinea butterfly. Science 325:80–83Google Scholar
  112. Thorn S, Hacker HH, Seibold S, Jehl H, Bässler C, Müller J (2015) Guild-specific responses of forest Lepidoptera highlight conservation oriented forest management—implications from conifer-dominated forests. Forest Ecol Manag 337:41–47Google Scholar
  113. Toivonen M, Herzon I, Kuussaari M (2016) Community composition of butterflies and bumblebees in fallows: niche breadth and dispersal capacity modify responses to fallow type and landscape. J Insect Conserv 20:23–34Google Scholar
  114. Travis JMJ (2003) Climate change and habitat destruction: a deadly anthropogenic cocktail. Proc R Soc Lond B 270:467–473Google Scholar
  115. Tuck SL, Winqvist C, Mota F, Ahnström J, Turnbull LA, Bengtsson J (2014) Land-use intensity and the effects of organic farming on biodiversity: a hierarchical meta-analysis. J Appl Ecol 51:746–755Google Scholar
  116. Ulrich W, Zalewski M, Hajdamowicz I, Stańska M, Ciurzycki W, Tykarski P (2013) Towards a general species –time–area–sampling effort relationship. Polish J Ecol 61:345–354Google Scholar
  117. Ulrich W, Baselga A, Kusumoto B, Shiono T, Tuomisto H, Kubota Y (2017a) The tangled link between β- and γ-diversity: a Narcissus effect weakens statistical inferences in null model analyses of diversity patterns. Glob Ecol Biogeogr 26:1–5Google Scholar
  118. Ulrich W, Kryszewski W, Sewerniak P, Puchałka R, Strona G, Gotelli NJ (2017b) A comprehensive framework for the study of species co-occurrences, nestedness and turnover. Oikos 126:1607–1616Google Scholar
  119. Ulrich W, Kubota Y, Kusumoto B, Baselga A, Tuomisto H, Gotelli NJ (2018) Species richness correlates of raw and standardized co-occurrence metrics. Glob Ecol Biogeogr 27:395–399Google Scholar
  120. Van Swaay C, Cuttelod A, Collins S, Maes D, López Munguira M, Šašić M, Settele J, Verovnik R, Verstrael T, Warren M, Wiemers M, Wynhof I (2010) European Red List of Butterflies. Publications Office of the European Union, LuxembourgGoogle Scholar
  121. Vandewalle M, De Bello F, Berg MP, Bolger T, Dolédec S, Dubs F, Feld CK, Harrington R, Harrison PA, Lavorel S, da Silva P, Moretti M, Niemelä J, Santos P, Sattler T, Sousa J, Sykes M, Vanbergen A, Woodcock B (2010) Functional traits as indicators of biodiversity response to land use changes across ecosystems and organisms. Biodiv Conserv 19:2921–2947Google Scholar
  122. WallisDeVries MF, van Swaay CAM (2017) A nitrogen index to track changes in butterfly species assemblages under nitrogen deposition. Biol Conserv 212:448–453Google Scholar
  123. Wenzel M, Schmitt T, Weitzel M, Seitz A (2006) The severe decline of butterflies on western German calcareous grasslands during the last 30 years: a conservation problem. Biol Conserv 128:542–552Google Scholar
  124. Wilsey BJ, Martin LM, Kaul AD (2018) Phenology differences between native and novel exotic-dominated grasslands rival the effects of climate change. J Appl Ecol 55:863–873Google Scholar
  125. Wilson JF, Baker D, Cheney J, Cook M, Ellis M, Freestone R, Gardner D, Geen G, Hemming R, Hodgers D, Howarth S, Jupp A, Lowe N, Orridge S, Shaw M, Smith B, Turner A, Young H (2018) A role for artificial night-time lighting in long-term changes in populations of 100 widespread macro-moths in UK and Ireland: a citizen-science study. J Insect Conserv 22:189–196Google Scholar
  126. Woodcock BA, Bullock JM, Shore RF, Heard MS, Pereira MG et al (2017) Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 356:1393–1395Google Scholar
  127. Yekwayo I, Pryke JS, Gaigher R, Samways MJ (2018) Only multi-taxon studies show the full range of arthropod responses to fire. PLoS ONE 13(4):e0195414Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Jan Christian Habel
    • 1
    • 2
    Email author
  • Michael J. Samways
    • 3
  • Thomas Schmitt
    • 4
    • 5
  1. 1.Evolutionary Zoology Group, Department of BiosciencesUniversity of SalzburgSalzburgAustria
  2. 2.Terrestrial Ecology Research Group, Department of Ecology and Ecosystem Management, School of Life Science WeihenstephanTechnische Universität MünchenFreisingGermany
  3. 3.Department of Conservation Ecology and EntomologyStellenbosch UniversityStellenboschSouth Africa
  4. 4.Senckenberg Deutsches Entomologisches InstitutMünchebergGermany
  5. 5.Department of Zoology, Institute of Biology, Faculty of Natural Sciences IMartin-Luther-University Halle-WittenbergHalle (Saale)Germany

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