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Long-term yield trends of insect-pollinated crops vary regionally and are linked to neonicotinoid use, landscape complexity, and availability of pollinators

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Abstract

Time series data on crop yields for two main wind-pollinated crops (barley and wheat) and for three crops benefitting from insect pollination (turnip rapeseed, caraway, and black currant), were compiled from official agricultural statistics. In Finland, these statistics are available at aggregate national level, and at the level of each of the 15 provinces of the country. Yields of wind-pollinated crops have steadily increased in Finland, while yields of insect-pollinated crops have been highly variable. The largest crop benefitting from insect pollination is turnip rapeseed, which shows first a clear tendency to increased yields from 1980 to 1993, after which there has been a continuous decline in yields at the national average level. Regionally, the trends in turnip rapeseed yield show large variation, so that in six provinces of Finland, the trend has been significantly decreasing; in five provinces, there has been no significant trend; and in two provinces, there has been a significant linear increase in yields. Yield trends in the two other insect-pollinated crops, caraway and black currants, show similar trend variations. However, at the national average level, caraway yields show no significant trend, while black currant yields have increased during the past 6 years. The possible impact on the trends of insect-pollinated crops of three explanatory variables was analyzed. Significant linear correlation was found between the yield trends (slope of the trends) in rapeseed, and the extent of using neonicotinoid seed dressing in the provinces; the magnitude of yield decline in turnip rapeseed increased, as the use of neonicotinoid seed dressing increased. Similar significant linear correlation was found for the magnitude of yield decline in turnip rapeseed and the complexity of the agricultural landscape in each province; yield trend changed from negative to positive as the proportion of agricultural land of the total terrestrial land area declined from 28% to below 10%. The availability of honey bee colonies with respect to the growing area of crops benefitting from insect pollination also had a linear, significant impact on turnip rapeseed yield trends: yields tended to decline in provinces, where the supply of managed pollinators with respect to demand was low, but tended to increase in provinces, where the number of honey bee colonies were over 30% of the estimated demand. As neither the landscape complexity (proportion of arable land of total terrestrial land area), nor the number of honey bee colonies for pollination have changed significantly over the past 10–20 years, these factors cannot explain the observed differences in the yield trends of the examined insect-pollinated crops. It appears that only the uptake of neonicotinoid insecticide seed dressing about 15 years ago can explain the crop yield declines in several provinces, and at the national level for turnip rapeseed, most likely via disruption of pollination services by wild pollinators.

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References

  • Aakkula J, Leppänen J (eds.) (2014) Maatalouden ympäristötuen vaikuttavuuden seurantatutkimus (MYTVAS 3) -loppuraportti. Maa- ja metsätalousministeriön julkaisuja 3/14.265p. (Abstract in English: Follow-up study on the impacts of agri-environment measures (MYTVAS 3)–Final report). http://mmm.fi/documents/1410837/1720628/MMM_mytvas_loppuraportti_WEB.pdf/2cc8f041-82f2-4bbf-85e3-bd4a8d6964b3

  • Ahvenniemi P (1990) Uudet rypsilajikkeet tulevat (New turnip rapeseed varieties are coming; in Finnish). Käytännön Maamies 1990(3):44–45

    Google Scholar 

  • Aizen MA, Garibaldi LA, Cunningham SA, Klein AM (2008) Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr Biol 18:1572–1575. doi:10.1016/j.cub.2008.08.066

    Article  CAS  PubMed  Google Scholar 

  • Aizen MA, Garibaldi LA, Cunningham SA, Klein AM (2009) How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann Bot 103:1579–1588. doi:10.1093/aob/mcp076

    Article  PubMed  PubMed Central  Google Scholar 

  • Bailey S, Requier F, Nusillard B, Roberts SPM, Potts SG, Bouget C (2014) Distance from forest edge affects bee pollinators in oilseed rape fields. Ecol Evol 4:370–380. doi:10.1002/ece3.924

    Article  PubMed  PubMed Central  Google Scholar 

  • Bartomeus I, Potts SG, Steffan-Dewenter I, Vaissière BE, Woyciechowski M, Krewenka KM, Tscheulin T, Roberts SPM, Szentgyörgyi H, Westphal C, Bommarco R (2014) Contribution of insect pollinators to crop yield and quality varies with agricultural intensification. Peer J 2:e328. doi:10.7717/peerj.328

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Blacquière T, Smagghe G, van Gestel CAM, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21:973–992. doi:10.1007/s10646-012-0863-x

    Article  PubMed  PubMed Central  Google Scholar 

  • Breeze TD, Vaissière BE, Bommarco R, Petanidou T, Seraphides N, Kozák L, Scheper Jeroen, Biesmeijer JC, Kleijn D, Gyldenkærne S, Moretti M, Holzschuh A, Steffan-Dewenter I, Stout JC, Pärtel M, Zobel M, Potts SG (2014) Agricultural policies exacerbate honeybee pollination service supply–demand mismatches across Europe. PLoS ONE 9(1):e82996. doi:10.1371/journal.pone.0082996

    Article  PubMed  PubMed Central  Google Scholar 

  • Calderone NW (2012) Insect pollinated crops, insect pollinators and US agriculture: trend analysis of aggregate data for the period 1992–2009. PLoS ONE 7:e37235. doi:10.1371/journal.pone.0037235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Danner N, Molitor AM, Schiele S, Härtel S, Steffan-Dewenter I (2016) Season and landscape composition affect pollen foraging distances and habitat use of honey bees. Ecol Appl 26:1920–1929. doi:10.1890/15-1840.1

    Article  PubMed  Google Scholar 

  • EFSA (2013a) Conclusion on the peer review of the pesticide risk assessment for bees for the active substance clothianidin. EFSA J 11:3066. doi:10.2903/j.efsa.2013.3066

    Article  Google Scholar 

  • EFSA (2013b) Conclusion on the peer review of the pesticide risk assessment for bees for the active substance thiamethoxam. EFSA J 11:3067. doi:10.2903/j.efsa.2013.3067

    Article  Google Scholar 

  • EFSA (2013c) Conclusion on the peer review of the pesticide risk assessment for bees for the active substance imidacloprid. EFSA J 11:3068. doi:10.2903/j.efsa.2013.3068

    Article  Google Scholar 

  • Ellis S, Berry P. (2012) Re-evaluating thresholds for pollen beetle in oilseed rape. Agriculture and Horticulture Development Board, Project Report No. 495. https://cereals.ahdb.org.uk/media/200518/pr495.pdf

  • European Union (2012) Existing Scientific Evidence of the Effects of Neonicotinoid Pesticides on Bees. European Parliament, Directorate General for Internal Policies, Policy Department A: Economic and Scientific Policy. IP/A/ENVI/NT/2012-09 PE 492.465

  • FERA (2013) Effects of neonicotinoid seed treatments on bumble bee colonies under field conditions. Food and Environment Research Agency, Sand Hutton, p 76

    Google Scholar 

  • Gaines-Day HR, Gratton C (2016) Crop yield is correlated with honey bee hive density but not in high-woodland landscapes. Agric Ecosyst Environ 218:53–57. doi:10.1016/j.agee.2015.11.001

    Article  Google Scholar 

  • Garibaldi L, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R et al (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science. doi:10.1126/science.1230200

    PubMed  Google Scholar 

  • Gathmann A, Tscharntke T (2002) Foraging ranges of solitary bees. J Anim Ecol 71:757–764

    Article  Google Scholar 

  • Godfray HCJ, Blacquiere T, Field LM, Hails RS, Petrokofsky G, Potts SG, McLean AR (2014) A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc R Soc B 281:20140558

    Article  PubMed  PubMed Central  Google Scholar 

  • Godfray HCJ, Blacquiere T, Field LM, Hails RS, Potts SG, Raine NE, McLean AR (2015) A restatement of recent advances in the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc R Soc B 282:20151821

    Article  PubMed  PubMed Central  Google Scholar 

  • Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596. doi:10.1007/s00442-007-0752-9

    Article  PubMed  Google Scholar 

  • Kennedy CM, Lonsdorf E, Neel MC, Williams NM, Ricketts TH, Winfree R et al (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol Lett 16:584–599. doi:10.1111/ele.12082

    Article  PubMed  Google Scholar 

  • Ketola J, Hakala K, Ruottinen L, Ojanen H, Rämö S, Jauhiainen L, Raiskio S, Kukkola M, Heinikainen S, Pelkonen S (2015) The impact of the use of neonicotinoid insecticides on honey bees in the cultivation of spring oilseed crops in Finland in 2013–2015. Natural Resources Institute Finland, Helsinki. Natural resources and bioeconomy studies. 73/2015

  • Koltowski Z, Pluta S, Jablonski B, Szklanowska K (1999) Pollination requirements of eight cultivars of black currant (Ribes nigrum L.). J Hortic Sci Biotechnol 74:472–474. doi:10.1080/14620316.1999.11511139

    Article  Google Scholar 

  • Lindström SAM, Herbertsson L, Rundlöf M, Smith HG, Bommarco R (2016a) Large-scale pollination experiment demonstrates the importance of insect pollination in winter oilseed rape. Oecologia 180:759–769. doi:10.1007/s00442-015-3517-x

    Article  PubMed  Google Scholar 

  • Lindström SAM, Herbertsson L, Rundlöf M, Bommarco R, Smith HG (2016b) Experimental evidence that honeybees depress wild insect densities in a flowering crop. Proc R Soc B 283:20161641. doi:10.1098/rspb.2016.1641

    Article  PubMed  Google Scholar 

  • Manning R, Wallis IR (2005) Seed yields in canola (Brassica napus cv. Karoo) depend on the distance of plants from honeybee apiaries. Aust J Exp Agric 45:1307–1313. doi:10.1071/EA02170

    Article  Google Scholar 

  • McGregor SE (1976) Insect pollination of cultivated crop plants. USDA Agriculture handbook nr. 496. Washington DC

  • Neokosmidis L, Tscheulin T, Devalez J, Petanidou T (2016) Landscape spatial configuration is a key driver of wild bee demographics. Insect Sci. doi:10.1111/1744-7917.12383

    PubMed  Google Scholar 

  • Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  PubMed  Google Scholar 

  • Potts SG, Imperatriz-Fonseca V, Ngo HT, Biesmeijer JC, Breeze TD, Dicks LV, Garibaldi LA, Hill R, Settele J, Vanbergen AJ (2016) The assessment report on pollinators, pollination and food production: summary for policymakers. Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, Bonn

    Google Scholar 

  • Rader R, Bartomeus I, Garibaldi LA, Garratt MPD, Howlett BG, Winfree R, Cunningham SA, Mayfield MM, Arthur AD, Andersson GKS, Bommarco R, Brittain C, Carvalheiro LG, Chacoff NP, Entling MH, Foully B, Freitas BM, Gemmill-Herren B, Ghazoul J, Griffin SR, Gross CL, Herbertsson L, Herzog F, Hipólito J, Jaggar S, Jauker F, Klein A-M, Kleijn D, Krishnan S, Lemos CQ, Lindström SAM, Mandelik Y, Monteiro VM, Nelson W, Nilsson L, Pattemore DE, Pereira NO, Pisanty G, Potts SG, Reemer M, Rundlöf M, Sheffield CS, Scheper J, Schüepp C, Smith HG, Stanley DA, Stout JC, Szentgyörgyi H, Taki H, Vergara CH, Viana BF, Woyciechowski M (2016) Non-bee insects are important contributors to global crop pollination. Proc Natl Acad Sci 113:146–151. doi:10.1073/pnas.1517092112

    Article  CAS  PubMed  Google Scholar 

  • Riitters KH, O’Neill RV, Hunsaker CT, Wickham JD, Yankee DH, Timmins SP, Jones KB, Jackson BL (1995) A factor analysis of landscape pattern and structure metrics. Landsc Ecol. 10:23. doi:10.1007/BF00158551

    Article  Google Scholar 

  • Saarinen A (2016) Bee pollination effect on caraway harvest level. B.Sc. Thesis, Forssa Degree Programme in Sustainable Development, Forssa, Finland (in Finnish, with English abstract). http://urn.fi/URN:NBN:fi:amk-201605127375

  • Sabbahi R, de Oliveira D, Marceau J (2005) Influence of honey bee (Hymenoptera: Apidae) density on the production of canola (Crucifera: Brassicacae). J Econ Entomol 98:367–372. doi:10.1603/0022-0493-98.2.367

    Article  PubMed  Google Scholar 

  • Sandhu H, Waterhouse B, Boyer S, Wratten S (2016) Scarcity of ecosystem services: an experimental manipulation of declining pollination rates and its economic consequences for agriculture. Peer J 4:e2099. doi:10.7717/peerj.2099

    Article  PubMed  PubMed Central  Google Scholar 

  • Schulp CJE, Lautenbach S, Verburg PH (2014) Quantifying and mapping ecosystem services: demand and supply of pollination in the European Union. Ecol Indic 36:131–141. doi:10.1016/j.ecolind.2013.07.014

    Article  Google Scholar 

  • SPSS (2015) IBM SPSS Statistics for Windows, Version 240. IBM Corp, Armonk

    Google Scholar 

  • Tiilikainen TM, Hokkanen HMT (2008) Pyrethroid resistance in Finnish pollen beetle (Meligethes aeneus) populations—is it around the corner? Bull OEPP/EPPO Bull 38:99–103

    Article  Google Scholar 

  • Tukes (2015) Temporary authorisation for plant protection products containing neonicotinoids. The Finnish Safety and Chemicals Agency, http://tukes.fi/en/Current-and-News/News/Plant-Protection-Products/Temporary-authorisation-for-plant-protection-products-containing-neonicotinoids/. (Press release 30.11.2015)

  • VYR (2017). Rypsin ja rapsin viljelyopas: Kasvinsuojelu. Vilja-alan yhteistyöryhmä, The Finnish Cereal Committee (VYR), Helsinki. http://www.vyr.fi/rypsin-ja-rapsin-viljelyopas/kasvinsuojelu/

  • Williams IH (1985) The pollination of swede rape (Brassica napus L.). Bee World 66:16–22

    Article  Google Scholar 

  • Woodcock BA, Isaac NJ, Bullock JM, Roy DB, Garthwaite DG, Crowe A, Pywell RF (2016) Impacts of neonicotinoid use on long-term population changes in wild bees in England. Nat Commun 7:12459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Breeze T, Bailey A, Garthwaite D, Harrington R, Potts SG (2017) Arthropod pest control for UK oilseed rape—comparing insecticide efficacies, side effects and alternatives. PLoS ONE 12(1):e0169475. doi:10.1371/journal.pone.0169475

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Support for our study from the following projects is acknowledged: EU-ERA-NET program, C-IPM project “IPM4Meligethes”; EU-COST-Action FA1307 “Super-B”; and University of the Arctic Thematic Network “Sustainable Production and Foraging of Natural Products in the North.” Comments from several colleagues and two anonymous reviewers on a previous version of the manuscript are highly appreciated and helped us to improve and clarify our text.

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Correspondence to Heikki M. T. Hokkanen.

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Hokkanen, H.M.T., Menzler-Hokkanen, I. & Keva, M. Long-term yield trends of insect-pollinated crops vary regionally and are linked to neonicotinoid use, landscape complexity, and availability of pollinators. Arthropod-Plant Interactions 11, 449–461 (2017). https://doi.org/10.1007/s11829-017-9527-3

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