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Plant biodiversity enhances bees and other insect pollinators in agroecosystems. A review

Abstract

Thirty-five percent of global production from crops including at least 800 cultivated plants depend on animal pollination. The transformation of agriculture in the past half-century has triggered a decline in bees and other insect pollinators. In North America, losses of bee colonies have accelerated since 2004, leaving the continent with fewer managed pollinators than at any time in the past 50 years. A number of factors linked to industrial modes of agriculture affect bee colonies and other pollinators around the world, ranging from habitat degradation due to monocultures with consequent declines in flowering plants and the use of damaging insecticides. Incentives should be offered to farmers to restore pollinator-friendly habitats, including flower provisioning within or around crop fields and elimination of use of insecticides by adopting agroecological production methods. Conventional farmers should be extremely cautious in the choice, timing, and application of insecticides and other chemicals. Here, we review the literature providing mounting evidence that the restoration of plant biodiversity within and around crop fields can improve habitat for domestic and wild bees as well as other insects and thus enhance pollination services in agroecosystems. Main findings are the following: (1) certain weed species within crop fields that provide food resources and refuge should be maintained at tolerable levels within crop fields to aid in the survival of viable populations of pollinators. (2) Careful manipulation strategies need to be defined in order to avoid weed competition with crops and interference with certain cultural practices. Economic thresholds of weed populations, as well as factors affecting crop–weed balance within a crop season, need to be defined for specific cropping systems. (3) More research is warranted to advance knowledge on identifying beneficial weed species and ways to sponsor them to attract pollinators while not reducing yields through interference. (4) In areas of intensive farming, field margins, field edges and paths, headlands, fence-lines, rights of way, and nearby uncultivated patches of land are important refuges for many pollinators. (5) Maintenance and restoration of hedgerows and other vegetation features at field borders is therefore essential for harboring pollinators. (6) Appropriate management of non-cropped areas to encourage wild pollinators may prove to be a cost-effective means of maximizing crop yield.

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References

  • Adams JB, Drew ME (1965) Grain aphids in New Brunswick. Ill. Aphid populations in herbicide-treated oat fields. Can J Zool 43:789–794

    Article  CAS  Google Scholar 

  • Aizen MA, Garibaldi LA, Cunningham SA, Klein AM (2008) Long term global trends in crop yields and production reveal no current pollinator shortage but increasing pollinator dependency. Curr Biol 18:1572–1575

    PubMed  Article  CAS  Google Scholar 

  • Al Ghamdil A (2003) The impact of insect pollinators on yield and yield components of faba bean (Vicia faba L.). Saudi J Biol Sci 10:56–62

    Google Scholar 

  • Aldrich RJ (1984) Weed-crop ecology-principles in weed management. Breton Publishers, North Scituate

    Google Scholar 

  • Allen-Wardell G, Bernhardt P, Bitner R, Burquez A, Buchmann S (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Cons Biol 12:8–17

    Article  Google Scholar 

  • Allsopp M, de Lange WJ, Veldtman R (2008) Valuing insect pollination services with cost of replacement. PLS one 3(9):e3128. doi:10.1371/Journal.pone.0003128

    Article  Google Scholar 

  • Altieri MA, Letourneau DK (1982) Vegetation management and biological control in agroecosystems. Crop Prot 1:405–430

    Article  Google Scholar 

  • Altieri MA, Nicholls CI (2004) Biodiversity and pest management in agroecosystems. Haworth Press, New York

    Google Scholar 

  • Altieri MA, Whitcomb WH (1979a) The potential use of weeds in the manipulation of beneficial insects. HortScience 14:12–18

    Google Scholar 

  • Altieri MA, Whitcomb WH (1979b) Manipulation of insect populations through seasonal disturbance of weed communities. Prot Ecol 1:185–202

    Google Scholar 

  • Altieri MA, Schoonhoven AV, Doll JD (1977) The ecological role of weeds in insect pest management systems: a review illustrated with bean (Phaseolus vulgaris L.) cropping systems. PANS 23:195–205

    Google Scholar 

  • Anderson RN (1968) Germination and establishment of weeds for experimental purposes. Weed Science Society of America, Washington

    Google Scholar 

  • Bäckman JC, Tiainen J (2002) Habitat quality of field margins in a Finnish farmland area for bumblebees (Hymenoptera: Bombus and Psithyrus). Agric Ecosyst Environ 89:53–68

    Article  Google Scholar 

  • Baliddawa CW (1985) Plant species diversity and crop pest control: an analytical review. Insect Sci Appl 6:479–487

    Google Scholar 

  • Ball DA (1992) Weed seed-bank response to tillage, herbicides, and crop rotation sequences. Weed Sci 40:654–659

    Google Scholar 

  • Ball DA, Miller SD (1990) Weed seed population response to tillage and herbicide use in three irrigated cropping sequences. Weed Sci 38:511–517

    CAS  Google Scholar 

  • Bantilan RT, Palada M, Harwood RR (1974) Integrated weed management. I. Key factors affecting weed-crop balance. Phil Weed Sci Bull 1:14–36

    Google Scholar 

  • Barberi P (2002) Weed management in organic agriculture: are we addressing the right issues. Weed Res 42:177–193

    Article  Google Scholar 

  • Belfrage K, BJörklund J, Salomonsson L (2005) The effects of farm size and organic farming on diversity of birds, pollinators, and plants in a Swedish landscape. Ambio 8:582–588

    Google Scholar 

  • Benedek P (1972) Possible indirect effect of weed control on population changes of wild bees pollinating lucerne. Acta Pathol Acad Sci Hung 7:267–278

    Google Scholar 

  • Benedek P (1996) Structure and density of lucerne pollinating wild bee populations as affected by changing agriculture. Acta Hort 437:353–357

    Google Scholar 

  • Bohart GE (1972) Management of habitats for wild bees. Proc Tall Timbers Conf Ecol Animal Control Habitat Manag 3:253–266

    Google Scholar 

  • Buchanan GA (1977) Weed biology and competition. In: Truelove B (ed) Research methods in weed science. 2nd ed. Southern Weed Sci. Soc, Auburn Printing, Inc., Auburn, AL, pp. 25–41

  • Buchmann SL, Nabhan GP (1996) The forgotten pollinators. Island Press, Washington

    Google Scholar 

  • Carreck NL, Williams IH (2002) Food for insect pollinators on farmland: insect visits to flowers of annual seed mixtures. J Insect Conser 6:13–23

    Article  Google Scholar 

  • Carvalheiro LG, Veldtman R, Shenkute AG, Tesfay G, Werner CW, Donaldson JS, Nicolson SW (2011) Natural and within-farmland biodiversity enhances crop productivity. Ecology Letters 14, 251–259

    Google Scholar 

  • Chacoff NP, Aizen MA (2006) Edge effects on flower-visiting insects in grapefruit plantations bordering premontane subtropical forest. J Appl Ecol 43:18–27

    Article  Google Scholar 

  • Clements DR, Weise SF, Swanton CJ (1994) Integrated weed management and weed species diversity. Phytoprotection 75:1–18

    Article  Google Scholar 

  • Coble HD, Mortense DA (1992) The threshold concept and its application to weed science. Weed Tech 6:191–195

    Google Scholar 

  • Corbet SA (1995) Insects, plants and succession: advantages of long term aside. Agric Ecosyst Environ 53:201–217

    Article  Google Scholar 

  • Dempster JP (1969) Some effects of weed control on the numbers of the small cabbage white (Pieris rapae L.) on Brussels sprouts. J Appl Ecol 6:339–405

    Article  Google Scholar 

  • Dixon DP, Fingler BG (1982) The effects of the 1981 Manitoba emergency mosquito control program on honey bees. In: Western equine encephilitis in Manitoba. Government of Manitoba, Winnipeg, pp 243–247

    Google Scholar 

  • Dixon DP, Fingler BG (1984) The effects of the mosquito control program on bees. In: Final technical report on environmental monitoring program for the 1983 spraying of malathion to combat western equine encephalitis. Government of Manitoba, Winnipeg, pp 101–121

    Google Scholar 

  • Dover JW, Sotherton N, Gobbett K (1990) Reduced pesticide inputs on cereal field margins: the effects on butterfly abundance. Ecol Entomol 15:17–24

    Article  Google Scholar 

  • Feber RE, Firbank LG, Johnson PJ, Macdonald DW (1997) The effects of organic farming on pest and non-pest butterfly abundance. Agric Ecosys Envir 64:133–139

    Article  Google Scholar 

  • Flaherty D (1969) Ecosystem trophic complexity and the Willamette mite, Eotetranychus willamettei (Acarine: Tetranychidae) densities. Ecol 50:911–916

    Article  Google Scholar 

  • Free JB (1993) Insect pollination of crops. Academic, London

    Google Scholar 

  • Gallai N, Settele JM, Vaissiere BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollination decline. Ecol Econ 68:810–821

    Article  Google Scholar 

  • Garibaldi LA, Aizen MA, Cunningham SA, Klein AM (2009) Pollinator shortage and global crop yield. Comm Integ Biol 2:37–39

    Article  Google Scholar 

  • Goulson D (2003) Conserving wild bees for crop pollination. Food Agric Envir 1:142–144

    Google Scholar 

  • Groot AT, Dicke M (2002) Insect resistant transgenic plants in a multiple-trophic level. Plant J 31:387–406

    PubMed  Article  CAS  Google Scholar 

  • Hausammann A (1996) Strip-management in rape crop: is winter rape endangered by negative impacts of sown weed strips? J Appl Ent 120:505–512

    Article  Google Scholar 

  • Hawes CJ, Haughton JL, Osborne DB, Roy SJ, Clark JN, Perry P, Rothery DA, Bohan DR, Brooks GT, Champion AM, Dewar MS, Heard IP, Woiwod RE, Daniels MW, Young AM, Parish RJ, Scott LG, Firbank B, Squire GR (2003) Responses of plants and invertebrate trophic groups to contrasting herbicide regimes in the farm scale evaluations of genetically modified herbicide-tolerant crops. Phil Trans R Soc Lond B 358:1899–1913

    Article  CAS  Google Scholar 

  • Hole DG, Perkins AJ, Wilson JD, Alexander IH, Grice PV, Evans AD (2004) Does organic farming benefit biodiversity? Biol Cons 122:113–130

    Article  Google Scholar 

  • Horowitz MT, Blumdel T, Hertz-linger G, Hulin N (1962) Effects of repeated applications of ten soil-active herbicides on weed populations. Weed Res 14:97–109

    Article  Google Scholar 

  • Hoveland CS, Buchanan GA, Harris MC (1976) Response of weeds to soil phosphorous and potassium. Weed Sci 24:194–201

    CAS  Google Scholar 

  • Idris AB, Grafius E (1995) Wildflowers as nectar sources for Diadegma insulare (Hymenoptera: Ichneumonidae), a parasitoid of diamondback moth (Lepidoptera: Yponomeutidae). Environ Entomol 24:1726–1735

    Google Scholar 

  • Johansen CA (1977) Pesticides and pollinators. Ann Rev Entomol 22:177–192

    Article  CAS  Google Scholar 

  • Johansen CA, Mayer DF (1990) Pollinator protection: a bee and pesticide handbook. Wicwas Press, Cheshire

    Google Scholar 

  • Keams CA, Inouye DW (1997) Pollinators, flowering plants, and conservation biology. BioSci 47:297–307

    Article  Google Scholar 

  • Kevan PG (1983) Insects as flower visitors and pollinators. Ann Rev Entomol 28:407–453

    Article  Google Scholar 

  • Kevan PG (1999) Pollinators as bioindicators of the state of the environment: species, activity and diversity. Agric Ecosyst Environ 74:373–393

    Article  Google Scholar 

  • Kevan PG, Plowright RC (1989) Fenitrothion and insect pollination. In: Ernst WR, Pearce PA, Pollock TL (eds) Environmental effects of fenitrothion use in forestry: impacts on insect pollinators, songbirds, and aquatic organisms. Environment Canada, Dartmouth, pp 13–42

    Google Scholar 

  • Kevan PG, Greco CF, Belaoussoff S (1997) Log-normality of biodiversity and abundance in diagnosis and measuring of ecosystemic health: pesticide stress on pollinators on blueberry heaths. J Appl Ecol 34:1122–1136

    Article  Google Scholar 

  • Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc Lond B Biol Sci 274:303–313

    Article  Google Scholar 

  • Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci 99:16812–16816

    Google Scholar 

  • Kremen C, Williams NM, Bugg RL, Fay JP, Thorp RW (2004) The area requirements of an ecosystem service: crop pollination by native bee communities in California. Ecol Lett 7:1109–1119

    Article  Google Scholar 

  • Lagerlof J, Starkb J, Svensson B (1992) Margins of agricultural fields as habitats for pollinating insects. Agric Ecosyst Environ 40:117–124

    Article  Google Scholar 

  • Landis D, Menalled FD, Costamagna AC, Wilkinson TK (2005) Manipulating plant resources to enhance beneficial arthropods in agricultural landscapes. Weed Sci 53:902–908

    Article  CAS  Google Scholar 

  • Leius K (1967) Influence of wild flowers on parasitism of tent caterpillar and codling moth. Can Entomol 99:444–446

    Article  Google Scholar 

  • Liebman M, Davis AS (2000) Integration of soil, crop and weed management in low-external input farming systems. Weed Res 40:27–47

    Article  Google Scholar 

  • Liebman M, Dyck E (1993) Crop rotation and intercropping strategies for weed management. Ecol Appl 3:92–122

    Article  Google Scholar 

  • Liebman M, Gallandt ER (1997) Many little hammers: ecological management of crop–weed interactions. In: Jackson LE (ed) Ecology in Agriculture. Academic Press, San Diego, pp 291–342

    Chapter  Google Scholar 

  • Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. BioSci 56:311–323

    Article  Google Scholar 

  • Mackenzie KE, Winston ML (1984) Diversity and abundance of native bee pollinators of berry crops and natural vegetation in the lower Fraser Valley, British Columbia. Can Entomol 116:965–974

    Article  Google Scholar 

  • Morandin LA, Winston ML (2005) Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecol Appl 15:871–881

    Article  Google Scholar 

  • Morandin LA, Winston ML (2006) Pollinators provide economic incentive to preserve natural land in agroecosystems. Agric Ecosyst Environ 116:292–298

    Article  Google Scholar 

  • Morandin LA, Winston ML, Abbott VA, Franklin MT (2007) Can pastureland increase wild bee abundance in agriculturally intense areas? Basic Appl Ecol 8:117–124

    Article  Google Scholar 

  • Moreby SJ, Southway SE (1999) Influence of autumn applied herbicides on summer and autumn food available to birds in winter wheat fields in southern England. Agric Ecosyst Environ 72:285–297

    Article  Google Scholar 

  • National Academy of Sciences (1969) Insect-pest management and control. Prin Plant Anim Pest Control Ser 3:100–164

    Google Scholar 

  • Naumkin VP (1992) Species composition of insects- pollinators of buckwheat, pp. 443–446. In: Proc Fifth Inter Symp Buckwheat Res, Agricultural Publishing House, Beijing. Pp. 443–446

  • Nentwig W (1998) Weedy plant species and their beneficial arthropods: potential for manipulation in field crops. In: Pickett CH, Bugg RL (eds) Enhancing biological control: habitat management to promote natural enemies of agricultural pests. UC Press, Berkeley, pp 49–72

    Google Scholar 

  • Nentwig W, Frank T, Lethmayer C (1998) Sown weed strips: artificial ecological compensation areas an important tool in conservation biological control. In: Barbosa P (ed) conservation biological control. Academic, New York, pp 133–151

    Chapter  Google Scholar 

  • New TR (2005) Invertebrate conservation and agricultural ecosystems. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Norris RR (1982) Interactions between weeds and other pests in the agroecosystem. In: Hatfield JL, Thomason IJ (eds) Biometeorology in integrated pest management. Academic, New York, pp 343–406

    Google Scholar 

  • O’Callaghan M, Glare TR, Burgess EPJ, Malone LA (2005) Effects of plants genetically modified for insect resistance on non- target organism. Ann Rev Entom 50:271–292

    PubMed  Article  Google Scholar 

  • Ockinger E, Smith HG (2007) Seminatural grasslands as population sources for pollinating insects in agricultural landscapes. J Appl Ecol 44:50–59

    Article  Google Scholar 

  • Oliver LR (1988) Principles of weed threshold research. Weed Tech 2:398–403

    Google Scholar 

  • Perrin RM (1975) The role of the perennial stinging nettle Urtica dioica as a reservoir of beneficial natural enemies. Ann Appl Biol 81:289–297

    Article  Google Scholar 

  • Picard-Nizou AL, Grison R, Olsen L, Pioche C, Arnold G, Pham-Delegue MH (1997) Impact of proteins used in plant genetic engineering toxicity and behavioral studies in the honeybee. J Econ Entomol 90:1710–1716

    CAS  Google Scholar 

  • Pimentel D (1961) Species diversity and insect population outbreaks. Ann Entomol Soc Amer 54:76–86

    Google Scholar 

  • Pontin DR, Wade MR, Kehrli P, Wratten SD (2006) Attractiveness of single and multiple species flower patches to beneficial insects in agroecosystems. Annals of Applied Biology 148:39–47

    Google Scholar 

  • Richards AJ (2001) Does low biodiversity resulting from modern agriculture practice affect crop pollination and yield? Ann Bot 88:165–172

    Article  Google Scholar 

  • Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–124

    Article  Google Scholar 

  • Scott-Dupree CD, Winston ML (1987) Wild bee pollinator diversity and abundance in orchard and uncultivated habitats in the Okanagan Valley, British Columbia. Can Entomol 119:735–745

    Article  Google Scholar 

  • Sears MK, Hellmich RL, Stanley-Horn DE, Oberhauser KS, Pleasants JM, Mattila HR, Siegfried BD, Dively GP (2001) Impact of Bt corn pollen on monarch butterfly populations: a risk assessment. PNAS 98:11937–11942

    PubMed  Article  CAS  Google Scholar 

  • Sheperd MD, Buchmann SL, Vaughan M, Black SH (2003) Pollinator conservation handbook. Xerces Society, Portland

    Google Scholar 

  • Shuler R, Roulston TH, Farris GE (2005) Farming practices influence wild pollinator populations on squash and pumpkin. J Econ Entomol 98:790–795

    PubMed  Article  Google Scholar 

  • Smith JG (1969) Some effects of crop background on populations of aphids and their natural enemies on Brussels sprouts. Ann Appl Biol 63:326–330

    Article  Google Scholar 

  • Speight MR, Lawton JH (1976) The influence of weed cover on the mortality imposed on artificial prey by predatory ground beetles in cereal fields. Oecol 23:211–223

    Article  Google Scholar 

  • Steffan-Dewenter I (2002) Landscape context affects trap-nesting bees, wasps, and their natural enemies. Ecol Entomol 27:631–637

    Article  Google Scholar 

  • Steffan-Dewenter I, Potts SG, Packer L (2005) Pollinator diversity and crop pollination services are at risk. Trends Ecol Evol 20:651–652

    PubMed  Article  Google Scholar 

  • Stephen WP (1955) Alfalfa pollination in Manitoba. J Econ Entomol 48:543–548

    Google Scholar 

  • Syme PD (1975) The effects of flowers on the longevity and fecundity of two native parasites of the European pine shoot moth in Ontario. Environ Entomol 4:337–346

    Google Scholar 

  • Telenga NA (1958) Biological method of pest control in crops and forest plants in the USSR. In: Report of the Soviet Delegation. Ninth International Conference on Quarantine and Plant Protection, Moscow, pp. 1–15

  • Thresh JM (1981) Pests, pathogens and vegetation: the role of weeds and wild plants in the ecology of crop pests and diseases. Pitman, Boston, MA

    Google Scholar 

  • Ulbert L, Horst-Henning S, Klimek S (2010) Using selective herbicides to manage beneficial and rare weed species in winter wheat. J Plant Dis Prot 117:233–239

    Google Scholar 

  • van Emden HF (1963) Observations of the effects of flowers on the activity of parasitic Hymenoptera. Entomol Mon Mag 98:265–270

    Google Scholar 

  • van Emden HF (1965) The role of uncultivated land in the biology of crop pests and beneficial insects. Sci Hortic 17:121–136

    Google Scholar 

  • William RD (1981) Complementary interactions between weeds, weed control practices, and pests in horticultural cropping systems. HortScience 16:508–513

    Google Scholar 

  • Willmer P (2011) Pollination and floral ecology. Princeton University Press, Princeton

    Google Scholar 

  • Wratten SD, van Emden HF (1995) Habitat management for enhanced activity of natural enemies of insect pests. In: Glen DM, Greaves MP, Anderson HM (eds) Ecology and integrated farming systems. John Wiley and Sons, Chichester, pp 117–145

    Google Scholar 

  • Wrucke MA, Arnold WE (1985) Weed species distribution as influenced by tillage and herbicides. Weed Sci 33:853–856

    Google Scholar 

  • Zimdahl RL (1980) Weed–crop competition—a review. International Plant Protection Center, Oregon State University, Corvallis

    Google Scholar 

Download references

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Correspondence to Miguel A. Altieri.

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Nicholls, C.I., Altieri, M.A. Plant biodiversity enhances bees and other insect pollinators in agroecosystems. A review. Agron. Sustain. Dev. 33, 257–274 (2013). https://doi.org/10.1007/s13593-012-0092-y

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Keywords

  • Pollinators
  • Habitat management
  • Weed manipulation
  • Hedgerows
  • Agroecosystems