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
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
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
Aldrich RJ (1984) Weed-crop ecology-principles in weed management. Breton Publishers, North Scituate
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
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
Altieri MA, Letourneau DK (1982) Vegetation management and biological control in agroecosystems. Crop Prot 1:405–430
Altieri MA, Nicholls CI (2004) Biodiversity and pest management in agroecosystems. Haworth Press, New York
Altieri MA, Whitcomb WH (1979a) The potential use of weeds in the manipulation of beneficial insects. HortScience 14:12–18
Altieri MA, Whitcomb WH (1979b) Manipulation of insect populations through seasonal disturbance of weed communities. Prot Ecol 1:185–202
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
Anderson RN (1968) Germination and establishment of weeds for experimental purposes. Weed Science Society of America, Washington
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
Baliddawa CW (1985) Plant species diversity and crop pest control: an analytical review. Insect Sci Appl 6:479–487
Ball DA (1992) Weed seed-bank response to tillage, herbicides, and crop rotation sequences. Weed Sci 40:654–659
Ball DA, Miller SD (1990) Weed seed population response to tillage and herbicide use in three irrigated cropping sequences. Weed Sci 38:511–517
Bantilan RT, Palada M, Harwood RR (1974) Integrated weed management. I. Key factors affecting weed-crop balance. Phil Weed Sci Bull 1:14–36
Barberi P (2002) Weed management in organic agriculture: are we addressing the right issues. Weed Res 42:177–193
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
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
Benedek P (1996) Structure and density of lucerne pollinating wild bee populations as affected by changing agriculture. Acta Hort 437:353–357
Bohart GE (1972) Management of habitats for wild bees. Proc Tall Timbers Conf Ecol Animal Control Habitat Manag 3:253–266
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
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
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
Chacoff NP, Aizen MA (2006) Edge effects on flower-visiting insects in grapefruit plantations bordering premontane subtropical forest. J Appl Ecol 43:18–27
Clements DR, Weise SF, Swanton CJ (1994) Integrated weed management and weed species diversity. Phytoprotection 75:1–18
Coble HD, Mortense DA (1992) The threshold concept and its application to weed science. Weed Tech 6:191–195
Corbet SA (1995) Insects, plants and succession: advantages of long term aside. Agric Ecosyst Environ 53:201–217
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
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
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
Dover JW, Sotherton N, Gobbett K (1990) Reduced pesticide inputs on cereal field margins: the effects on butterfly abundance. Ecol Entomol 15:17–24
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
Flaherty D (1969) Ecosystem trophic complexity and the Willamette mite, Eotetranychus willamettei (Acarine: Tetranychidae) densities. Ecol 50:911–916
Free JB (1993) Insect pollination of crops. Academic, London
Gallai N, Settele JM, Vaissiere BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollination decline. Ecol Econ 68:810–821
Garibaldi LA, Aizen MA, Cunningham SA, Klein AM (2009) Pollinator shortage and global crop yield. Comm Integ Biol 2:37–39
Goulson D (2003) Conserving wild bees for crop pollination. Food Agric Envir 1:142–144
Groot AT, Dicke M (2002) Insect resistant transgenic plants in a multiple-trophic level. Plant J 31:387–406
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
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
Hole DG, Perkins AJ, Wilson JD, Alexander IH, Grice PV, Evans AD (2004) Does organic farming benefit biodiversity? Biol Cons 122:113–130
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
Hoveland CS, Buchanan GA, Harris MC (1976) Response of weeds to soil phosphorous and potassium. Weed Sci 24:194–201
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
Johansen CA (1977) Pesticides and pollinators. Ann Rev Entomol 22:177–192
Johansen CA, Mayer DF (1990) Pollinator protection: a bee and pesticide handbook. Wicwas Press, Cheshire
Keams CA, Inouye DW (1997) Pollinators, flowering plants, and conservation biology. BioSci 47:297–307
Kevan PG (1983) Insects as flower visitors and pollinators. Ann Rev Entomol 28:407–453
Kevan PG (1999) Pollinators as bioindicators of the state of the environment: species, activity and diversity. Agric Ecosyst Environ 74:373–393
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
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
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
Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci 99:16812–16816
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
Lagerlof J, Starkb J, Svensson B (1992) Margins of agricultural fields as habitats for pollinating insects. Agric Ecosyst Environ 40:117–124
Landis D, Menalled FD, Costamagna AC, Wilkinson TK (2005) Manipulating plant resources to enhance beneficial arthropods in agricultural landscapes. Weed Sci 53:902–908
Leius K (1967) Influence of wild flowers on parasitism of tent caterpillar and codling moth. Can Entomol 99:444–446
Liebman M, Davis AS (2000) Integration of soil, crop and weed management in low-external input farming systems. Weed Res 40:27–47
Liebman M, Dyck E (1993) Crop rotation and intercropping strategies for weed management. Ecol Appl 3:92–122
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
Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. BioSci 56:311–323
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
Morandin LA, Winston ML (2005) Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecol Appl 15:871–881
Morandin LA, Winston ML (2006) Pollinators provide economic incentive to preserve natural land in agroecosystems. Agric Ecosyst Environ 116:292–298
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
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
National Academy of Sciences (1969) Insect-pest management and control. Prin Plant Anim Pest Control Ser 3:100–164
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
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
New TR (2005) Invertebrate conservation and agricultural ecosystems. Cambridge University Press, Cambridge
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
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
Ockinger E, Smith HG (2007) Seminatural grasslands as population sources for pollinating insects in agricultural landscapes. J Appl Ecol 44:50–59
Oliver LR (1988) Principles of weed threshold research. Weed Tech 2:398–403
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
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
Pimentel D (1961) Species diversity and insect population outbreaks. Ann Entomol Soc Amer 54:76–86
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
Richards AJ (2001) Does low biodiversity resulting from modern agriculture practice affect crop pollination and yield? Ann Bot 88:165–172
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
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
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
Sheperd MD, Buchmann SL, Vaughan M, Black SH (2003) Pollinator conservation handbook. Xerces Society, Portland
Shuler R, Roulston TH, Farris GE (2005) Farming practices influence wild pollinator populations on squash and pumpkin. J Econ Entomol 98:790–795
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
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
Steffan-Dewenter I (2002) Landscape context affects trap-nesting bees, wasps, and their natural enemies. Ecol Entomol 27:631–637
Steffan-Dewenter I, Potts SG, Packer L (2005) Pollinator diversity and crop pollination services are at risk. Trends Ecol Evol 20:651–652
Stephen WP (1955) Alfalfa pollination in Manitoba. J Econ Entomol 48:543–548
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
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
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
van Emden HF (1963) Observations of the effects of flowers on the activity of parasitic Hymenoptera. Entomol Mon Mag 98:265–270
van Emden HF (1965) The role of uncultivated land in the biology of crop pests and beneficial insects. Sci Hortic 17:121–136
William RD (1981) Complementary interactions between weeds, weed control practices, and pests in horticultural cropping systems. HortScience 16:508–513
Willmer P (2011) Pollination and floral ecology. Princeton University Press, Princeton
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
Wrucke MA, Arnold WE (1985) Weed species distribution as influenced by tillage and herbicides. Weed Sci 33:853–856
Zimdahl RL (1980) Weed–crop competition—a review. International Plant Protection Center, Oregon State University, Corvallis
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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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DOI: https://doi.org/10.1007/s13593-012-0092-y