Comparison of pollinators and natural enemies: a meta-analysis of landscape and local effects on abundance and richness in crops
Shackelford, G., Steward, P.R., Benton, T.G., Kunin, W.E., Potts, S. G. Full text not archived in this repository. It is advisable to refer to the publisher's version if you intend to cite from this work. See Guidance on citing. To link to this item DOI: 10.1111/brv.12040 Abstract/SummaryTo manage agroecosystems for multiple ecosystem services, we need to know whether the management of one service has positive, negative, or no effects on other services. We do not yet have data on the interactions between pollination and pest-control services. However, we do have data on the distributions of pollinators and natural enemies in agroecosystems. Therefore, we compared these two groups of ecosystem service providers, to see if the management of farms and agricultural landscapes might have similar effects on the abundance and richness of both. In a meta-analysis, we compared 46 studies that sampled bees, predatory beetles, parasitic wasps, and spiders in fields, orchards, or vineyards of food crops. These studies used the proximity or proportion of non-crop or natural habitats in the landscapes surrounding these crops (a measure of landscape complexity), or the proximity or diversity of non-crop plants in the margins of these crops (a measure of local complexity), to explain the abundance or richness of these beneficial arthropods. Compositional complexity at both landscape and local scales had positive effects on both pollinators and natural enemies, but different effects on different taxa. Effects on bees and spiders were significantly positive, but effects on parasitoids and predatory beetles (mostly Carabidae and Staphylinidae) were inconclusive. Landscape complexity had significantly stronger effects on bees than it did on predatory beetles and significantly stronger effects in non-woody rather than in woody crops. Effects on richness were significantly stronger than effects on abundance, but possibly only for spiders. This abundance-richness difference might be caused by differences between generalists and specialists, or between arthropods that depend on non-crop habitats (ecotone species and dispersers) and those that do not (cultural species). We call this the ‘specialist-generalist’ or ‘cultural difference’ mechanism. If complexity has stronger effects on richness than abundance, it might have stronger effects on the stability than the magnitude of these arthropod-mediated ecosystem services. We conclude that some pollinators and natural enemies seem to have compatible responses to complexity, and it might be possible to manage agroecosystems for the benefit of both. However, too few studies have compared the two, and so we cannot yet conclude that there are no negative interactions between pollinators and natural enemies, and no trade-offs between pollination and pest-control services. Therefore, we suggest a framework for future research to bridge these gaps in our knowledge.
Albrecht, M., Duelli, P., Muller, C., Kleijn, D. & Schmid, B. (2007). The
Swiss agri-environment scheme enhances pollinator diversity and plant reproductive
success in nearby intensively managed farmland. Journal of Applied Ecology 44,
813–822.
Ameixa, O. & Kindlmann, P. (2008). Agricultural policy-induced landscape changes:
effects on carabid abundance and their biocontrol potential. European Journal of
Entomology 105, 467–476.
Andow, D. A. (1991). Vegetational diversity and arthropod population response.
Annual Review of Entomology 36, 561–586.
Anjum-Zubair, M., Schmidt-Entling, M. H., Querner, P. & Frank, T. (2010).
Influence of within-field position and adjoining habitat on carabid beetle assemblages
in winter wheat. Agricultural and Forest Entomology 12, 301–306.
Arthur, A. D., Li, J., Henry, S. & Cunningham, S. A. (2010). Influence of woody
vegetation on pollinator densities in oilseed Brassica fields in an Australian temperate
landscape. Basic and Applied Ecology 11, 406–414.
Attwood, S. J., Maron, M., House, A. P. N. & Zammit, C. (2008). Do arthropod
assemblages display globally consistent responses to intensified agricultural land use
and management? Global Ecology and Biogeography 17, 585–599.
Backman, J. P. C. & Tiainen, J. (2002). Habitat quality of field margins in a Finnish
farmland area for bumblebees (Hymenoptera: Bombus and Psithyrus). Agriculture,
Ecosystems & Environment 89, 53–68.
Banaszak, J. (1992). Strategy for conservation ofwild bees in an agricultural landscape.
Agriculture, Ecosystems & Environment 40, 179–192.
Banaszak, J. (1996). Ecological bases of conservation of wild bees. In The Conservation
of Bees (eds A. Matheson, S. L. Buchmann, C. O’Toole, P. Westrich and I.
H. Williams), pp. 55–62. Academic Press, London.
Barbosa, P. (1998). Conservation Biological Control. Academic Press, San Diego.
Bat´ary, P., Andras, B., Kleijn, D. & Tscharntke, T. (2011). Landscapemoderated
biodiversity effects of agri-environmental management: a meta-analysis.
Proceedings of the Royal Society B: Biological Sciences 278, 1894–1902.
Bennett, E. M., Peterson, G. D. & Gordon, L. J. (2009). Understanding
relationships among multiple ecosystem services. Ecology Letters 12, 1394–1404.
Benton, T. G., Vickery, J. A. & Wilson, J. D. (2003). Farmland biodiversity: is
habitat heterogeneity the key? Trends in Ecology & Evolution 18, 182–188.
Blanche, R. & Cunningham, S. A. (2005). Rain forest provides pollinating beetles
for atemoya crops. Journal of Economic Entomology 98, 1193–1201.
Blanche, K. R., Ludwig, J. A. & Cunningham, S. A. (2006). Proximity to
rainforest enhances pollination and fruit set in orchards. Journal of Applied Ecology 43,
1182–1187.
Bohart, G. E. (1972). Management of wild bees for the pollination of crops. Annual
Review of Entomology 17, 287–312.
Bommarco, R. & Banks, J. E. (2003). Scale as modifier in vegetation diversity
experiments: effects on herbivores and predators. Oikos 102, 440–448.
Bommarco, R., Biesmeijer, J. C., Meyer, B., Potts, S. G., Poyry, J., Roberts,
S. P. M., Steffan-Dewenter, I. & Ockinger, E. (2010). Dispersal capacity and
diet breadth modify the response of wild bees to habitat loss. Proceedings of the Royal
Society B: Biological Sciences 277, 2075–2082.
Borenstein, M., Hedges, L. V., Higgins, J. P. T. & Rothstein, H. R. (2009).
Introduction to Meta-Analysis. Wiley, Chichester.
Brittain, C., Bommarco, R., Vighi, M., Settele, J. & Potts, S. G. (2010).
Organic farming in isolated landscapes does not benefit flower-visiting insects and
pollination. Biological Conservation 143, 1860–1867.
Bruggisser, O. T., Schmidt-Entling, M. H. & Bacher, S. (2010). Effects of
vineyard management on biodiversity at three trophic levels. Biological Conservation
143, 1521–1528.
B¨uchi, R. (2002).Mortality of pollen beetle (Meligethes spp.) larvae due to predators and
parasitoids in rape fields and the effect of conservation strips. Agriculture, Ecosystems
& Environment 90, 255–263.
Burel, F., Butet, A., Delettre, Y.R. & Mill`an de la Pe˜na,N. (2004).Differential
response of selected taxa to landscape context and agricultural intensification.
Landscape and Urban Planning 67, 195–204.
Cardinale, B. J., Harvey, C. T., Gross, K. & Ives, A. R. (2003). Biodiversity and
biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and
crop yield in an agroecosystem. Ecology Letters 6, 857–865.
Carvalheiro, L. G., Seymour, C. L., Veldtman, R. & Nicolson, S. W. (2010).
Pollination services decline with distance from natural habitat even in biodiversityrich
areas. Journal of Applied Ecology 47, 810–820.
Chacoff, N. P. & Aizen, M. A. (2006). Edge effects on flower-visiting insects in
grapefruit plantations bordering premontane subtropical forest. Journal of Applied
Ecology 43, 18–27.
Chaplin-Kramer, R., O’Rourke, M. E., Blitzer, E. J. & Kremen, C. (2011). A
meta-analysis of crop pest and natural enemy response to landscape complexity.
Ecology Letters 14, 922–932.
Clay, J. (2011). Freeze the footprint of food. Nature 475, 287–289.
Clough, Y., Holzschuh, A., Gabriel, D., Purtauf, T., Kleijn, D., Kruess,
A., Steffan-Dewenter, I. & Tscharntke, T. (2007). Alpha and beta diversity
of arthropods and plants in organically and conventionally managed wheat fields.
Journal of Applied Ecology 44, 804–812.
Clough, Y., Kruess, A., Kleijn, D. & Tscharntke, T. (2005). Spider diversity
in cereal fields: comparing factors at local, landscape and regional scales. Journal of
Biogeography 32, 2007–2014.
Cooper, H. & Hedges, L. V. (1994). The Handbook of Research Synthesis. Russell Sage
Foundation, New York.
Crawley, M. J. (2007). The R Book. John Wiley and Sons Ltd, Chichester.
Daily, G. C. (1997). Nature’s Services: Societal Dependence on Natural Ecosystems. Island
Press, Washington.
Delaplane, K. S. & Mayer, D. F. (2000). Crop Pollination by Bees. CABI, New York.
Drapela, T., Moser, D., Zaller, J. G. & Frank, T. (2008). Spider assemblages in
winter oilseed rape affected by landscape and site factors. Ecography 31, 254–262.
Duelli, P. & Obrist,M.K. (2003).Regional biodiversity in an agricultural landscape:
the contribution of seminatural habitat islands. Basic and Applied Ecology 4, 129–138.
Eilenberg, J., Hajek, A. & Lomer, C. (2001). Suggestions for unifying the
terminology in biological control. Biocontrol 46, 387–400.
Eilers, E. J. & Klein, A. M. (2009). Landscape context and management effects on
an important insect pest and its natural enemies in almond. Biological Control 51,
388–394.
Fahrig, L., Baudry, J., Brotons, L., Burel, F. G., Crist, T. O., Fuller, R. J.,
Sirami, C., Siriwardena, G. M. & Martin, J.-L. (2011). Functional landscape
heterogeneity and animal biodiversity in agricultural landscapes. Ecology Letters 14,
101–112.
Fiedler, A. K., Landis, D. A. & Wratten, S. D. (2008). Maximizing ecosystem
services from conservation biological control: the role of habitat management.
Biological Control 45, 254–271.
Firle, S., Bommarco, R., Ekbom, B. & Natiello, M. (1998). The influence of
movement and resting behavior on the range of three carabid beetles. Ecology 79,
2113–2122.
Forehand, L. M., Orr, D. B. & Linker, H.M. (2006). Evaluation of a commercially
available beneficial insect habitat for management of Lepidoptera pests. Journal of
Economic Entomology 99, 641–647.
Foresight (2011). The Future of Food and Farming: Final Project Report. The Government
Office for Science, London.
Free, J. B. (1993). Insect Pollination of Crops. Academic Press, London.
Gabriel, D., Sait, S. M., Hodgson, J. A., Schmutz, U., Kunin, W. E. & Benton,
T. G. (2010). Scale matters: the impact of organic farming on biodiversity at different
spatial scales. Ecology Letters 13, 858–869.
Gardiner, M. M., Landis, D. A., Gratton, C., DiFonzo, C. D., O’Neal, M.,
Chacon, J. M., Wayo, M. T., Schmidt, N. P., Mueller, E. E. & Heimpel, G.
E. (2009a). Landscape diversity enhances biological control of an introduced crop
pest in the north-central USA. Ecological Applications 19, 143–154.
Gardiner, M. M., Landis, D. A., Gratton, C., Schmidt, N., O’Neal, M.,
Mueller, E., Chacon, J., Heimpel, G. E. & DiFonzo, C. D. (2009b). Landscape
composition influences patterns of native and exotic lady beetle abundance. Diversity
and Distributions 15, 554–564.
Gardiner, M. M., Landis, D. A., Gratton, C., Schmidt, N., O’Neal, M.,
Mueller, E., Chacon, J. & Heimpel, G. E. (2010). Landscape composition
influences the activity density of Carabidae and Arachnida in soybean fields.
Biological Control 55, 11–19.
Garibaldi, L. A., Steffan-Dewenter, I., Kremen, C., Morales, J. M.,
Bommarco, R., Cunningham, S. A., Carvalheiro, L. G., Chacoff, N. P.,
Dudenhoffer, J.H., Greenleaf, S. S., Holzschuh, A., Isaacs, R., Krewenka,
K., Mandelik, Y., Mayfield,M.M., Morandin, L. A., Potts, S. G., Ricketts,
T. H., Szentgyorgyi, H., Viana, B. F., Westphal, C., Winfree, R. & Klein,
A. M. (2011). Stability of pollination services decreases with isolation from natural
areas despite honey bee visits. Ecology Letters 14, 1062–1072.
Gemmill-Herren, B. & Ochieng, A. O. (2008). Role of native bees and natural
habitats in eggplant (Solanum melongena) pollination in Kenya. Agriculture, Ecosystems &
Environment 127, 31–36.
Greenleaf, S. S. & Kremen, C. (2006a). Wild bee species increase tomato production
and respond differently to surrounding land use in Northern California. Biological
Conservation 133, 81–87.
Greenleaf, S. S. & Kremen, C. (2006b). Wild bees enhance honey bees’ pollination
of hybrid sunflower. Proceedings of the National Academy of Sciences of the United States of
America 103, 13890–13895.
Grundel, R., Jean, R. P., Frohnapple, K. J., Glowacki, G. A., Scott, P. E. &
Pavlovic, N. B. (2010). Floral and nesting resources, habitat structure, and fire influence bee distribution across an open-forest gradient. Ecological Applications 20,
1678–1692.
Gurevitch, J. & Hedges, L. V. (2001). Meta-analysis: combining the results of
independent experiments. In Design and Analysis of Ecological Experiments (eds S. M.
Scheiner and J. Gurevitch), pp. 347–369. Oxford University Press, New York.
Gurr, G. M., Wratten, S. D. & Luna, J. M. (2003). Multi-function agricultural
biodiversity: pest management and other benefits. Basic and Applied Ecology 4,
107–116.
Hagen, M. & Kraemer, M. (2010). Agricultural surroundings support flower-visitor
networks in an Afrotropical rain forest. Biological Conservation 143, 1654–1663.
Hagen, M., Wikelski, M. & Kissling, W. D. (2011). Space use of bumblebees
(Bombus spp.) revealed by radio-tracking. PLoS ONE 6, 1–10.
Hajek, A. E., Hannam, J. J., Nielsen, C., Bell, A. J. & Liebherr, J. K. (2007).
Distribution and abundance of Carabidae (Coleoptera) associated with soybean
aphid (Hemiptera: Aphididae) populations in central New York. Annals of the
Entomological Society of America 100, 876–886.
Hendrickx, F., Maelfait, J. P., Desender, K., Aviron, S., Bailey, D.,
Diekotter,T., Lens, L., Liira, J., Schweiger, O., Speelmans,M.,Vandomme,
V. & Bugter, R. (2009). Pervasive effects of dispersal limitation on within- and
among-community species richness in agricultural landscapes. Global Ecology and
Biogeography 18, 607–616.
Hoehn, P., Tscharntke, T., Tylianakis, J. M. & Steffan-Dewenter, I. (2008).
Functional group diversity of bee pollinators increases crop yield. Proceedings of the
Royal Society B: Biological Sciences 275, 2283–2291.
Hogg, B. N., Bugg, R. L. & Daane, K. M. (2011). Attractiveness of common
insectary and harvestable floral resources to beneficial insects. Biological Control 56,
76–84.
Holzschuh, A., Steffan-Dewenter, I. & Tscharntke, T. (2009). Grass strip
corridors in agricultural landscapes enhance nest-site colonization by solitary wasps.
Ecological Applications 19, 123–132.
Hothorn, T., Bretz, F. & Westfall, P. (2008). Simultaneous inference in general
parametric models. Biometrical Journal 50, 346–363.
Isaacs, R. & Kirk, A. K. (2010). Pollination services provided to small and large
highbush blueberry fields by wild and managed bees. Journal of Applied Ecology 47,
841–849.
Isaacs, R., Tuell, J., Fiedler, A., Gardiner, M. & Landis, D. (2009).Maximizing
arthropod-mediated ecosystem services in agricultural landscapes: the role of native
plants. Frontiers in Ecology and the Environment 7, 196–203.
Jervis,M. A. (2007). Insects as Natural Enemies: A Practical Perspective. Springer,Dordrecht.
Julier, H. E. & Roulston, T. H. (2009).Wild bee abundance and pollination service
in cultivated pumpkins: farm management, nesting behavior and landscape effects.
Journal of Economic Entomology 102, 563–573.
Kleijn, D., Rundlof, M., Scheper, J., Smith, H. G. & Tscharntke, T. (2011).
Does conservation on farmland contribute to halting the biodiversity decline? Trends
in Ecology & Evolution 26, 474–481.
Klein, A. M. (2009). Nearby rainforest promotes coffee pollination by increasing
spatio-temporal stability in bee species richness. Forest Ecology and Management 258,
1838–1845.
Klein, A. M., Steffan-Dewenter, I. & Tscharntke, T. (2006). Rain forest
promotes trophic interactions and diversity of trap-nesting hymenoptera in adjacent
agroforestry. Journal of Animal Ecology 75, 315–323.
Klein, A.M., Vaissi`ere, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham,
S. A., Kremen, C. & Tscharntke, T. (2007). Importance of pollinators in changing
landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274,
303–313.
Koh, L. P., Levang, P. & Ghazoul, J. (2009). Designer landscapes for sustainable
biofuels. Trends in Ecology & Evolution 24, 431–438.
Kremen, C. (2005). Managing ecosystem services: what do we need to know about
their ecology? Ecology Letters 8, 468–479.
Kremen, C. & Chaplin-Kramer, R. (2007). Insects as providers of ecosystem
services: crop pollination and pest control. In Insect Conservation Biology: Proceedings of
the Royal Entomological Society’s 23rd Symposium (eds A. J. A. Stewart, T. R. New and
O. T. Lewis), pp. 349–382. CABI Publishing, Wallingford.
Kremen, C. & Ostfeld, R. S. (2005). A call to ecologists: measuring, analyzing, and
managing ecosystem services. Frontiers in Ecology and the Environment 3, 540–548.
Kremen, C., Williams, N. M., Aizen, M. A., Gemmill-Herren, B., LeBuhn, G.,
Minckley, R., Packer, L., Potts, S. G., Roulston, T., Steffan-Dewenter,
I., Vazquez, D. P., Winfree, R., Adams, L., Crone, E. E., Greenleaf, S. S.,
Keitt, T. H., Klein, A. M., Regetz, J. & Ricketts, T. H. (2007). Pollination and
other ecosystem services produced by mobile organisms: a conceptual framework
for the effects of land-use change. Ecology Letters 10, 299–314.
Kremen, C., Williams, N. M., Bugg, R. L., Fay, J. P. & Thorp, R. W. (2004).
The area requirements of an ecosystem service: crop pollination by native bee
communities in California. Ecology Letters 7, 1109–1119.
Kremen, C., Williams, N. M. & Thorp, R. W. (2002). Crop pollination from
native bees at risk from agricultural intensification. Proceedings of the National Academy
of Sciences of the United States of America 99, 16812–16816.
Landis, D. A., Wratten, S. D. & Gurr, G. M. (2000). Habitat management to
conserve natural enemies of arthropod pests in agriculture. Annual Review of Entomology
45, 175–201.
Lawton, J. H. & Brown, V. K. (1993). Redundancy in ecosystems. In Biodiversity and
Ecosystem Function (eds E. D. Schulze and H. A. Mooney), pp. 225–270. Springer,
New York.
Lee, J. C. & Heimpel, G. E. (2005). Impact of flowering buckwheat on Lepidopteran
cabbage pests and their parasitoids at two spatial scales. Biological Control 34, 290–301.
Letourneau, D. K., Armbrecht, I., Rivera, B. S., Lerma, J. M., Carmona, E. J.,
Daza, M. C., Escobar, S., Galindo, V., Gutierrez, C., Lopez, S. D., Mejia,
J. L., Rangel, A. M. A., Rangel, J. H., Rivera, L., Saavedra, C. A., Torres,
A. M. & Trujillo, A. R. (2011). Does plant diversity benefit agroecosystems? A
synthetic review. Ecological Applications 21, 9–21.
Letourneau, D. K. & Bothwell, S. G. (2008). Comparison of organic and
conventional farms: challenging ecologists to make biodiversity functional. Frontiers
in Ecology and the Environment 6, 430–438.
Letourneau, D. K., Jedlicka, J. A., Bothwell, S. G. & Moreno, C. R. (2009).
Effects of natural enemy biodiversity on the suppression of arthropod herbivores in
terrestrial ecosystems. Annual Review of Ecology, Evolution, and Systematics 40, 573–592.
Losey, J. E. & Denno, R. F. (1998). Positive predator-predator interactions: enhanced
predation rates and synergistic suppression of aphid populations. Ecology 79,
2143–2152.
Luck, G. W., Harrington, R., Harrison, P. A., Kremen, C., Berry, P. M.,
Bugter, R., Dawson, T. P., de Bello, F., Diaz, S., Feld, C. K., Haslett, J.
R., Hering, D., Kontogianni, A., Lavorel, S., Rounsevell, M., Samways,
M. J., Sandin, L., Settele, J., Sykes, M. T., van den Hove, S., Vandewalle,
M. & Zobel, M. (2009). Quantifying the contribution of organisms to the provision
of ecosystem services. Bioscience 59, 223–235.
Marshall, E. J. P., West, T. M. & Kleijn, D. (2006). Impacts of an agrienvironment
field margin prescription on the flora and fauna of arable farmland in
different landscapes. Agriculture, Ecosystems & Environment 113, 36–44.
Martins, D. J. & Johnson, S. D. (2009). Distance and quality of natural habitat
influence hawkmoth pollination of cultivated papaya. International Journal of Tropical
Insect Science 29, 114–123.
McNaughton, S. J. (1977). Diversity and stability of ecological communities: a
comment on the role of empiricism in ecology. American Naturalist 111, 515–525.
MEA (2005). Ecosystems and Human Well-Being: Synthesis. Island Press, Washington.
Menalled, F. D., Lee, J. C. & Landis, D. A. (1999). Manipulating carabid beetle
abundance alters prey removal rates in corn fields. Biocontrol 43, 441–456.
Michener, C. D. (2007). The Bees of the World. Second Edition. The Johns Hopkins
University Press, Baltimore.
Miliczky, E. R. & Horton, D. R. (2005). Densities of beneficial arthropods within
pear and apple orchards affected by distance from adjacent native habitat and
association of natural enemies with extra-orchard host plants. Biological Control 33,
249–259.
Morandin, L. A. & Winston, M. L. (2006). Pollinators provide economic incentive
to preserve natural land in agroecosystems. Agriculture, Ecosystems & Environment 116,
289–292.
Morandin, L. A., Winston, M. L., Abbott, V. A. & Franklin,M. T. (2007). Can
pastureland increase wild bee abundance in agriculturally intense areas? Basic and
Applied Ecology 8, 117–124.
Nakagawa, S. & Cuthill, I. C. (2007). Effect size, confidence interval and statistical
significance: a practical guide for biologists. Biological Reviews 82, 591–605.
Nash, M. A., Thomson, L. J. & Hoffmann, A. A. (2008). Effect of remnant
vegetation, pesticides, and farm management on abundance of the beneficial
predator Notonomus gravis (Chaudoir) (Coleoptera: Carabidae). Biological Control 46,
83–93.
Oberg, S., Mayr, S. & Dauber, J. (2008). Landscape effects on recolonisation
patterns of spiders in arable fields. Agriculture, Ecosystems&Environment 123, 211–218.
Otieno, M., Woodcock, B. A., Wilby, A., Vogiatzakis, I. N., Mauchline, A.
L., Gikungu, M. W. & Potts, S. G. (2011). Local management and landscape
drivers of pollination and biological control services in a Kenyan agro-ecosystem.
Biological Conservation 144, 2424–2431.
Palmer, M., Bernhardt, E., Chornesky, E., Collins, S., Dobson, A., Duke, C.,
Gold, B., Jacobson, R., Kingsland, S., Kranz, R., Mappin, M., Martinez,
M. L., Micheli, F., Morse, J., Pace, M., Pascual, M., Palumbi, S., Reichman,
O. J., Simons, A., Townsend, A. & Turner, M. (2004). Ecology for a crowded
planet. Science 304, 1251–1252.
Pease, C. G. & Zalom, F. G. (2010). Influence of non-crop plants on stink bug
(Hemiptera: Pentatomidae) and natural enemy abundance in tomatoes. Journal of
Applied Entomology 134, 626–636.
Pinheiro, J., Bates, D., DebRoy, S. & Sarkar, D., R Development Core Team
(2010). nlme: linear and nonlinear mixed effects models. R package version 3.1-97.
Pluess, T., Opatovsky, I., Gavish-Regev, E., Lubin, Y. & Schmidt-Entling,
M. H. (2010). Non-crop habitats in the landscape enhance spider diversity in wheat
fields of a desert agroecosystem. Agriculture, Ecosystems & Environment 137, 68–74.
Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O. &
Kunin, W. E. (2010). Global pollinator declines: trends, impacts and drivers. Trends
in Ecology & Evolution 25, 345–353.
Potts, S. G., Vulliamy, B., Dafni, A., Ne’eman, G. & Willmer, P. (2003). Linking
bees and flowers: how do floral communities structure pollinator communities?
Ecology 84, 2628–2642.
Pretty, J., Toulmin, C. & Williams, S. (2011). Sustainable intensification in
African agriculture. International Journal of Agricultural Sustainability 9, 5–24.
Prieto-Benítez, S. & M´endez, M. (2011). Effects of land management on the
abundance and richness of spiders (Araneae): a meta-analysis. Biological Conservation
144, 683–691.
Pywell, R. F., James, K. L., Herbert, I., Meek, W. R., Carvell, C., Bell, D.
& Sparks, T. H. (2005). Determinants of overwintering habitat quality for beetles
and spiders on arable farmland. Biological Conservation 123, 79–90.
Raudsepp-Hearne, C., Peterson, G. D. & Bennett, E. M. (2010). Ecosystem
service bundles for analyzing tradeoffs in diverse landscapes. Proceedings of the National
Academy of Sciences of the United States of America 107, 5242–5247.
R Development Core Team (2010). R: A Language and Environment for Statistical
Computing. R Foundation for Statistical Computing, Vienna.
Ricketts, T. H. (2004). Tropical forest fragments enhance pollinator activity in
nearby coffee crops. Conservation Biology 18, 1262–1271.
Ricketts, T. H., Daily, G. C., Ehrlich, P. R. & Michener, C. D. (2004).
Economic value of tropical forest to coffee production. Proceedings of the National
Academy of Sciences of the United States of America 101, 12579–12582.
Ricketts, T. H., Regetz, J., Steffan-Dewenter, I., Cunningham, S. A.,
Kremen, C., Bogdanski, A., Gemmill-Herren, B., Greenleaf, S. S., Klein,
A. M., Mayfield, M. M., Morandin, L. A., Ochieng, A. & Viana, B. F. (2008).
Landscape effects on crop pollination services: are there general patterns? Ecology
Letters 11, 499–515.
Roschewitz, I., Hucker, M., Tscharntke, T. & Thies, C. (2005). The influence
of landscape context and farming practices on parasitism of cereal aphids. Agriculture,
Ecosystems & Environment 108, 218–227.
Rosenberg, M. S. (2005). The file-drawer problem revisited: a general weighted
method for calculating fail-safe numbers in meta-analysis. Evolution 59, 464–468.
Rosenheim, J. A., Kaya, H. K., Ehler, L. E., Marois, J. J. & Jaffee, B. A. (1995).
Intraguild predation among biological-control agents: theory and evidence. Biological
Control 5, 303–335.
Roulston, T. H. & Goodell, K. (2011). The role of resources and risks in regulating
wild bee populations. Annual Review of Entomology 56, 293–312.
Rundlof, M., Nilsson, H. & Smith, H. G. (2008). Interacting effects of farming
practice and landscape context on bumblebees. Biological Conservation 141, 417–426.
Sanchez, P. A. (2010). Tripling crop yields in tropical Africa. Nature Geoscience 3,
299–300.
Saska, P., Vodde, M., Heijerman, T., Westerman, P. & van der Werf, W.
(2007). The significance of a grassy field boundary for the spatial distribution of
carabids within two cereal fields. Agriculture, Ecosystems & Environment 122, 427–434.
Schmidt, M. H., Roschewitz, I., Thies, C. & Tscharntke, T. (2005). Differential
effects of landscape and management on diversity and density of ground-dwelling
farmland spiders. Journal of Applied Ecology 42, 281–287.
Schmidt, M. H., Thies, C., Nentwig, W. & Tscharntke, T. (2008). Contrasting
responses of arable spiders to the landscape matrix at different spatial scales. Journal
of Biogeography 35, 157–166.
Schmidt-Entling, M. H. & Dobeli, J. (2009). Sown wildflower areas to enhance
spiders in arable fields. Agriculture, Ecosystems & Environment 133, 19–22.
Sharpe, D. (1997). Of apples and oranges, file drawers and garbage: why validity
issues in meta-analysis will not go away. Clinical Psychology Review 17, 881–901.
Stallman, H. R. (2011). Ecosystem services in agriculture: determining suitability for
provision by collective management. Ecological Economics 71, 131–139.
Steffan-Dewenter, I. (2003). Importance of habitat area and landscape context
for species richness of bees and wasps in fragmented orchard meadows. Conservation
Biology 17, 1036–1044.
Steffan-Dewenter, I., Munzenberg, U., Burger, C., Thies, C. & Tscharntke,
T. (2002). Scale-dependent effects of landscape context on three pollinator guilds.
Ecology 83, 1421–1432.
Steingr¨over, E. G., Geertsema, W. & van Wingerden, W. K. R. E. (2010).
Designing agricultural landscapes for natural pest control: a transdisciplinary
approach in the Hoeksche Waard (The Netherlands). Landscape Ecology 25, 825–838.
Straub, C. S. & Snyder, W. E. (2006). Species identity dominates the relationship
between predator biodiversity and herbivore suppression. Ecology 87, 277–282.
Suter,R. B. (1999).An aerial lottery: the physics of ballooning in a chaotic atmosphere.
Journal of Arachnology 27, 281–293.
Symondson, W. O. C., Sunderland, K. D. & Greenstone, M. H. (2002). Can
generalist predators be effective biocontrol agents? Annual Review of Entomology 47,
561–594.
Taki, H., Okabe, K., Yamaura, Y., Matsuura, T., Sueyoshi, M., Makino, S. &
Maeto, K. (2010). Effects of landscape metrics on Apis and non-Apis pollinators and
seed set in common buckwheat. Basic and Applied Ecology 11, 594–602.
Thomson, L. J. & Hoffmann, A. A. (2010). Natural enemy responses and pest
control: importance of local vegetation. Biological Control 52, 160–166.
Thomson, L. J., McKenzie, J., Sharley, D. J., Nash, M. A., Tsitsilas, A. &
Hoffmann, A. A. (2010). Effect of woody vegetation at the landscape scale on the
abundance of natural enemies in Australian vineyards. Biological Control 54, 248–254.
Tilman, D. (1999). The ecological consequences of changes in biodiversity: a search
for general principles. Ecology 80, 1455–1474.
Tilman, D., Balzer, C., Hill, J. & Befort, B. L. (2011). Global food demand
and the sustainable intensification of agriculture. Proceedings of the National Academy of
Sciences of the United States of America 108, 20260–20264.
Tscharntke, T., Bommarco, R., Clough, Y., Crist, T. O., Kleijn, D., Rand,
T. A., Tylianakis, J. M., van Nouhuys, S. & Vidal, S. (2007). Conservation
biological control and enemy diversity on a landscape scale. Biological Control 43,
294–309.
Tscharntke, T., Klein, A. M., Kruess, A., Steffan-Dewenter, I. & Thies,
C. (2005). Landscape perspectives on agricultural intensification and biodiversityecosystem
service management. Ecology Letters 8, 857–874.
Tscharntke, T., Tylianakis, J. M., Rand, T. A., Didham, R. K., Fahrig,
L., Bat´ary, P., Bengtsson, J., Clough, Y., Crist, T. O., Dormann, C.
F., Ewers, R. M., Fr¨und, J., Holt, R. D., Holzschuh, A., Klein, A. M.,
Kleijn, D., Kremen, C., Landis, D. A., Laurance, W., Lindenmayer, D.,
Scherber, C., Sodhi, N., Steffan-Dewenter, I., Thies, C., van der Putten,
W. H. & Westphal, C. (2012). Landscape moderation of biodiversity patterns and
processes – eight hypotheses. Biological Reviews 87, 661–685.
Tuell, J. K., Ascher, J. S. & Isaacs, R. (2009). Wild bees (Hymenoptera: Apoidea:
Anthophila) of the Michigan highbush blueberry agroecosystem. Annals of the
Entomological Society of America 102, 275–287.
Vaissi`ere, B. E., Freitas, B. M. & Gemmill-Herren, B. (2011). Protocol to Detect and
Assess Pollination Deficits in Crops: A Handbook for its Use. FAO, Rome.
Varchola, J. M. & Dunn, J. P. (2001). Influence of hedgerow and grassy field
borders on ground beetle (Coleoptera: Carabidae) activity in fields of corn. Agriculture,
Ecosystems & Environment 83, 153–163.
Viechtbauer, W. (2010). Conducting meta-analyses in R with the metafor package.
Journal of Statistical Software 36, 1–48.
Vollhardt, I. M. G., Tscharntke, T., W¨ackers, F. L., Bianchi, F. & Thies,
C. (2008). Diversity of cereal aphid parasitoids in simple and complex landscapes.
Agriculture, Ecosystems & Environment 126, 289–292.
W¨ackers, F. L. (2004). Assessing the suitability of flowering herbs as parasitoid food
sources: flower attractiveness and nectar accessibility. Biological Control 29, 307–314.
W¨ackers, F. L. & van Rijn, P. C. J. (2005). Food for protection: an introduction. In
Plant-Provided Food for Carnivorous Insects: A Protective Mutualism and its Applications (eds
F. L. W¨ackers, P. C. J. van Rijn and J. Bruin), pp. 1–14. Cambridge University
Press, Cambridge.
Westerkamp, C. & Gottsberger, G. (2000). Diversity pays in crop pollination.
Crop Science 40, 1209–1222.
Westphal, C., Steffan-Dewenter, I. & Tscharntke, T. (2003). Mass flowering
crops enhance pollinator densities at a landscape scale. Ecology Letters 6, 961–965.
Westrich, P. (1996).Habitat requirements of central European bees and the problems
of partial habitats. In The Conservation of Bees (eds A. Matheson, S. L. Buchmann,
C. O’Toole, P. Westrich and I. H. Williams), pp. 1–16. Academic Press,
London.
Winfree, R., Aguilar, R., Vazquez, D. P., LeBuhn, G. & Aizen, M. A.
(2009). A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology
90, 2068–2076.
Winfree, R., Griswold, T. & Kremen, C. (2007). Effect of human disturbance on
bee communities in a forested ecosystem. Conservation Biology 21, 213–223.
Winfree, R. & Kremen, C. (2009). Are ecosystem services stabilized by differences
among species? A test using crop pollination. Proceedings of the Royal Society B: Biological
Sciences 276, 229–237.
Wyckhuys, K. A. G. & O’Neil, R. J. (2007). Influence of extra-field characteristics
to abundance of key natural enemies of Spodoptera frugiperda Smith (Lepidoptera:
Noctuidae) in subsistence maize production. International Journal of Pest Management
53, 89–99.
Yachi, S. & Loreau, M. (1999). Biodiversity and ecosystem productivity in a
fluctuating environment: the insurance hypothesis. Proceedings of the National Academy
of Sciences of the United States of America 96, 1463–1468.
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. & Smith, G. M. (2009).
Mixed Effects Models and Extensions in Ecology with R. Springer. University Staff: Request a correction | Centaur Editors: Update this record |
University of Reading
CentAUR: Central Archive at the University of Reading
Accessibility navigation
Comparison of pollinators and natural enemies: a meta-analysis of landscape and local effects on abundance and richness in crops
Shackelford, G., Steward, P.R., Benton, T.G., Kunin, W.E., Potts, S. G. Full text not archived in this repository. It is advisable to refer to the publisher's version if you intend to cite from this work. See Guidance on citing. To link to this item DOI: 10.1111/brv.12040 Abstract/SummaryTo manage agroecosystems for multiple ecosystem services, we need to know whether the management of one service has positive, negative, or no effects on other services. We do not yet have data on the interactions between pollination and pest-control services. However, we do have data on the distributions of pollinators and natural enemies in agroecosystems. Therefore, we compared these two groups of ecosystem service providers, to see if the management of farms and agricultural landscapes might have similar effects on the abundance and richness of both. In a meta-analysis, we compared 46 studies that sampled bees, predatory beetles, parasitic wasps, and spiders in fields, orchards, or vineyards of food crops. These studies used the proximity or proportion of non-crop or natural habitats in the landscapes surrounding these crops (a measure of landscape complexity), or the proximity or diversity of non-crop plants in the margins of these crops (a measure of local complexity), to explain the abundance or richness of these beneficial arthropods. Compositional complexity at both landscape and local scales had positive effects on both pollinators and natural enemies, but different effects on different taxa. Effects on bees and spiders were significantly positive, but effects on parasitoids and predatory beetles (mostly Carabidae and Staphylinidae) were inconclusive. Landscape complexity had significantly stronger effects on bees than it did on predatory beetles and significantly stronger effects in non-woody rather than in woody crops. Effects on richness were significantly stronger than effects on abundance, but possibly only for spiders. This abundance-richness difference might be caused by differences between generalists and specialists, or between arthropods that depend on non-crop habitats (ecotone species and dispersers) and those that do not (cultural species). We call this the ‘specialist-generalist’ or ‘cultural difference’ mechanism. If complexity has stronger effects on richness than abundance, it might have stronger effects on the stability than the magnitude of these arthropod-mediated ecosystem services. We conclude that some pollinators and natural enemies seem to have compatible responses to complexity, and it might be possible to manage agroecosystems for the benefit of both. However, too few studies have compared the two, and so we cannot yet conclude that there are no negative interactions between pollinators and natural enemies, and no trade-offs between pollination and pest-control services. Therefore, we suggest a framework for future research to bridge these gaps in our knowledge.
Altmetric Deposit Details References University Staff: Request a correction | Centaur Editors: Update this record |
Lists
Lists
