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Selecting native perennial plants for ecological intensification in Mediterranean greenhouse horticulture

Published online by Cambridge University Press:  04 December 2017

E. Rodríguez ,
M. González ,
D. Paredes ,
M. Campos  and
E. Benítez
E. Rodríguez*
Affiliation:
IFAPA, La Mojonera- Centre, Almería, Spain
M. González
Affiliation:
Cajamar- Experimental Station ‘Las Palmerillas’, El Ejido, Almería, Spain
D. Paredes
Affiliation:
Department of Environmental Protection, Zaidín-Experimental Station (EEZ), CSIC, Granada, Spain
M. Campos
Affiliation:
Department of Environmental Protection, Zaidín-Experimental Station (EEZ), CSIC, Granada, Spain
E. Benítez
Affiliation:
Department of Environmental Protection, Zaidín-Experimental Station (EEZ), CSIC, Granada, Spain
*
*Author for correspondence Phone: +34950156453 Fax: +34950558055 E-mail: [email protected]
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Abstract

Natural control by predators and parasitoids provides an important and often unnoticed ecosystem service to agricultural landscapes by reducing pest populations in crops. The current model of horticultural intensification in south-eastern Spain produces high yields but has also resulted in a landscape almost completely covered by plastic. Promoting natural areas among greenhouses could enhance biodiversity, by being beneficial insects, and reduce pest pressure outdoors. The first step is to ascertain how pests and their natural enemies (NEs) use Mediterranean vegetation for selecting the best plants for pest suppression outdoors. The abundance of the two major horticultural pests, the tobacco whitefly, Bemisia tabaci, and the western flower thrips, Frankliniella occidentalis, together with their NEs, were assayed in 22 flowering perennial plants, which were newly planted in an experimental field surrounded by greenhouses. Eight plant species were identified as the most critical species for sustaining pest populations outdoors. A set of five plant species supported a medium level of pests, and another set of ten plant species supported the lowest level of both pests. Tobacco whitefly occurred in a few plants species, whereas western flower thrips occurred on almost all the plant species studied, and was favoured by the presence of flowers in perennial plants. The results suggest that plant diversity may provide relatively few acceptable host plants for tobacco whitefly than for western flower thrips. NEs were generally collected in plants that also supported abundance of pests, indicating that host/prey availability, more than food resources from flowers, was a stronger predictor of NE abundance in perennial plants. Field trials using the plants with the lowest host acceptance by pests are needed in order to ascertain whether pest abundance outdoors is reduced.

Keywords

bottom–up effectconservation biocontrolwestern flower thripstobacco whiteflytop–down effect
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 5 , October 2018 , pp. 694 - 704
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Copyright
Copyright © Cambridge University Press 2017 

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References

Aguilar-Fenollosa, E., Ibáñez-Gual, M.V., Pascual-Ruiz, S., Hurtado, M. & Jacas, J.A. (2011) Effect of ground-cover management on spider mites and their phytoseiid natural enemies in clementine mandarin orchards (I): bottom-up regulation mechanisms. Biological Control 59, 158–170.Google Scholar
Allsopp, E. (2010) Seasonal occurrence of Western flower thrips, Frankliniella occidentalis (Pergande), on table grapes in the Hex River Valley, South Africa. South African Journal of Enology and Viticulture 31(1), 49–57.Google Scholar
Batary, P., Matthiesen, T. & Tscharntke, T. (2010) Landscape-moderated importance of hedges in conserving farmland bird diversity of organic vs. conventional croplands and grasslands. Biological Conservation 143, 2020–2027.Google Scholar
Bates, D., Maechler, M., Bolker, B. & Walker, S. (2014) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67(1), 1–48.Google Scholar
Bianchi, F.J.J.A., Booij, C.J.H. & Tscharntke, T. (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proceedings of the Royal Society of London B 273, 1715–1727. doi: 10.1098/rspb.2006.3530.Google Scholar
Bianchi, F.J.J.A., Shellhorn, N.A. & Cunningham, S.A. (2013) Habitat functionality for the ecosystem service of pest control: reproduction and feeding sites of pests and natural enemies. Agricultural and Forest Entomology 15, 12–23.Google Scholar
Biondi, A., Zappalà, L., Di Mauro, A., Garzia, G.T., Russo, A., Desneux, N. & Siscaro, G. (2016) Can alternative host plant and prey affect phytophagy and biological control by the zoophytophagous mirid Nesidiocoris tenuis? Biocontrol 6 (1), 79–90. doi: 10.1007/s10526-015-9700-5.Google Scholar
Bommarco, R., Kleijn, D. & Potts, S.G. (2013) Ecological intensification: harnessing ecosystem services for food security. Trends in Ecology and Evolution 28, 230–238. doi: 10.1016/j.tree.2012.10.012.Google Scholar
Bugg, R.L. (1987) Observations on insects associated with a nectar-bearing Chilean tree, Quillaja-saponaria molina (Rosaceae). Pan-Pacific Entomologist 63, 60–64.Google Scholar
Burel, F., Lavigne, C., Marshall, E.J.P., Moonen, A.C., Ouin, A. & Poggio, S.L. (2013) Landscape ecology and biodiversity in agricultural landscapes. Agriculture, Ecosystems and Environment 166, 1–2.Google Scholar
Burnham, K.P. & Anderson, D.R. (2002) Model Selection and Multimodel Inference: A Practical Information-theoretic Approach. Springer-Verlag, New York.Google Scholar
Calvo, F.J., Knapp, M., van Houten, Y.M., Hoogerbrugge, H. & Belda, J.E. (2015) Amblyseius swirskii: what made this predatory mite such a successful biocontrol agent? Experimental and Applied Acarology 65, 419. doi: 10.1007/s10493-014-9873-0.Google Scholar
Canham, C.D. & Uriarte, M. (2006) Analysis of neighborhood dynamics of forest ecosystems using likelihood methods and modeling. Ecological Applications 16, 62–73.Google Scholar
Cano, M., Vila, E., Janssen, D., Bretones, G., Salvador, E., Lara, L. & Téllez, M. (2009) Selection of refuges for Nesidiocoris tenuis (Het.: Miridae) and Orius laevigatus (Het.:Antohocoridae): virus reservoir risk assessment. IOBC/WPRS Bulletin 49, 281–286.Google Scholar
Cockfield, S.D., Beers, E.H. & Zack, R.S. (2007) Phenology of western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) on plant species in and near apple orchards in Washington State. Journal of the Entomological Society of British Columbia 104, 35–44.Google Scholar
Dainese, M., Inclán-Luna, D., Sitzia, T., Sigura, M. & Marini, L. (2015) Testing scale-dependent effects of seminatural habitats on farmland biodiversity. Ecological Applications 25, 1681–1690. doi: 10.1890/14-1321.1.Google Scholar
Dainese, M., Montecchiari, S., Sitzia, T., Sigura, M. & Marini, L. (2016) High cover of hedgerows in the landscape supports multiple ecosystem services in Mediterranean cereal fields. Journal of Applied Ecology 54(2), 380–388.Google Scholar
Danne, A., Thomson, L.J., Sharley, D.J., Penfold, C.M. & Hoffmann, A.A. (2010) Effects of native grass cover crops on beneficial and pest invertebrates in Australian vineyards. Environmental Entomology 39(3), 970–978.Google Scholar
Fiedler, A.K. & Landis, D.A. (2007 a) Attractiveness of Michigan native plants to arthropod natural enemies and herbivores. Environmental Entomology 36(4), 751–765.Google Scholar
Fiedler, A.K. & Landis, D.A. (2007 b) Plant characteristics associated with natural enemy abundance at Michigan native plants. Environmental Entomology 36(4), 878–886.Google Scholar
Finch, S. & Collier, R.H. (2000) Host-plant selection by insects- a theory based on ‘appropriate/inappropriate landings’ by pest insects of cruciferous plants. Entomologia Experimentalis et Applicata 96, 91–102.Google Scholar
Gaba, S., Bretagnolle, F., Rigaud, T. & Philippot, L. (2014) Managing biotic interactions for ecological intensification of agroecosystems. Frontiers in Ecology and Evolution 2, 29. doi: 10.3389/fevo.2014.00029.Google Scholar
Gareau, T.L.P., Letourneau, D.K. & Shennan, C. (2013) Relative densities of natural enemy and pest insects within California hedgerows. Environmental Entomology 42(4), 688–702.Google Scholar
Gilbertson, R.L., Batuman, O., Webster, C.G. & Adkins, S. (2015) Role of the Insect Supervectors Bemisia tabaci and Frankliniella occidentalis in the emergence and global spread of plant viruses. Annual Review of Virology 2, 67–93.Google Scholar
Glass, R. & González, F.J.E. (2012) Biological control in the greenhouses of Almeria and challenges for a sustainable intensive production. Outlooks on Pest Management 23(6), 276–279.Google Scholar
Griffiths, G.J.K., Holland, J.M., Bailey, A. & Thomas, M.B. (2008) Efficacy and economics of shelter habitats for conservation biological control. Biological Control 45, 200–209.Google Scholar
Gurr, G.M., Lu, Z., Zheng, X., Xu, H., Zhu, P., Chen, G., Yao, X., Cheng, J., Zhu, Z., Catindig, J.L., Villareal, S., Chien, H.V., Cuong, L.Q., Channoo, C., Chengwattana, N., Lan, L.P., Hai, L.H., Chaiwong, J., Nicol, H.I., Perovic, D. J., Wratten, S D. & Luen Heong, K. (2016) Multi-country evidence that crop diversification promotes ecological intensification of agriculture. Nature Plants 2, 16014.Google Scholar
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.Google Scholar
Haenke, S., Kovács-Hostyánszki, A., Frund, J., Batary, P., Jauker, B., Tscharntke, T. & Holzschuh, A. (2014) Landscape configuration of crops and hedgerows drives local syrphid fly abundance. Journal of Applied Ecology 51, 505–513. doi: 10.1111/1365-2664.12221.Google Scholar
Hannon, L.E. & Sisk, T.D. (2009) Hedgerows in an agri-natural land-scape: potential habitat value for native bees. Biological Conservation 142, 2140–2154.Google Scholar
Hartig, F. (2016) DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R package version 0.1.0.Google Scholar
Henri, D.C., Jones, O., Tsiattalos, A., Thébault, E., Seymour, C.L. & van Veen, F.J.F. (2015) Natural vegetation benefits synergistic control of the three main insect and pathogen pests of a fruit crop in Southern Africa. Journal of Applied Ecology 52, 1092–1101. doi: 10.1111/1365-2664.12465.Google Scholar
Hothorn, T., Bretz, F., Westfall, P., Heiberger, R.M., Schuetzenmeister, A. & Scheibe, S. (2016) Multcomp: Simultaneous Inference in General Parametric Models – R Package Version 1.4-6.Google Scholar
Inbar, M. & Gerling, D. (2008) Plant-mediated interactions between whiteflies, herbivores, and natural enemies. Annual Review of Entomology 53, 431–448.Google Scholar
Johnson, J.B. & Omland, K.S. (2004) Model selection in ecology and evolution. Trends in Ecology and Evolution 19, 101–108.Google Scholar
Kiman, Z.B. & Yeargan, K.V. (1985) Development and reproduction of the predator Orius insidiosus (Hemiptera, Anthocoridae) reared on diets of selected plant-material and arthropod prey. Annals of the Entomological Society of America 78, 464–467.Google Scholar
Lacasa, A., Sánchez, J.A. & Lorca, M. (1996) Aspectos ecológicos de los parásitos de los tisanópteros en España. Boletín de Sanidad Vegetal y Plagas 22, 339–349.Google Scholar
Landis, E.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.Google Scholar
Lavandero, B.I., Wratten, S.D., Didham, R.K. & Gurr, G.M. (2006) Increasing floral diversity for selective enhancement of biological control agents: a double-edged sword? Journal of Basic and Applied Biology 7, 236–243.Google Scholar
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. doi: 10.1146/annurev.ecolsys.110308.120320.Google Scholar
Lewis, T. (1997) Thrips as Crop Pests. Wallingford, UK, CABI.Google Scholar
Lozano, R., Diánez, F. & Camacho, F. (2010) Evolution of the phytosanitary control system in the intensive horticulture model of high yield in Almería (2005–2008). Journal of Food Agriculture and Environment 8(2), 330–338.Google Scholar
Lundgren, J.G., Fergen, J.K. & Riedell, W.E. (2008) The influence of plant anatomy on oviposition and reproductive success of the omnivorous bug Orius insidiosus. Animal Behaviour 75, 1495–1502.Google Scholar
MacLeod, M. & Winfree, R. (2011) Pollinators and natural enemies show different preferences for native plant species. 59th Annual Meeting of ESA, Reno 13–16 November 2011 Nevada, The Entomological Society of America.Google Scholar
Mendoza-Fernández, A.J., Martínez-Hernández, J., Pérez-García, F.J., Garrido-Becerra, J.A., Benito, B.M., Salmerón-Sánchez, E., Guirado, J., Merlo, M.E. & Mota, J.F. (2015) Extreme habitat loss in a Mediterranean habitat: Maytenus senegalensis subsp. Europaea. Plant Biosystem 149(3), 503–511.Google Scholar
Miliczky, E. & Horton, D. (2011) Occurrence of the Western flower thrips, Frankliniella occidentalis, and potential predators on host plants in near- orchard habitats of Washington and Oregon (Thysanoptera: Thripidae). Journal of the Entomological Society of British Columbia 108, 11–28.Google Scholar
Moradin, L.A. & Kremen, C. (2013) Hedgerow restoration promotes pollinator populations and exports native bees to adjacent fields. Ecological Applications 23, 829–839.Google Scholar
Moradin, L.A., Long, R.F. & Kremen, C. (2014) Hedgerows enhance beneficial insects on adjacent tomato fields in an intensive agriculture landscape. Agriculture, Ecosystems and Environment 189, 164–170.Google Scholar
Nakagawa, S. & Schielzeth, H. (2013) A general and simple method for obtaining R 2 from generalized linear mixed effect models. Methods in Ecology and Evolution 4, 283–294.Google Scholar
Park, M.G., Blitzer, E.J., Gibbs, J., Losey, J.E. & Danforth, B.N. (2015) Negative effects of pesticides on wild bee communities can be buffered by landscape context. Proceedings of the Royal Society of London B: Biological Sciences 282, 1809. doi: 10.1098/rspb.2015.0299.Google Scholar
Pérez-Mesa, J.C. & Galdeano-Gómez, E. (2010) Agrifood cluster and transfer of technology in the Spanish vegetables exporting sector: the role of multinational enterprises. Agricultural Economics 56(10), 478–488.Google Scholar
Piñero, F.S., Tinaut, A., Aguirre-Segura, A., Miñano, J., Lencina, J.L., Ortiz-Sánchez, F.J. & Pérez-López, F.J. (2011) Terrestrial arthropod fauna of arid areas of SE Spain: diversity, biogeography, and conservation. Journal of Arid Environment 75, 1321–1332.Google Scholar
Pollard, K.A. & Holland, J.M. (2006) Arthropods within the woody element of hedgerows and their distribution pattern. Agriculture for Entomology 8, 230–211.Google Scholar
R Development Core Team (2014) R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing. Available online at http://www.R-project.org.Google Scholar
Rebek, E.J., Sadof, C.A. & Hanks, L.M. (2005) Manipulating the abundance of natural enemies in ornamental landscapes with floral resource plants. Biological Control 33, 203–216.Google Scholar
Rencken, I.C. (2006) An investigation of the importance of native and non-crop vegetation in beneficial generalist predators in Australian cotton agroecosystems. PhD Thesis, University of New England, Armidale, Australia.Google Scholar
Ripa, R., Funderburk, J., Rodríguez, F., Espinoza, F. & Mound, L. (2009) Population abundance of Frankliniella occidentalis (Thysanoptera: Thripidae) and natural enemies on plant hosts in central Chile. Environmental Entomology 38(2), 333–344. doi: 10.1603/022.038.0205.Google Scholar
Rodríguez, E., Schwarzer, V., van der Blom, J. & González, M. (2012) The selection of insectary plants for landscaping in greenhouse areas of SE Spain. IOBC/WPRS Bulletin 75, 73–76.Google Scholar
Rodríguez, E., van der Blom, J., González, M., Sánchez, E., Janssen, D., Ruiz, L. & Elorrieta, M.A. (2014) Plant viruses and native vegetation in Mediterranean greenhouse areas. Scientia Horticulturae 165, 171–174.Google Scholar
Sánchez, J.A., Martínez-Cascales, J.I. & Lacasa, A. (2003) Abundance and wild host plants of predator mirids (Heteroptera: Miridae) in horticultural crops in the Southeast of Spain. IOBC/WPRS Bulletin 26, 147–151.Google Scholar
Schellhorn, N.A. & Bianchi, F.J.J.A. (2010) The role of forests in capturing the ecosystem service of pest control: a pathway to integrate pest control and biodiversity conservation. pp. 43–49 in Koizumi, T., Okabe, K., Thompson, I., Sugimora, K., Toma, T. & Fujita, K. (Eds) The Role of Forest Biodiversity in the Sustainable Use of Ecosystem Goods and Services in Agro-forestry, Fisheries, and Forestry: Proceedings of International Symposium for the Convention on Biological Diversity, 26–29 April 2010, Tokyo, Japan. Forest and Forest Products Researche Institute.Google Scholar
Schellhorn, N.A., Glatz, R.V. & Wood, G.M. (2010) The risk of exotic and native plants as hosts for four pests thrips (Thysanoptera: Thripinae). Bulletin of Entomological Research 100(5), 501–510.Google Scholar
Shah, M.M., Zhang, S. & Liu, T. (2015) Whitefly, host plant and parasitoid: a review on their interactions. Asian Journal of Applied Science and Engineering 4, 48–61.Google Scholar
Snyder, W.E. & Tylianakis, J.M. (2012) The ecology of biodiversity–biocontrol relationships. pp. 21–40 in Gurr, G.M., Wratten, S.D., Snyder, W.E. & Read, D.M.Y. (Eds) Biodiversity and Insect Pests. West Sussex, UK, Wiley.Google Scholar
Stephens, C.J., Schellhorn, N.A., Wood, G.M. & Austin, A.D. (2006) Parasitic wasp assemblages associated with native and weedy plant species in an agricultural landscape. Australian Journal of Entomology 45, 176–184.Google Scholar
Straub, C.S., Finke, D.L. & Snyder, W.E. (2008) Are the conservation of natural enemy biodiversity and biological control compatible goals? Biological Control 45, 225–237.Google Scholar
Thies, C. & Tscharntke, T. (1999) Landscape structure and biological control in agro-ecosystems. Science 285(5429), 893–895.Google Scholar
Tommasini, M. G. & Maini, S. (1995) Frankliniella occidentalis and other thrips harmful to vegetable and other ornamental crops in Europe. pp. 1–42 in Loomans, A.J.M., van Lenteren, J. C., Tommasini, M. G., Maini, S. & Riudavets, J. (Eds) Biological Control of Thrips Pests. Wageringen, The Netherlands, Wageningen Agriculture University.Google Scholar
Tscharntke, T., Karp, D.S., Chaplin-Kramer, R., Batáry, P., DeClerck, F., Gratton, C., Hunt, L., Ives, A., Jonsson, M., Larsen, A., Martin, E.A., Martínez-Salinas, A., Meehan, T.D., O'Rourke, M., Poveda, K., Rosenheim, J.A., Rusch, A., Schellhorn, N., Wanger, T.C., Wratten, S. & Zhang, W. (2016) When natural habitat fails to enhance biological pest control – Five hypotheses. Biological Conservation 204, 449–458.Google Scholar
Vandermeer, J., Perfecto, I. & Philpott, S. (2010) Ecological complexity and pest control in organic coffee production: uncovering an autonomous ecosystem service. BioScience 60, 527–537.Google Scholar
Winkler, K., Wäckers, FL, Termorshuizen, A.J. & van Lenteren, J.C. (2010) Assessing risks and benefits of floral supplements in conservation biological control. BioControl 55(6), 719–727. doi: 10.1007/s10526-010-9296-8.Google Scholar
Witting, B.E., Orr, D.B. & Linker, H.L. (2007) Attraction of insect natural enemies to habitat plantings in North Carolina. Journal of Entomology Science 42, 439–456.Google Scholar
Woltz, J.M. & Landis, D.A. (2014) Coccinellid response to landscape composition and configuration. Agricultural and Forest Entomology 16(4), 341–349.Google Scholar