Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-22T19:15:38.223Z Has data issue: false hasContentIssue false
  • English
  • Français

Disturbance and competition drive diversity effects in cabbage–aphid–onion systems with intra-specific genetic variation

Published online by Cambridge University Press:  13 June 2019

C.S.E. Guilbaud Open the ORCID record for C.S.E. Guilbaud [Opens in a new window]  and
M.S. Khudr
C.S.E. Guilbaud*
Affiliation:
Institut für Biologie, Freie Universität Berlin, Königin-Luise-Straße 1-3, 14195 Berlin, Germany
M.S. Khudr
Affiliation:
Faculty of Biology, Medicine and Health, The University of Manchester, Michael Smith Building, M13 9PT, Manchester, UK
*
*Author for correspondence Phone: 07.66.11.54.81 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Decreased reliance on pesticides can be achieved through a clever use of eco-evolutionary knowledge via intercropping economically valuable crops with companion plants that can hamper pest outbreaks. We created a greenhouse multi-layered microcosm system to test two potato peach aphid clones, performing alone or in competition, on mixes of genetically variable cultivars of cabbage, with and without onion. The onion acted as a nuisance/disturbance for the pest, which was generally for the benefit of the cabbage albeit both plants sharing space and nutrients. The onion effect was context-specific and differed by aphid genotype. Onion variable nuisance negatively affected the numbers of one aphid genotype (green) across all contexts, while the other genotype (pink) numbers were decreased in two contexts only. However, the green performed better than the pink on all cases of cabbage di-mixes despite its numbers being capped when the onion was present. Further, there was also a general aphid propensity to wander off the plant along with a differential production of winged morphs to escape the onion-affected environments. Moreover, through a comparative increase in dry mass, which was subject to onion and aphid effects, a diversity effect was found where the cabbages of fully genetically variable microcosms sustained similar final dry mass compared with non-infested microcosms. Our findings provide fresh insights into the use of multi-layered contextual designs that not only allow disentangling the relative effects of genetic variation and modes of interaction, but also help integrate their benefits into pest management in view of companion planting.

Keywords

genetic variabilitycompetitionintercroppingdisturbance
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 1 , February 2020 , pp. 123 - 135
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

Both authors contributed equally to this work.

References

Aktar, W., Sengupta, D. & Chowdhury, A. (2009). Impact of pesticides use in agriculture: their benefits and hazards. Interdisciplinary Toxicology 2, 1–12.10.2478/v10102-009-0001-7Google Scholar
Altieri, M. (2012). Insect pest management in the agroecosystems of the future. Atti Accademia Nazionale Italiana di Entomologia 60, 137–144.Google Scholar
Altieri, M. & Nicholls, C. (2004). Biodiversity and Pest Management in Agroecosystems. 2nd edn. Binghamton, NY, Haworth Press Inc.10.1201/9781482277937Google Scholar
Baidoo, P., Mochiah, M. & Apusiga, K. (2012). Onion as a pest control intercrop in organic cabbage (Brassica oleracea) production system in Ghana. Sustainable Agriculture Research 1, 36–41.10.5539/sar.v1n1p36Google Scholar
Baluška, F. & Ninkovic, V. (2010). Plant Communication From an Ecological Perspective. Berlin, Springer.Google Scholar
Barbera, G. & Cullotta, S. (2016). The traditional Mediterranean polycultural landscape as cultural heritage: its origin and historical importance, its agro-silvo-pastoral complexity and the necessity for its identification and inventory. pp. 21–48 in Agnoletti, M. & Emanueli, F. (Eds) Biocultural Diversity in Europe. Environmental History 5. Cham, Springer. doi: 10.1007/978-3-319-26315-1_2.Google Scholar
Barbosa, P. & Letourneau, D. (1988). Novel Aspects of Insect-Plant Interactions. New York, John Wiley & Sons.Google Scholar
Bates, D., Mächler, M., Bolker, B. & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.10.18637/jss.v067.i01Google Scholar
Bellostas, N., Sørensen, A.D., Sørensen, J.C. & Sørensen, H. (2007). Genetic variation and metabolism of glucosinolates. Advances in Botanical Research Rapeseed Breeding 45, 369–415. doi: 10.1016/s0065-2296(07)45013-3.Google Scholar
Ben-Ari, M. & Inbar, M. (2014). Aphids link different sensory modalities to accurately interpret ambiguous cues. Behavioral Ecology 25, 627–632.10.1093/beheco/aru033Google Scholar
Blackman, R. & Eastop, V. (2000). Aphids on the World's Crops. An Identification and Information Guide. 2nd edn. Chichester, John Wiley & Sons.Google Scholar
Brooker, R., Maestre, F., Callaway, R., Lortie, C., Cavieres, L.A., Kunstler, G., Liancourt, P., Tielborger, K., Travis, J.M.J., Anthelme, F., Armas, C., Coll, L., Corcket, E., DelzOn, S., Forey, E., Kikvidze, Z., Olofsson, J., Pugnaire, F., Quiroz, Q.L., Saccone, P., Schiffers, K., Seifan, M., Touzard, B. & Michalet, R. (2008). Facilitation in plant communities: the past, the present, and the future. Journal of Ecology 96, 18–34.Google Scholar
CABI Plantwise Technical Factsheet (2019). Cabbage (Brassica oleracea var. capitata). Available online at https://www.plantwise.org/KnowledgeBank/Datasheet.aspx?dsid=10109.Google Scholar
Cao, H., Zhang, Z., Wang, X. & Liu, T. (2018). Nutrition versus defense: why Myzus persicae (green peach aphid) prefers and performs better on young leaves of cabbage. PLoS One 13(4), e0196219.10.1371/journal.pone.0196219Google Scholar
Cartea, M.E., Francisco, M., Lema, M., Soengas, P. & Velasco, P. (2010). Resistance of Cabbage (Brassica oleracea capitata Group) Crops to Mamestra brassicae. Journal of Economic Entomology 103, 1866–1874.10.1603/EC09375Google Scholar
Castro, A., Aires, A., Rosa, E., Bloem, E., Stulen, I. & De Kok, LJ. (2004). Distribution of glucosinolates in Brassica oleracea cultivars. Phyton-Annales Rei Botanicae 44, 133–143.Google Scholar
Cerda, R., Avelino, J., Gary, C., Tixier, P., Lechevallier, E. & Allinne, C. (2017). Primary and secondary yield losses caused by pests and diseases: assessment and modeling in coffee. PLoS One 12, 1–17.10.1371/journal.pone.0169133Google Scholar
Culliney, T. (2014). Crop losses to arthropods. pp. 201–225 in Pimentel, D. & Peshin, R. (Eds) Integrated Pest Management: Pesticide Problems. Dordrecht, Springer.10.1007/978-94-007-7796-5_8Google Scholar
Dahlin, I., Radonjic, A. & Ninkovic, V. (2015). Changed host plant volatile emissions induced by chemical interaction between unattacked plants reduce aphid plant acceptance with intermorph variation. Journal of Pest Science 88(2), 249–257.Google Scholar
Dancewicz, K. & Gabryś, B. (2008). Effect of extracts of garlic (Allium sativum L.), wormwood (Artemisia absinthium L.) and tansy (Tanacetum vulgare L.) on the behaviour of the peach potato aphid Myzus persicae (Sulz.) during the settling on plants. Pesticides 3–4, 93–99.Google Scholar
Delong, J., Forbes, V. & Galic, N., Gibert, J., Laport, R., Phillips, J. & Vavra, J. (2016). How fast is fast? Eco-evolutionary dynamics and rates of change in populations and phenotypes. Ecology and Evolution 6, 573–581.Google Scholar
Dixon, A.F.G. (1985). Aphid Ecology An Optimization Approach. 2nd edn. Dordrecht, Netherlands, Springer.10.1007/978-94-011-5868-8Google Scholar
Dungey, H., Potts, B., Whitham, T. & Li, H. (2000). Plant genetics affects arthropod community richness and composition: evidence from a synthetic eucalypt hybrid population. Evolution 54, 1938–1946.10.1111/j.0014-3820.2000.tb01238.xGoogle Scholar
Fang, Z., Liu, Y., Lou, P. & Liu, G. (2005). Current trends in cabbage breeding. Journal of New Seeds 6, 75–107.10.1300/J153v06n02_05Google Scholar
Fox, J. & Weisberg, S. (2011). An R Companion to Applied Regression. 2nd edn. Los Angeles, Sage.Google Scholar
Fussmann, G., Loreau, M. & Abrams, P. (2007). Eco-evolutionary dynamics of communities and ecosystems. Functional Ecology 21, 465–477.10.1111/j.1365-2435.2007.01275.xGoogle Scholar
Gebru, H. (2015). A review on the comparative advantages of intercropping to mono-cropping system. Journal of Biology, Agriculture and Healthcare 5, 9. Available online at https://www.iiste.org/Journals/index.php/JBAH/article/viewFile/22307/23138.Google Scholar
Geem, M., Gols, R., Dam, N., der Putten, W., Fortuna, T. & Harvey, J. (2013). The importance of aboveground–belowground interactions on the evolution and maintenance of variation in plant defense traits. Frontiers in Plant Science 4, 431. doi: 10.3389/fpls.2013.00431.Google Scholar
Gersani, M., Brown, J., O'Brien, E., Maina, G. & Abramsky, Z. (2001) Tragedy of the commons as a result of root competition. Journal of Ecology, 89, 660–669.10.1046/j.0022-0477.2001.00609.xGoogle Scholar
Gough, L. & Grace, J. (1998). Herbivore effects on plant species density at varying productivity levels. Ecology 79, 1586–1594.Google Scholar
Green, J.P., Foster, R., Wilkins, L., Osorio, D. & Hartley, S.E. (2015). Leaf colour as a signal of chemical defence to insect herbivores in wild cabbage (Brassica oleracea). PLoS One 10(9), e0136884.10.1371/journal.pone.0136884Google Scholar
Guilbaud, C.S.E., Dalchau, N., Purves, D. & Turnbull, L. (2015). Is ‘peak N’ key to understanding the timing of flowering in annual plants? New Phytologist, 205, 918–927.10.1111/nph.13095Google Scholar
Haan, J. & Vasseur, L. (2014). Above and below ground interactions in monoculture and intercropping of onion and lettuce in greenhouse conditions. American Journal of Plant Sciences 5, 3319–3327.10.4236/ajps.2014.521347Google Scholar
Hauggaard-Nielsen, H. (2001). Competitive interactions, resource use and nitrogen dynamics in annual intercrops in low-input cropping systems. Ph.D. Thesis, The Royal Veterinary and Agricultural University, Copenhagen, Denmark. Available online at https://www.researchgate.net/publication/228852161_Competitive_interactions_resource_use_and_nitrogen_dynamics_in_annual_intercrops_in_low-input_cropping_systems.Google Scholar
Hersch-Green, E., Turley, N. & Johnson, M. (2011). Community genetics: what have we accomplished and where should we be going? Philosophical Transactions of the Royal Society B 366, 1453–1460.10.1098/rstb.2010.0331Google Scholar
Hooks, C., Fereres, A. & Wang, K. (2007). Using Protector Plants to Guard Crops From Aphid-Borne non-Persistent Viruses. Honolulu, HI, University of Hawaii. 7 p. (Soil and Crop Management; SCM-18). Available online at http://hdl.handle.net/10125/12470.Google Scholar
Hooper, D., Iii, F., Ewel, J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J., Lodge, D., Loreau, M., Naeem, S., Schmid, B., Setälä, H., Symstad, A., Vandermeer, J. & Wardle, D. (2005). Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75, 3–35.10.1890/04-0922Google Scholar
Hori, M. & Harada, H. (1995). Screening plants resistant to green peach aphid, Myzus persicae (Sulzer). Applied Entomology and Zoology 30, 246–249. Available online at https://ci.nii.ac.jp/els/contents110001105553.pdf?id=ART0001268935.Google Scholar
Hothorn, T., Bretz, F. & Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal 50, 346–363.Google Scholar
Kanvil, S., Powell, G. & Turnbull, C. (2014). Pea aphid biotype performance on diverse Medicago host genotypes indicates highly specific virulence and resistance functions. Bulletin of Entomological Research 104, 689–701.Google Scholar
Karban, R., Agramal, A. & Mangel, M. (1997). The benefits of induced defense against herbivores. Ecology 78, 1351–1355.Google Scholar
Khudr, MS., Potter, T., Rowntree, J. & Preziosi, R. (2014). Community genetic and competition effects in a model pea aphid system. Advances in Ecological Research 50, 243–265.Google Scholar
Khudr, MS., Buzhdygan, O., Petermann, J. & Wurst, S. (2017 a). Fear of predation alters clone-specific performance in phloem-feeding prey. Scientific Reports 7, 1–10.Google Scholar
Khudr, MS., Guilbaud, C.S.E. & Preziosi, R. (2017 b). Host plant and competitor identity matter in genotype × genotype × environment interactions between vetch and pea aphids. Ecological Entomology 42, 565–576.Google Scholar
Knörzer, H., Graeff-Hönninger, S., Guo, B., Wang, P. & Claupein, W. (2009). The rediscovery of intercropping in China: a traditional cropping system for future Chinese agriculture – a review. pp. 13–44 in Lichtfouse, E. (ed.) Climate Change, Intercropping, Pest Control and Beneficial Organisms, Sustainable Agriculture Reviews 2. Amsterdam, The Netherlands, Springer Science+Business Media B.V.Google Scholar
Kotowska, A., Cahill, J. Jr. & Keddie, B. (2010). Plant genetic diversity yields increased plant productivity and herbivore performance. Journal of Ecology 98, 237–245.Google Scholar
Li, L., Sun, J., Zhang, F., Li, X., Yang, S. & Rengel, K. (2001). Wheat/maize or wheat/soybean strip intercropping I. Yield advantage and interspecific interactions on nutrients. Field Crops Research 71, 123–137.Google Scholar
Lithourgidis, A., Dordas, C., Damalas, C. & Vlachostergios, D. (2011). Annual intercrops: an alternative pathway for sustainable agriculture. Australian Journal of Crop Science 5, 396–410. Available online at https://www.cropj.com/anastasios_5_4_2011_396_410.pdf.Google Scholar
Loreau, M. (1998). Biodiversity and ecosystem functioning: a mechanistic model. Proceedings of the National Academy of Sciences of the United States of America 95, 5632–5636.Google Scholar
Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J., Hector, A., Hooper, D., Huston, M., Raffaelli, D., Schmid, B., Tilman, D. & Wardle, D. (2001). Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804–808.Google Scholar
Machado, S. (2009). Does intercropping have a role in modern agriculture? Journal of Soil and Water Conservation 64, 55A–57A.Google Scholar
Mello, M. & Silva-Filho, M. (2002). Plant–insect interactions: an evolutionary arms race between two distinct defense mechanisms. Brazilian Journal of Plant Physiology 14, 71–81.Google Scholar
Moya-Laraño, J., Bilbao-Castro, J., Barrionuevo, G., Ruiz-Lupión, D., Casado, L., Montserrat, M., Melián, C. & Magalhães, S. (2014). Eco-evolutionary spatial dynamics: rapid evolution and isolation explain food web persistence. Advances in Ecological Research 50, 75–143.Google Scholar
Mushagalusa, G., Ledent, J. & Draye, X. (2008). Shoot and root competition in potato/maize intercropping: effects on growth and yield. Environmental and Experimental Botany 64, 180–188.Google Scholar
Ninkovic, V., Dahlin, I., Vucetic, A., Petrovic-Obradovic, O., Glinwood, R. & Webster, B. (2013). Volatile exchange between undamaged plants – a new mechanism affecting insect orientation in intercropping. PLoS One 8(7), e69431.Google Scholar
Otway, S., Hector, A. & Lawton, J. (2005). Resource dilution effects on specialist insect herbivores in a grassland biodiversity experiment. Journal of Animal Ecology 74, 234–240.Google Scholar
Pahla, I., Tumbare, T., Chitamba, J. & Kapenzi, A. (2014). Evaluation of Allium sativum and Allium cepa intercrops on the control of Brevicoryne brassicae (Homoptera: Aphididae) in Brassica napus. International Journal of Farming and Allied Sciences 3, 1069–1074.Google Scholar
Parker, J., Snyder, W., Hamilton, G. & Saona, C. (2013). Companion planting and insect pest control. pp. 1–29. in Soloneski, S. & Larramendy, M. (Eds) Weed and Pest Control – Conventional and New Challenges. London, IntechOpen limited. doi: 10.5772/55044. Available online at https://www.intechopen.com/books/weed-and-pest-control-conventional-and-new-challenges/companion-planting-and-insect-pest-control.Google Scholar
Patel, S., Awasthi, A. & Tomar, R. (2004). Asessment of yield losses in mustard (Brassica juncea L.) due to mustard aphid (Lipaphis erysimi Kalt.) under different thermal environments in Eastern Central India. Applied Ecology and Environmental Research 2, 1–15.Google Scholar
Petersen, M. & Sandström, J. (2001). Outcome of indirect competition between two aphid species mediated by responses in their common host plant. Functional Ecology 15, 525–534.Google Scholar
Powell, G., Tosh, C. & Hardie, J. (2006). Host plant selection by aphids: behavioral, evolutionary, and applied perspectives. Annual Review of Entomology 51, 309–330.Google Scholar
R Core Team (2017). 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
Razaq, M., Mehmood, A., Aslam, M., Ismail, M., Afzal, M. & Shad, S. (2011). Losses in yield and yield components caused by aphids to late sown Brassica napus L., Brassica juncea L. and Brassica carinata A. Braun at Multan, Punjab (Pakistan). Pakistan Journal of Botany 43, 319–324.Google Scholar
Sallam, M. (2013). Insect Damage: Damage on Post-harvest Compendium. AGSI/FAO: INPhO. Available online at http://www.fao.org/3/a-av013e.pdf.Google Scholar
Schuett, W., Dall, S., Baeumer, J., Kloesener, M., Nakagawa, S., Beinlich, F. & Eggers, T. (2011). Personality variation in a clonal insect: the pea aphid, Acyrthosiphon pisum. Developmental Psychobiology 53, 631–640.Google Scholar
Smith, H. & McSorely, R. (2000). Intercropping and pest management: a review of major concepts. American Entomologist 46, 156–161.Google Scholar
Smith, R., Mooney, K. & Agrawal, A. (2008). Coexistence of three specialist aphids on common milkweed, Asclepias syriaca. Ecology 89, 2187–2196.Google Scholar
Stenberg, J. (2017). A conceptual framework for integrated pest management. Trends in Plant Science 22, 759–769.Google Scholar
Sulvai, F., Chaúque, B. & Macuvele, D. (2016). Intercropping of lettuce and onion controls caterpillar thread, Agrotis ipsilon major insect pest of lettuce. Chemical and Biological Technologies in Agriculture 3, 28.Google Scholar
Suszkiw, J. (2011). Seeking saponins and other compounds to fortify crops. USDA AgResearch Magazine 59, 8–10. Available online at https://agresearchmag.ars.usda.gov/AR/archive/2011/Aug/August2011.pdf.Google Scholar
Thornley, J. (1972). A balanced quantitative model for root:shoot ratios in vegetative plants. Annals of Botany, 36, 431–441.Google Scholar
Tooker, J. & Frank, S. (2012). Genotypically diverse cultivar mixtures for insect pest management and increased crop yields. Journal of Applied Ecology 49, 974–985.Google Scholar
Tremmel, M. & Müller, C. (2013). Insect personality depends on environmental conditions. Behavioral Ecology 24, 386–392.Google Scholar
Underwood, N. (2009). Effect of genetic variance in plant quality on the population dynamics of a herbivorous insect. Journal of Animal Ecology 78, 839–847.Google Scholar
Utsumi, S., Ando, Y., Craig, T. & Ohgushi, T. (2011). Plant genotypic diversity increases population size of a herbivorous insect. Proceedings of the Royal Society of London B 278, 3108–3015.Google Scholar
Van Emden, H. & Harrington, R. (2007). Aphids as Crop Pests. Wallingford, UK, CABI.Google Scholar
Verkerk, R., Tebbenhoff, S. & Dekker, M. (2010). Variation and distribution of glucosinolates in 42 cultivars of Brassica oleracea vegetable crops. Acta Horticulturae 856, 63–70.Google Scholar
Vickers, L. (2012). Aphid responses to drought: a combined physiological and transcriptomic approach. Ph.D. Thesis, University of Birmingham. Available online at https://etheses.bham.ac.uk/id/eprint/3453/.Google Scholar
Vucetic, A., Dahlin, I., Petrovic-Obradovic, O., Glinwood, R., Webster, B. & Ninkovic, V. (2014). Volatile interaction between undamaged plants affects tritrophic interactions through changed plant volatile emission. Plant Signaling & Behavior 9, e29517.Google Scholar
Wang, S., Bao, X., Sun, Y., Chen, R. & Zhai, B. (1996). Effects of soybean aphid, Aphis glycines on soybean growth and yield. Soybean Science (China) 15, 243–247. Available online at http://www.refworks.com/refshare/?site=015251129867200000/RWWEB101202057/Soybean%20Aphid%20Literature%20for%20Translation&rn=17.Google Scholar
Whitham, T., Young, W., Martinsen, G., Gehring, C., Schweitzer, J., Shuster, S., Wimp, G., Fischer, D., Bailey, J., Lindroth, R., Woolbright, S. & Kuske, C. (2003). Community and ecosystem genetics: a consequence of the extended phenotype. Ecology 84, 559–573.Google Scholar
Wiczkowski, W., Szawara-Nowak, D. & Topolska, J. (2013). Red cabbage anthocyanins: profile, isolation, identification, and antioxidant activity. Food Research International 51, 303–309.Google Scholar
Wilson, C. & Tisdell, C. (2001). Why farmers continue to use pesticides despite environmental, health and sustainability costs. Ecological Economics 39, 449–462.Google Scholar
Windle, P. & Franz, E. (1979). The effects of insect parasitism on plant competition: greenbugs and barley. Ecology 60, 521–529.Google Scholar
Wu, X., Wu, F., Zhou, X., Fu, X., Tao, Y., Xu, W., Pan, K. & Liu, S. (2016). Effects of intercropping with potato onion on the growth of tomato and rhizosphere alkaline phosphatase genes diversity. Frontiers in Plant Science 7, 846.Google Scholar
Zhang, F. & Li, L. (2003). Using competitive and facilitative interactions in intercropping systems enhances crop productivity and nutrient-use efficiency. Plant and Soil 248, 305–312.Google Scholar
Zhang, W., Jia, X., Damgaard, C., Morris, E., Bai, Y., Pan, S. & Wang, G. (2012). The interplay between above- and below-ground plant–plant interactions along an environmental gradient: insights from two-layer zone-of-influence models. Oikos 122, 1147–1156.Google Scholar
Zhou, H., Chen, J., Liu, Y., Francis, F., Haubruge, E., Bragard, C., Sun, J. & Cheng, D. (2013). Influence of garlic intercropping or active emitted volatiles in releasers on aphid and related beneficial in wheat fields in China. Journal of Integrative Agriculture 12, 467–473.Google Scholar
Supplementary material: File

Guilbaud and Khudr supplementary material

Guilbaud and Khudr supplementary material 1

Download Guilbaud and Khudr supplementary material(File)
File 2.4 MB