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Brassica aphid (Hemiptera: Aphididae) populations are conditioned by climatic variables and parasitism level: a study case of Triângulo Mineiro, Brazil

Published online by Cambridge University Press:  20 March 2017

M.V. Sampaio
Affiliation:
Federal University of Uberlândia, Agronomic Institute, Uberlândia – Minas Gerais, Brazil
A.P. Korndörfer
Affiliation:
Federal University of Uberlândia, Agronomic Institute, Uberlândia – Minas Gerais, Brazil
J. Pujade-Villar
Affiliation:
Department of Animal Biology, Faculty of Biology, University of Barcelona, Spain
J.E.A. Hubaide
Affiliation:
Federal University of Uberlândia, Agronomic Institute, Uberlândia – Minas Gerais, Brazil
S.E. Ferreira
Affiliation:
Federal University of Uberlândia, Agronomic Institute, Uberlândia – Minas Gerais, Brazil
S.O. Arantes
Affiliation:
Federal University of Uberlândia, Agronomic Institute, Uberlândia – Minas Gerais, Brazil
D.M. Bortoletto
Affiliation:
Federal University of Uberlândia, Agronomic Institute, Uberlândia – Minas Gerais, Brazil
C.M. Guimarães
Affiliation:
Federal University of Uberlândia, Agronomic Institute, Uberlândia – Minas Gerais, Brazil
J.A. Sánchez-Espigares
Affiliation:
Department of Statistics and Operations Research, Technical University of Catalonia, Barcelona, Spain
B. Caballero-López*
Affiliation:
Natural Sciences Museum of Barcelona, Laboratory of Nature, Arthropods Department, MCNB, Barcelona, Spain Agroecosystems Research group Department of Plant Biology, Faculty of Biology, University of Barcelona, Barcelona, Spain
*
*Author for correspondence Phone: (+34) 93 256 22 11 E-mail: bcaballerolo@bcn.cat

Abstract

Cosmopolitan pests such as Brevicoryne brassicae, Lipaphis pseudobrassicae, and Myzus persicae (Aphididae) cause significant damage to Brassicaceae crops. Assessment of the important biotic and abiotic factors that regulate these pests is an essential step in the development of effective Integrated Pest Management programs for these aphids. This study evaluated the influence of leaf position, precipitation, temperature, and parasitism on populations of L. pseudobrassicae, M. persicae, and B. brassicae in collard greens fields in the Triângulo Mineiro region (Minas Gerais state), Brazil. Similar numbers of B. brassicae were found on all parts of the collard green plants, whereas M. persicae and L. pseudobrassicae were found in greatest numbers on the middle and lower parts of the plant. While temperature and precipitation were positively related to aphid population size, their effects were not accumulative, as indicated by a negative interaction term. Although Diaeretiella rapae was the main parasitoid of these aphids, hyperparasitism was dominant; the main hyperparasitoid species recovered from plant samples was Alloxysta fuscicornis. Parasitoids seem to have similar distributions on plants as their hosts. These results may help predict aphid outbreaks and gives clues for specific intra-plant locations when searching for and monitoring aphid populations.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

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References

Akhtar, M.S., Dey, D., Usmani, M.K. & Choudhury, R.A. (2010) Seasonal abundance of Diaeretiella rapae (M'Intosh) (Braconidae: Aphidiinae) parasitizing Lipaphis erysimi (Kaltenbach) (Hemiptera: Aphididae) in Brassica juncea variety Pusa bold. Munis Entomology and Zoology 5, 692696.Google Scholar
Assunção, J. & Chiavari, J. (2015) Towards efficient land use in Brazil. The New Climate Economy. Available online at http://2015.newclimateeconomy.report/wp-content/uploads/2015/09/Towards-Efficient-Land-Use-Brazil.pdf (accessed 20 October 2015).Google Scholar
Auad, A.M., Bueno, V.H.P., Kato, C.M. & Gamarra, D.C. (1997). Ocorrência e Flutuação Populacional de Predadores e Parasitóides de Brachycaudus (Appelia) schwartzi (Börner) (Homoptera: Aphididae), em Pessegueiro, em Jacuí-MG. Anais da Sociedade Entomológica do Brasil 26(2) 257263.Google Scholar
Ayal, Y. (1987) The foraging strategy of Diaeretiella rapae . Journal of Animal Ecology 56, 10571068.Google Scholar
Bates, D., Maechler, M. & Dai, B. (2008) Lme4: linear mixed-effects models using S4 classes. R package version 0.999375–28 (CD.ROM).Google Scholar
Blackman, R.L. & Eastop, V.P. (2000) Aphids on the World's Crops: an Identification and Information Guide, 2nd edn. New York, J. Wiley & Sons.Google Scholar
Brown, P.D., Tokuhisa, J.G., Reichelt, M. & Gershenzon, J. (2003) Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana . Phytochemistry 62, 471481.Google Scholar
Bridges, M., Jones, A.M.E., Bones, A.M., Hodgson, C., Cole, R., Bartlet, E., Wallsgrove, R., Karapapa, V.K., Watts, N. & Rossiter, J. (2002) Spatial organization of the glucosinolate-myrosinase system in brassicae specialist aphids is similar to that of the host plant. Proceedings of the Royal Society of London B 269, 187191.Google Scholar
Caballero-López, B., Blanco-Moreno, J.M., Pérez, N., Michelena, J.M., Pujade-Villar, J., Guerreri, E., Sánchez-Espigares, J.A. & Sans, F.X. (2012) Weeds and aphid-parasitoid communities benefit differently from organic and conventional cropping of spring cereals. Journal of Pest Science 85(1), 8188.Google Scholar
Cividanes, F.J. (2002) Impacto de inimigos naturais e de fatores meteorológicos sobre uma população de Brevicoryne brassicae (L.) (Hemiptera: Aphididae) em couve. Neotropical Entomology 31, 249255.Google Scholar
Cividanes, F.J. (2003) Exigências térmicas de Brevicoryne brassicae e previsão de pios populacionais. Pesquisa Agropecuaria Brasileira 38, 561566.Google Scholar
Cividanes, F.J. & Souza, V.P. (2004) Distribuição vertical de pulgões (Hemiptera: Aphididae) em couve. Arquivos do Instituto Biológico 71, 254256.Google Scholar
CONAB (2015) (Companhia Nacional de Abastecimento). Séries Históricas. Open source. Available online at http://www.conab.gov.br/conteudos.php?a=1252&. (accessed 20 October 2015).Google Scholar
Collier, R.H., Finch, S. (2007) IPM case studies: brassicas. pp. 549559 in van Emden, H., Harrington, R. (Eds) Aphids as Crop Pests. Wallingford, UK, CABI.Google Scholar
Dent, D. (1995) Insect Pest Management. London, Chapman & Hall.Google Scholar
Desneux, N. & Ramirez-Romero, R. (2009) Plant characteristics mediated by growing conditions can impact parasitoid's ability to attack host aphids in winter canola. Journal of Pest Science 82, 335342.Google Scholar
Dixon, A.F.G. (1977) Aphid ecology: life cycles, polymorphism, and population regulation. Annual Review of Ecology, Evolution and Systematics 8, 329353.Google Scholar
Filgueira, F.A.R. (2003) Novo manual de olericultura: agrotecnologia moderna na produção e comercialização de hortaliças, 2nd edn. Viçosa, UFV.Google Scholar
Godoy, K.B. & Cividanes, F.J. (2002) Tabelas de esperança de vida e fertilidade para Lipaphis erysimi (Kalt.) (Hemiptera: Aphididae) em condições de laboratório e campo. Neotropical Entomology 31, 4148.Google Scholar
Gu, H., Fitt, G.P., & Baker, G.H. (2007) Invertebrate pests of canola and their management in Australia: a review. Australian Journal of Entomology 46, 231243.Google Scholar
Haddad, N.M., Tilman, D., Haarstad, J., Ritchie, M. & Knopa, M.H. (2001) Contrasting effects of plant richness and composition on insect communities: a field experiment. The American Naturalist 158, 1735.Google Scholar
Höller, C., Borgemeister, C., Haardt, H. & Powell, W. (1993) The relationship between primary parasitoids and hyperparasitoids of cereal aphids: an analysis of field data. Journal of Animal Ecology 62, 1221.Google Scholar
Hughes, R.D. (1962) A method for estimating the effects of mortality on aphid populations. Journal of Animal Ecology 31, 389396.Google Scholar
IBGE (Instituto Brasileiro de Geografia e Estatística) (2010) Open source. Available online at http://www.ibge.gov.br (accessed 7 December 2011).Google Scholar
Jenkins, L., Brill, R. & McCaffery, D. (2011) Managing aphids in flowering canola in central west NSW. p. 82 in Proceedings of Seventeenth Australian Research Assembly on Brassicas (ARAB) organized by the Australian Oilseeds Federation, 15–17 August 2011, Wagga Wagga, New South Wales, Australia.Google Scholar
Jeon, H.Y., Kim, H.H., Lee, Y.H., Chang, Y.D. & Yiem, M.S. (2005) Biological control of the turnip aphid (Lipaphis erysimi K.) using the braconid wasp (Diaeretiella rapae M.). Korean Journal of Horticultural Science and Technology 23, 337341.Google Scholar
Kanegae, A.P. & Lomônaco, C. (2003) Plasticidade morfológica, reprodutiva e assimetria flutuante de Myzus persicae (Sulzer) (Hemiptera: Aphididae) sob diferentes temperaturas. Neotropical Entomology 32, 3743.Google Scholar
Karley, A.J., Parker, W.E. & Pitchford, J.W. (2004) The mid-season crash in aphid populations: why and how does it occur? Ecological Entomology 29, 383388.Google Scholar
Kuznetsova, A., Brockhoff, P.B. & Christensen, R.H.B. (2013). lmerTest: Tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package). R-Version:1.1–0. Available online at http://cran.rproject.org/web/packages/lmerTest/index.html Google Scholar
Leclair, M., Pons, I., Mahéo, F., Morlière, S., Simon, J.C. & Outreman, Y. (2016) Diversity in symbiont consortia in the pea aphid complex is associated with large phenotypic variation in the insect host. Evolutionary Ecology 30, 925941.Google Scholar
Liu, S.S. & Meng, X.D. (1999) Modeling development time of Myzus persicae (Hemiptera: Aphididae) at constant and natural temperatures. Bulletin of Entomological Research 89, 5363.Google Scholar
Liu, S.S. & Meng, X.D. (2000) Modeling development time of Lipaphis erysimi (Hemiptera: Aphididae) at constant and variable temperatures. Bulletin of Entomological Research 90, 337347.Google Scholar
MacGibbon, D.B. & Beuzenberg, E.J. (1978) Location of glucosinolase in Brevicoryne brassicae and Lipaphis erysimi (Aphididae). New Zealand Journal of Science 21, 389392.Google Scholar
Mackauer, M. & Völkl, W. (1993) Regulation of aphid populations by aphidian wasps: does parasitoid foraging behaviour or hyperparasitism limit impact? Oecologia 94, 339350.Google Scholar
Malavolta, E. & Kliemann, H.J. (1985) Desordens nutricionais nos cerrados. 136p, Piracicaba, POTAFOS.Google Scholar
Martinez, A.J., Ritter, S.G., Doremus, M.R., Russell, J.A. & Oliver, K.M. (2014) Aphid-encoded variability in susceptibility to a parasitoid. BMC Evolutionary Biology 14, 127.Google Scholar
Maunder, M.N. & Punt, A.E. (2004) Standardizing catch and effort data: a review of recent approaches. Fisheries Research 70, 141159.Google Scholar
Mayer, D., Roy, D., Robins, J., Halliday, I. & Sellinet, M. (2005) Modelling zero-inflated fish counts in estuaries: a comparison of alternative statistical distributions. pp. 25812587 in Zerger, A., Argent, R.M. (Eds) International Congress on Modelling and Simulation, Anaheim, Nano Science and Technology Institute.Google Scholar
McCullagh, P. & Nelder, J.A. (1989) Generalized Linear Models. London, Chapman & Hall.Google Scholar
Micic, S. (2005) Identification and Cultural Control of Insect and Applied Pests of Canola. Bulletion 4650. South Perth, Western Australia, Australia, Department of Agriculture.Google Scholar
Oliveira, R.S., Sampaio, M.V., Ferreira, S.E., Ribeiro, L.C.M. & Tannús-Neto, J. (2013) Low parasitism by Diaeretiella rapae (Hym.: Braconidae) of Lipaphis pseudobrassicae (Hemip.: Aphididae): pre- or post-ovipositional host resistance? Biocontrol Science and Technology 23, 7991.Google Scholar
O'Neill, M.F. & Faddy, M.J. (2003) Use of binary and truncated negative binomial modeling in the analysis of recreational catch data. Fisheries Research 60, 471477.Google Scholar
Pike, K.S., Starý, P., Miller, T., Allison, D., Boydston, L., Graf, G. & Gillespie, R. (1997). Small-grain aphid parasitoids (Hymenoptera: Aphelinidae and Aphidiidae) of Washington: distribution, relative abundance, seasonal occurrence, and key to known North American species. Environmental Entomology 16, 12991311.Google Scholar
Pike, K.S., Starý, P., Miller, T., Allison, D., Graf, G., Boydston, L., Miller, R. & Gillespie, R. (1999) Host range and habitats of the aphid parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae) in Washington state. Environmental Entomology 28, 6171.Google Scholar
Pinto, R.M., Bueno, V.H.P. & Santa-Cecília, L.V.C. (2000) Flutuação populacional de afídeos (Hemiptera: Aphididae) associados à cultura da batata Solanum tuberosum L., no plantio de inverno em Alfenas, Sul de Minas Gerais. Anais da Sociedade Entomologica do Brasil 29, 649657.Google Scholar
Pope, R.D. (1983) Some aphid waxes, their form and function (Homoptera: Aphididae). Journal of Natural History 17, 489506.Google Scholar
Potts, J.M. & Elith, J. (2006) Comparing species abundance models. Ecological Modelling 199, 153163.Google Scholar
Powell, W. (1982) The identification of hymenopterous parasitoids attacking cereal aphids in Britain. Systematic Entomology 7, 465473.Google Scholar
Price, P.W., Denno, R.F., Eubanks, M.D., Finke, D.L. & Kaplan, I. (2011) Insect Ecology: Behavior, Population and Communities. Cambridge, UK, Cambridge University Press.Google Scholar
R Development Core Team, R. (2013) A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. In: R Development Core Team. Vienna, Austria. Open source. Available online at http://www.R-project.org Google Scholar
Reifenrath, K. & Müller, C. (2007) Species-specific and leaf-age dependent effects of ultraviolet radiation on two Brassicaceae. Phytochemistry 68, 875885.Google Scholar
Rothacher, L., Ferrer-Suay, M. & Vorburger, C. (2016) Bacterial endosymbionts protect aphids in the field and alterparasitoidcommunity composition. Ecology 97, 17121723.Google Scholar
Satar, S., Kersting, U. & Ulusoy, M. (2005) Temperature dependent life history traits of Brevicoryne brassicae (L.) (Hom., Aphididae) on white cabbage. Turkish Journal of Agriculture and Forestry 29, 341346.Google Scholar
Shaltiel, L. & Ayal, Y. (1998) The use of kairomones for foraging decisions by an aphid parasitoid in small host aggregations. Ecological Entomology 23, 319329.Google Scholar
Sheehan, W. & Shelton, A.M. (1989) Parasitoid response to concentration of herbivore food plants: finding and leaving plants. Ecology 70, 993998.Google Scholar
Starý, P., Sampaio, M.V., Bueno, V.H.P. (2007) Aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae) and their associations related to biological control in Brazil. Revista Brasileira de Entomologia 51, 107118.Google Scholar
Sullivan, D.J. & Völkl, W. (1999) Hyperparasitism: multitrophic ecology and behavior. Annual Review of Entomology 44, 291315.Google Scholar
Waterhouse, D.F. & Sands, D.P.A. (2001) Classical Biological Control of Arthropods in Australia. Canberra, Australia, Csiro Entomology, Australian Centre for International Agricultural Research.Google Scholar
Weber, G., Oswald, S. & Zollner, U. (1986) Suitability of rape cultivars with different glucosinolate content for Brevicoryne brassicae (L.) and Myzus persicae (Sulzer) (Hemiptera: Aphididae). Journal of Plant Diseases and Protection 93, 113124.Google Scholar
Zamani, A.A., Talebi, A.A., Fathipour, Y. & Baniameri, V. (2006) Temperature-dependent functional response of two aphid parasitoids, Aphidius colemani and Aphidius matricariae (Hymenoptera: Aphidiidae), on the cotton aphid. Journal of Pest Science 79, 183188.Google Scholar