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Negative interaction between twospotted spider mites and aphids mediated by feeding damage and honeydew

Published online by Cambridge University Press:  09 October 2012

C.V. Cédola
Affiliation:
Centro de Estudios Parasitológicos y de Vectores (CCT La Plata, CONICET-UNLP) Calle 2 N° 584 CP 1900 La Plata, Argentina Facultad de Ciencias Naturales y Museo, UNLP
M.F. Gugole Ottaviano
Affiliation:
Centro de Estudios Parasitológicos y de Vectores (CCT La Plata, CONICET-UNLP) Calle 2 N° 584 CP 1900 La Plata, Argentina
M.E. Brentassi
Affiliation:
Facultad de Ciencias Naturales y Museo, UNLP Comisión de Investigaciones Científicas de la Provincia de Buenos Aires. División Entomología, Paseo del Bosque s/n CP 1900 La Plata, Argentina
M.F. Cingolani
Affiliation:
Centro de Estudios Parasitológicos y de Vectores (CCT La Plata, CONICET-UNLP) Calle 2 N° 584 CP 1900 La Plata, Argentina Facultad de Ciencias Naturales y Museo, UNLP
N.M. Greco*
Affiliation:
Centro de Estudios Parasitológicos y de Vectores (CCT La Plata, CONICET-UNLP) Calle 2 N° 584 CP 1900 La Plata, Argentina Facultad de Ciencias Naturales y Museo, UNLP
*
*Author for correspondence Fax: +54 0221 4232327 E-mail: [email protected]

Abstract

Among the herbivorous arthropods that feed on strawberry, the most important are the two-spotted spider mite (TSSM), Tetranychus urticae Koch, and several species of aphids. Mites and aphids belong to different guilds that coexist in the field and feed on the undersides of strawberry leaflets. However, the occurrence of large numbers of individuals of both species on the same leaflet is rarely recorded. We hypothesize that negative interactions between TSSM and aphids explain the intraplant distribution of these herbivores. We first examined the spatial coincidence of both herbivores in the field. Under experimental conditions, we then analyzed: (i) the rate of increase of TSSM and the aphid Chaetosiphon fragaefolii (Cockerell), growing individually and together; (ii) the effect of honeydew on TSSM preference; and (iii) the effect of previous strawberry leaflet damage by TSSM on C. fragaefolii preference. The proportion of TSSM that coincided with at least one aphid decreased as the percentage of leaflets with TSSM increased. The spatial coincidence index between aphids and TSSM increased together with the percentage of TSSM-infested leaflets. TSSM showed both a lower rate of increase when they shared the same leaflet with C. fragaefolii and lower fecundity on strawberry discs with honeydew. The rate of increase of C. fragaefolii did not change on co-occupied leaves, but the aphid species moved to the other side of leaflets shared with TSSM. Negative interactions resulting in a tendency for species to avoid each other, such as demonstrated herein, can affect distribution and performance of herbivorous arthropods.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2012

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References

Andow, D. (1991) Vegetational diversity and arthropod population response. Annual Review of Entomology 36, 561586.Google Scholar
Arouni, R., Garrido, A., Carbonell, E.A., Pérez-Panadés, J., Muñoz, A., Jacas, J., Urbaneja, A. & Hermoso de Mendoza, A. (2008) Interacción entre los pulgones de los cítricos (Hemiptera, Aphididae) y el minador de las hojas de los cítricos Phyllocnistis citrella Stainton (Lepidoptera, Gracillariidae). Boletín de Sanidad Vegetal 34, 89102.Google Scholar
Bardner, R. & Fletcher, K. (1974) Insect infestations and their effects on the growth and yield of field crops, a review. Bulletin of Entomological Research 64, 141160.Google Scholar
Bezemer, T., Wagenaar, R., van Dam, N. & Wäckers, F. (2003) Interactions between above and belowground insect herbivores as mediated by the plant defense system. Oikos 101, 555562.Google Scholar
Blossey, B. & Hunt-Joshi, T.R. (2003) Belowground herbivory by insects: influence on plants and aboveground herbivores. Annual Review of Entomology 48, 521547.Google Scholar
Cammell, M.E. (1981) The black bean aphid, Aphis fabae. Biologist 28, 247258.Google Scholar
Cédola, C. & Greco, N. (2010) Presence of the aphid, Chaetosiphon fragaefolli, on strawberry in Argentina. Journal of Insect Science 10, 19.CrossRefGoogle ScholarPubMed
Daugherty, M.P. (2009) Specialized feeding modes promote coexistence of competing herbivores: insights from a metabolic pool model. Environmental Entomology 38, 667676.Google Scholar
Denno, R., McClure, M. & Ott, J. (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annual Review of Entomology 40, 297331.Google Scholar
Dixon, A.F. (1998) Aphid Ecology: An Optimization Approach. 2nd edn.London, UK, Chapman & Hall.Google Scholar
Dixon, A.F. & Wratten, S.D. (1971) Laboratory studies on aggregation, size and fecundity in the black bean aphid, Aphis fabae Scop. Bulletin of Entomological Research 61, 97111.Google Scholar
Faeth, S. (1986) Indirect interactions between temporally separated herbivores mediated by the host plant. Ecology 67, 479494.Google Scholar
Fox, J. (2008) Applied Regression Analysis and Generalized Linear Models. 2nd edn.Thousand Oaks, CA, USA, Sage Publications.Google Scholar
Gharidi, V. (2002) Black ban aphid Aphis fabae Scopoli (Homopthera: Aphididae) an important pest of seed beet. Journal of Sugar Beet 18, 9394.Google Scholar
Greco, N., Llijesthrom, G. & Sánchez, N. (1999) Spatial distribution and coincidence of Neoseiulus californicus and Tetranychus urticae (Acari: Tetranychidae: Phytoseiidae) on strawberry. Experimental and Applied Acarology 23, 567580.Google Scholar
Greco, N.M., Tetzlaff, G.T. & Liljesthröm, G.G. (2004) Presence-absence sampling for Tetranychus urticae and its predator Neoseiulus californicus (Acari: Tetranychidae, Phytoseiidae) on strawberries in La Plata, Argentina. International Journal of Pest Management 50, 2327.Google Scholar
Greco, N.M., Liljesthröm, G.G., Ottaviano, Gugole M.F., Cluigt, N., Cingolani, M.F., Zembo, J.C. & Sánchez, N.E. (2011) Pest management plan for Tetranychus urticae based on the natural occurrence of Neoseiulus californicus (Acari: Tetranychidae, Phytoseiidae) in strawberry. International Journal of Pest Management 57, 299308.Google Scholar
Griffiths, K. (1969) The importance of coincidence in the functional response of two parasites of the european pine sawfly, Neodiprion sertifer. Canadian Entomology 101, 673713.Google Scholar
Hill, D. (1983) Agricultural Insect Pest of the Tropics and their Control. Cambridge, UK, Press Syndicate of the University of Cambridge.Google Scholar
Jones, M. & Russell, F. (2009) An evaluation of indirect interactions between herbivore guilds: effects of meristem miners on flower head feeders. pp. 116–117 in Proceedings of the 5th Annual GRASP Symposium, 1 May 2009, Wichita State University.Google Scholar
Kagata, H. & Ohgushi, T. (2001) Resource partitioning among three willow leaf miners: consequences of host plant phenology. Entomological Science 4, 257263.Google Scholar
Kaplan, I. & Denno, R. (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition. Ecology Letters 10, 977994.Google Scholar
Kaplan, I., Sardinelli, S. & Denno, R. (2009) Field evidence for indirect interactions between foliar-feeding insect and root-feeding nematode communities on Nicotiana tabacum. Ecological Entomology 34, 262270.Google Scholar
Karban, R. (1986) Interspecific competition between folivorous insects on Erigeron glaucus. Ecology 67, 10631072.CrossRefGoogle Scholar
Karban, R. & Baldwin, I. (1997) Induced Responses to Herbivory. Chicago, Il, USA, The University of Chicago Press.Google Scholar
Kareiva, P. (1986) Trivial movements and foraging by crop colonizers. pp. 5982in Kogan, M. (Ed.) Ecological Theory and Integrated Pest Management Practice. New York, USA, Willey & Sons.Google Scholar
Kennedy, G. & Smitley, D. (1985) Dispersal. pp. 233242in Helle, W. & Sabelis, M. (Eds) Spider Mites: Their Biology, Natural Enemies and Control. The Netherland, Elsevier.Google Scholar
Kielkiewicz, M. (1985) Ultrastructural changes in strawberry leaves infested by two-spotted spider mites. Entomologia Experimentalis et Applicata 37, 4954.Google Scholar
Kielkiewicz, M. & van de Vrie, M. (1983) Histological studies on strawberry leaves damaged by the two-spotted spider mite (Tetranychus urticae): some aspects of plant self defence. Faculteit Landbouwwettenschappen Gent 48, 236245.Google Scholar
Lindsey, J. (1997) Applying Generalized Linear Models. New York, USA, Springer Verlag.Google Scholar
Luczynski, A., Isman, M. & Raworth, D. (1990) Strawberry foliar phenolics and their relationship to development of the two-spotted spider mite. Journal of Economic Entomology 83, 557563.Google Scholar
Lynch, M.E., Kaplan, I., Dively, G.P. & Denno, R.F. (2006) Host-plant-mediated competition via induced resistance: interactions between pest herbivores on potatoes. Ecological Applications 16, 855864.Google Scholar
Masters, G. & Brown, V. (1997) Host-plant mediated interactions between spatially separated herbivores: effects on community structure. pp. 217237in Gange, A.C. & Brown, V.K. (Eds) Multitrophic Interactions in Terrestrial Systems. Oxford, UK, Blackwell Science.Google Scholar
Miles, P.W. (1972) The saliva of Hemiptera. Advances in Insect Physiology 9, 183255.Google Scholar
Miles, P.W. (1999) Aphid saliva. Biological Review 74, 4185.Google Scholar
Ohgushi, T. (2005) Indirect interaction webs: herbivore induced effects through trait change in plants. Annual Review of Ecology, Evolution and Systematics 36, 81105.Google Scholar
Ohgushi, T. (2008) Herbivore-induced indirect interaction webs on terrestrial plants: the importance of non-trophic, indirect, and facilitative interactions. Entomologia Experimentalis et Applicata 128, 217229.Google Scholar
Peeters, P., Gordon, S. & Read, J. (2007) Leaf biomechanical properties and the densities of herbivorous insect guilds. Functional Ecology 21, 246255.Google Scholar
Pianka, E.R. (1983) Evolutionary Ecology. New York, Usa, Harper & Row Publishers.Google Scholar
Powell, G., Tosh, C. & Hardie, J. (2005) Host plant selection by aphids: behavioural, evolutionary and applied perspective. Annual Review of Entomology 51, 309330.Google Scholar
Soroker, V., Grinberg, M., Adad, T., Katabi, D., Perl-Treves, R. & Walling, L. (2010) Broad mites and whiteflies: partners or rivals? p. 262 in Abstract, Book of XIII International Congress of Acarology, Recife, 23–27August 2010, Brasil.Google Scholar
Tjallingii, W.F. (1978) Electronic recording of penetration behaviour by aphids. Entomologia Experimentalis et Applicata 24, 521530.Google Scholar
van den Boom, C., van Beek, T.A., Posthumus, M.A., de Groot, A. & Dicke, M. (2004) Qualitative and quantitative variation among volatile profiles induced by Tetranychus urticae feeding on plants from various families. Journal Chemical Ecology 30, 6989.Google Scholar
van Emden, H., Eastop, V., Hughes, R. & Way, M. (1969) Ecology of Myzus persicae. Annual Review of Entomology 14, 197270.Google Scholar
van Veen, F., Morris, R. & Godfray, H. (2006) Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annual. Review. of Entomology 51, 187208.Google Scholar
van Zandt, P.A. & Agrawal, A.A. (2004) Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85, 26162629.Google Scholar
Vereijken, P.H. (1979) Feeding and multiplication of three cereal aphid species and their effect on yield of winter wheat. Agricultural Research Report 888 , Wageningen, The Netherlands, Pudoc.Google Scholar
Wyman, J., Oatman, E. & Voth, V. (1979) Effects of varying twospotted spider mite infestation levels on strawberry yield. Journal of Economic Entomolology 72, 747753.Google Scholar
Yano, S., Wakabayashi, M., Takabayashi, J. & Takafuji, A. (1998) Factors determining the host plant range of the phytophagous mite, Tetranychus urticae, (Acari: Tetranychidae) a method for quantifying host plant acceptance. Experimental and Applied Acarology 22, 595601.CrossRefGoogle Scholar
Zar, J. (1996) Biostatistical Analysis. NJ, USA, Prentice Hall.Google Scholar
Zucker, W. (1982) How aphids choose leaves: the roles of phenolics in host selection by a galling aphid. Ecology 63, 972981.Google Scholar