Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-15T01:31:53.332Z Has data issue: false hasContentIssue false

Predator performance is impaired by the presence of a second prey species

Published online by Cambridge University Press:  07 November 2016

D.B. Lima*
Affiliation:
Department of Agronomy – Entomology, Federal Rural University of Pernambuco, Av. Dom Manoel de Medeiros s/n, Dois Irmãos, 52171-900 Recife, PE, Brazil
H.K.V. Oliveira
Affiliation:
Department of Agronomy – Entomology, Federal Rural University of Pernambuco, Av. Dom Manoel de Medeiros s/n, Dois Irmãos, 52171-900 Recife, PE, Brazil
J.W.S. Melo
Affiliation:
Department of Fitotecnia, Federal University of Ceará, Fortaleza, CE, Brazil
M.G.C. Gondim Jr.
Affiliation:
Department of Agronomy – Entomology, Federal Rural University of Pernambuco, Av. Dom Manoel de Medeiros s/n, Dois Irmãos, 52171-900 Recife, PE, Brazil
M. Sabelis
Affiliation:
Institute of Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, The Netherlands
A. Pallini
Affiliation:
Department of Entomology, Federal University of Viçosa, Campus Universitário, 36570-000, Viçosa, MG, Brazil
A. Janssen
Affiliation:
Institute of Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, The Netherlands
*
*Author for correspondence Phone: +(55)(81) 3320-6207 Fax: +(55)(81) 3320-6207 E-mail: [email protected]

Abstract

The simultaneous infestation of a plant by several species of herbivores may affect the attractiveness of plants to the natural enemies of one of the herbivores. We studied the effect of coconut fruits infested by the pests Aceria guerreronis and Steneotarsonemus concavuscutum, which are generally found together under the coconut perianth. The predatory mite Neoseiulus baraki produced lower numbers of offspring on fruits infested with S. concavuscutum and on fruits infested with both prey than on fruits with A. guerreronis only. The predators were attracted by odours emanating from coconuts with A. guerreronis, but not by odours from coconuts with S. concavuscutum, even when A. guerreronis were present on the same fruit. Fewer N. baraki were recaptured on fruits with both prey or with S. concavuscutum than on fruits with only A. guerreronis. Furthermore, the quality of A. guerreronis from singly and multiply infested coconuts as food for N. baraki did not differ. Concluding, our results suggest that N. baraki does not perform well when S. concavuscutum is present on the coconuts, and the control of A. guerreronis by N. baraki may be negatively affected by the presence of S. concavuscutum.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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.)

References

Agrawal, A.A. & Klein, C.N. (2000) What omnivores eat: direct effects of induced plant resistance on herbivores and indirect consequences for diet selection by omnivores. Journal of Animal Ecology 69, 525535.Google Scholar
Bezemer, T.M., De Deyn, G.B., Bossinga, T.M., Van Dam, N.M., Harvey, J.A. & van der Putten, W.H. (2005) Soil community composition drives aboveground plant–herbivore–parasitoid interactions. Ecology Letters 8, 652661.Google Scholar
Campbell, B.C. & Duffey, S.S. (1979) Tomatine and parasitic wasps: potential incompatibility of plant antibiosis with biological control. Science 205, 700702.CrossRefGoogle ScholarPubMed
Crawley, M.J. (2007) The R Book. Chichester, UK, John Wiley & Sons Ltd. Google Scholar
Da Silva, F.R., de Moraes, G.J., Lesna, I., Sato, Y., Vasquez, C., Hanna, R., Sabelis, M.W. & Janssen, A. (2016) Size of predatory mites and refuge entrance determine success of biological control of the coconut mite. BioControl 19. doi: 10.1007/s10526-016-9751-2.Google Scholar
De Boer, J.G., Hordijk, C.A., Posthumus, M.A. & Dicke, M. (2008) Prey and non-prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction. Journal of Chemical Ecology 34, 281290.Google Scholar
Dicke, M., van Baarlen, P., Wessels, R. & Dijkman, H. (1993) Herbivory induces systemic production of plant volatiles that attract predators of the herbivore: extraction of endogenous elicitor. Journal of Chemical Ecology 3, 582599.Google Scholar
Dicke, M. & Sabelis, M.W. (1988) How plants obtain predatory mites as bodyguards. Netherlands Journal of Zoology 38, 148165.CrossRefGoogle Scholar
Dicke, M., van Beek, T.A., Posthumus, M.A., Ben Dom, N., van Bokhoven, N.H. & de Groot, A. (1990 a) Isolation and identification of volatile kairomone that affects acarine predator-prey interactions. Involvement of host plant in its production. Journal of Chemical Ecology 16, 381396.CrossRefGoogle Scholar
Dicke, M., Sabelis, M.W., Takabayashi, J., Bruin, J. & Posthumus, M.A. (1990 b) Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application in pest control. Journal of Chemical Ecology 16, 30913118.CrossRefGoogle ScholarPubMed
Domingos, C.A., Melo, J.W.S., Gondim, M.G.C., de Moraes, G.J., Hanna, R., Lawson-Balagbo, L.M. & Schausberger, P. (2010) Diet-dependent life history, feeding preference and thermal requirements of the predatory mite, Neoseiulus baraki (Acari: Phytoseiidae). Experimental & Applied Acarology 50, 201215.CrossRefGoogle ScholarPubMed
Fernando, L.C.P., Waidyarathne, K.P., Perera, K.F.G. & da Silva, P.H.P.R. (2010) Evidence for suppressing coconut mite, Aceria guerreronis by inundative release of the predatory mite, Neoseiulus baraki . Biological Control 53, 108111.Google Scholar
Galvão, A.S., Gondim, M.G.C. & Michereff, S.J. (2008) Escala diagramática de dano de Aceria guerreronis Keifer (Acari: Eriophyidae) em coqueiro. Neotropical Entomology 37, 723728.Google Scholar
Galvão, A.S., Melo, J.W.S., Monteiro, V.B., Lima, D.B., de Moraes, G.J. & Gondim, M.G.C. (2012) Dispersal strategies of Aceria guerreronis (Acari: Eriophyidae), a coconut pest. Experimental & Applied Acarology 57, 113.Google Scholar
Gange, A.C., Brown, V.K. & Aplin, D.M. (2003) Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids. Ecology Letters 6, 10511055.Google Scholar
Griffith, R. (1984) The problem of the coconut mite, Eriophyes guerreronis (Keifer), in the coconut groves of Trinidad and Tobago. pp. 128132. In Proceedings of 20th Annual Meeting of the Caribbean Food Crop Society, 21–26 October 1984 Coll. Virgin Islands & Caribbean Food Crops Society, Virgin Islands.Google Scholar
Guerrieri, E., Lingua, G., Digilio, M.C., Massa, N. & Berta, G. (2005) Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecological Entomology 30, 753756.Google Scholar
Haq, M.A. (2011) Coconut destiny after the invasion of Aceria guerreronis in India. Zoosymposia 6, 160169.CrossRefGoogle Scholar
Hothorn, T., Bretz, F. & Westfall, P. (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346363.Google Scholar
Janssen, A., Pallini, A., Venzon, M. & Sabelis, M.W. (1999) Absence of odour-mediated avoidance of heterospecific competitors by the predatory mite Phytoseiulus persimilis . Entomologia Experimentalis et Applicata 92, 7382.CrossRefGoogle Scholar
Lawson-Balagbo, L.M., Gondim, M.G.C., de Moraes, G.J., Hanna, R. & Schausberger, P. (2008) Exploration of the acarine fauna on coconut palm in Brazil with emphasis on Aceria guerreronis (Acari: Eriophyidae) and its natural enemies. Bulletin of Entomological Research 98, 8396.Google Scholar
Lima, D.B., Melo, J.W.S., Gondim, M.G.C. & de Moraes, G.J. (2012) Limitations of Neoseiulus baraki and Proctolaelaps bickleyi as control agents of Aceria guerreronis Keifer. Experimental & Applied Acarology 56, 233246.Google Scholar
Lofego, A.C. & Gondim, M.G.C. (2006) A new species of Steneotarsonemus (Acari: Tarsonemidae) from Brazil. Systematic & Applied Acarology 11, 195203.Google Scholar
Masters, G.J., Jones, T.H. & Rogers, M. (2001) Host-plant mediated effects of root herbivory on insect seed predators and their parasitoids. Oecologia 127, 246250.Google Scholar
Melo, J.W.S., Lima, D.B., Pallini, A., Oliveira, J.E.M. & Gondim, M.G.C. (2011) Olfactory response of predatory mites to vegetative and reproductive parts of coconut palm infested by Aceria guerreronis . Experimental & Applied Acarology 55, 191202.Google Scholar
Melo, J.W.S., Domingos, C.A., Pallini, A., Oliveira, J.E.M. & Gondim, M.G.C. (2012) Removal of bunches or spikelets is not effective for the control of Aceria guerreronis . HortScience 47, 15.Google Scholar
Melo, J.W.S., Lima, D.B., Sabelis, M.W., Pallini, A. & Gondim, M.G.C. (2014) Limits to ambulatory displacement of coconut mites in absence and presence of food-related cues. Experimental & Applied Acarology 62, 449461.Google Scholar
Melo, J.W.S., Lima, D.B., Staudacher, H., Silva, F.R., Gondim, M.G.C. & Sabelis, M.W. (2015) Evidence of Amblyseius largoensis and Euseius alatus as biological control agent of Aceria guerreronis . Experimental & Applied Acarology 67, 411421.Google Scholar
Moore, D. & Alexander, L. (1987) Aspects of migration and colonization of the coconut palm by the coconut mite, Eriophyes guerreronis (Keifer) (Acari: Eriophyidae). Bulletin of Entomological Research 77, 641650.CrossRefGoogle Scholar
Moore, D. & Howard, F.W. (1996) Coconuts. pp. 561570 in Lindquist, E.E., Sabelis, M.W. & Bruin, J. (Eds) Eriophyoid Mites: Their Biology, Natural Enemies and Control. Amsterdam, The Netherlands, Elsevier.Google Scholar
Monteiro, V.B., Lima, D.B., Gondim, M.G.C. & Siqueira, H.A.A. (2012) Residual bioassay to assess the toxicity of acaricides against Aceria guerreronis (Acari: Eriophyidae) under laboratory conditions. Journal of Economic Entomology 105, 14191425.Google Scholar
Navia, D., de Moraes, G.J., Roderick, G. & Navajas, M. (2005 a) The invasive coconut mite Aceria guerreronis (Acari: Eriophyidae): origin and invasion sources inferred from mitochondrial (16S) and nuclear (ITS) sequences. Bulletin of Entomological Research 95, 505516.CrossRefGoogle Scholar
Navia, D., de Moraes, G.J., Lofego, A.C. & Flechtmann, C.H.W. (2005 b) Acarofauna associada a frutos de coqueiro (Cocos nucifera L.) de algumas localidades das Américas. Neotropical Entomology 34, 349354.Google Scholar
Navia, D., Gondim, M.G.C., Aratchige, N.S. & de Moraes, G.J. (2013) A review of the status of the coconut mite, Aceria guerreronis (Acari: Eriophyidae), a major tropical mite pest. Experimental & Applied Acarology 59, 6794.CrossRefGoogle Scholar
Negloh, K., Hanna, R. & Schausberger, P. (2011) The coconut mite, Aceria guerreronis, in Benin and Tanzania: occurrence, damage and associated acarine fauna. Experimental & Applied Acarology 55, 361374.CrossRefGoogle ScholarPubMed
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., R Core Team (2014) NLME: Linear and Nonlinear Mixed Effects Models. http://CRAN.R-project.org/package=nlme Google Scholar
Ponzio, C., Gols, R., Weldegergis, B.T. & Dicke, M. (2014) Caterpillar-induced plant volatiles remain a reliable signal for foraging wasps during dual attack with a plant pathogen or non-host insect herbivore. Plant, Cell and Environment 37, 19241935.Google Scholar
Poveda, K., Steffan-Dewenter, I., Scheu, S. & Tscharntke, T. (2005) Effects of decomposers and herbivores on plant performance and aboveground plant-insect interactions. Oikos 108, 503510.Google Scholar
R Development Core Team (2014) R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing.Google Scholar
Rasmann, S. & Turlings, T.C.J. (2007) Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecology Letters 10, 926936.Google Scholar
Reis, A.C., Gondim, M.G.C. Jr, de Moraes, G.J., Hanna, R., Schausberger, P., Lawson-Balagbo, L.M. & Barros, R. (2008) Population dynamics of Aceria guerreronis Keifer (Acari: Eriophyidae) and associated predators on coconut fruits in northeastern Brazil. Neotropical Entomology 37, 457462.CrossRefGoogle ScholarPubMed
Rezende, D., Melo, J.W.S., Oliveira, J.E.M. & Gondim, M.G.C. (2016) Estimated crop loss due to coconut mite and financial analysis of controlling the pest using the acaricide abamectin. Experimental & Applied Acarology 69, 297310.Google Scholar
Rodriguez-Saona, C., Crafts-Brandner, S.J. & Canas, L.A. (2003) Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. Journal of Chemical Ecology 29, 25392550.Google Scholar
Sabelis, M.W. (1990) How to analyse prey preference when prey density varies? A new method to discriminate between effects of gut fullness and prey type composition. Oecologia 82, 289298.Google Scholar
Sabelis, M.W. & van de Baan, H.E. (1983) Location of distant spider mite colonies by phytoseiid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi . Entomologia Experimentalis et Applicata 40, 109115.Google Scholar
Shiojiri, K., Takabayashi, J., Yano, S. & Takafuji, A. (2001) Infochemically mediated tritrophic interaction webs on cabbage plants. Population Ecology 43, 2329.Google Scholar
Shiojiri, K., Takabayashi, J., Yano, S. & Takafuji, A. (2002) Oviposition preferences of herbivores are affected by tritrophic interaction webs. Ecology Letters 5, 186192.Google Scholar
Schwartzberg, E.G., Böröczky, K. & Tumlinson, J.H. (2011) Pea aphids, Acyrthosiphon pisum, suppress induced plant volatiles in broad bean, Vicia faba . Journal of Chemical Ecology 37, 10551062.CrossRefGoogle ScholarPubMed
Soler, R., Bezemer, T.M., van der Putten, W.H., Vet, L.E.M. & Harvey, J.A. (2005) Root herbivore effects on above-ground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality. Journal of Animal Ecology 74, 11211130.Google Scholar
Soler, R., Harvey, J.A., Kamp, A.F.D., Vet, L.E.M., van der Putten, W.H., Van Dam, N.M., Stuefer, J.F., Gols, R., Hordijk, K.A. & Bezemer, T.M. (2007 a) Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals. Oikos 116, 367376.Google Scholar
Soler, R., Harvey, J.A. & Bezemer, T.M. (2007 b) Foraging efficiency of a parasitoid of a leaf herbivore is influenced by root herbivory on neighbouring plants. Functional Ecology 21, 969974.Google Scholar
Sumangala, K. & Haq, M.A. (2005) Diurnal periodicity and dispersal of coconut mite, Aceria guerreronis Keifer. Journal of Entomological Research 29, 303307.Google Scholar
Turlings, T.C.J. & Tumlinson, J.H. (1992) Systemic release of chemical signals by herbivore- injured corn. Proceedings of the National Academy of Sciences of the United States of America 89, 83998402.Google Scholar
Turlings, T.C.J., Tumlinson, J.H. & Lewis, W.J. (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250, 12511253.Google Scholar
Zhang, P.J., Zheng, S.J., van Loon, J.J.A., Boland, W., David, A., Mumm, R. & Dicke, M. (2009) Whiteflies interfere with indirect plant defense against spider mites in Lima bean. Proceedings of the National Academy of Sciences of the United States of America 106, 2120221207.Google Scholar
Zhang, P.J., Broekgaarden, C., Zheng, S.J., Snoeren, T.A.L., van Loon, J.J.A., Gols, R. & Dicke, M. (2013) Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana . New Phytologist 197, 12911299.Google Scholar