Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-25T20:58:52.429Z Has data issue: false hasContentIssue false
  • English
  • Français

Alternative food improves the combined effect of an omnivore and a predator on biological pest control. A case study in avocado orchards

Published online by Cambridge University Press:  08 December 2008

J.J. González-Fernández ,
F. de la Peña ,
J.I. Hormaza ,
J.R. Boyero ,
J.M. Vela ,
E. Wong ,
M.M. Trigo  and
M. Montserrat
J.J. González-Fernández
Affiliation:
E.E. La Mayora, CSIC,29750 Algarrobo-Costa, Málaga, Spain
F. de la Peña
Affiliation:
E.E. La Mayora, CSIC,29750 Algarrobo-Costa, Málaga, Spain
J.I. Hormaza
Affiliation:
E.E. La Mayora, CSIC,29750 Algarrobo-Costa, Málaga, Spain
J.R. Boyero
Affiliation:
IFAPA, Centro de Churriana, Cortijo de la Cruz, s/n, 29140 Churriana, Málaga, Spain
J.M. Vela
Affiliation:
IFAPA, Centro de Churriana, Cortijo de la Cruz, s/n, 29140 Churriana, Málaga, Spain
E. Wong
Affiliation:
IFAPA, Centro de Churriana, Cortijo de la Cruz, s/n, 29140 Churriana, Málaga, Spain
M.M. Trigo
Affiliation:
Departamento Biología Vegetal, Universidad de Málaga, Campus de Teatinos, 29080 Málaga, Spain
M. Montserrat*
Affiliation:
E.E. La Mayora, CSIC,29750 Algarrobo-Costa, Málaga, Spain
*
*Author for correspondence Fax: +34 952552677 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Ecological communities used in biological pest control are usually represented as three-trophic level food chains with top-down control. However, at least two factors complicate this simple way of characterizing agricultural communities. First, agro-ecosystems are composed of several interacting species forming complicated food webs. Second, the structure of agricultural communities may vary in time. Efficient pest management approaches need to integrate these two factors to generate better predictions for pest control. In this work, we identified the food web components of an avocado agro-ecosystem, and unravelled patterns of co-occurrence and interactions between these components through field and laboratory experiments. This allowed us to predict community changes that would improve the performance of the naturally occurring predators and to test these predictions in field population experiments. Field surveys revealed that the food-web structure and species composition of the avocado community changed in time. In spring, the community was characterized by a linear food chain of Euseius stipulatus, an omnivorous mite, feeding on pollen. In the summer, E. stipulatus and a predatory mite, Neoseiulus californicus, shared a herbivorous mite prey. Laboratory experiments confirmed these trophic interactions and revealed that N. californicus can feed inside the prey nests, whereas E. stipulatus cannot, which may further reduce competition among predators. Finally, we artificially increased the coexistence of the two communities via addition of the non-herbivore food source (pollen) for the omnivore. This led to an increase in predator numbers and reduced populations of the herbivore. Therefore, the presence of pollen is expected to improve pest control in this system.

Keywords

food-web dynamicscommunity structureOlygonychus perseaePhytoseiidaeIntraguild predationapparent competition
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 99 , Issue 5 , October 2009 , pp. 433 - 444
Copyright
Copyright © 2008 Cambridge University Press

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

Addison, J.A., Hardman, J.M. & Walde, S.J. (2000) Pollen availability for predacious mites on apple: spatial and temporal heterogeneity. Experimental and Applied Acarology 24, 1–18.Google Scholar
Aponte, O. & McMurtry, J.R. (1997) Damage on ‘Hass’ avocado leaves, webbing and nesting behaviour of Oligonychus perseae (Acari: Tetranichidae). Experimental and Applied Acarology 21, 265–272.CrossRefGoogle Scholar
Armstrong, W.W. (1964) Distribution of oil cells in Persea. Master Thesis. University of California, Riverside, CA, USA.Google Scholar
Birkhofer, K., Wise, D.H. & Scheu, S. (2007) Subsidy from detrital food web, but not microhabitat complexity, affects the rol of generalist predators in an aboveground herbivore food web. Oikos 117, 494–500.CrossRefGoogle Scholar
Breslow, N.E. (1996) Generalized linear models: checking assumptions and strengthening conclusions. Statistics Applications 8, 23–41.Google Scholar
Çakmak, I., Janssen, A. & Sabelis, M.W. (2006) Intraguild interactions between the predatory mites Neoseiulus californicus and Phytoseiulus persimilis. Experimental and Applied Acarology 38, 33–46.Google Scholar
Diehl, S. & Feißel, M. (2000) Effects of enrichment on three-level food chains with omnivory. American Naturalist 155, 200–218.CrossRefGoogle ScholarPubMed
Diehl, S. & Feissel, M. (2001) Intraguild prey suffer from enrichment of their resources: A microcosm experiment with ciliates. Ecology 82, 2977–2983.CrossRefGoogle Scholar
Domínguez, E., Galán, C., Villamandos, F. & Infante, F. (1991) Manejo y evaluación de los datos obtenidos en los muestreos aerobiológicos. Monografías REA/EAN 1, 1–18.Google Scholar
Faraji, F., Janssen, A. & Sabelis, M.W. (2002) Oviposition patterns in a predatory mite reduce the risk of egg predation caused by prey. Ecological Entomology 27, 660–664.Google Scholar
Ferragut, F. & Escudero, A. (1997) Taxonomía y distribución de los ácaros depredadores del género Euseius Wainstein 1962, en España (Acari: Phytoseiidae). Boletín Sanidad Vegetal Plagas 23, 227–235.Google Scholar
Ferragut, F., García-Marí, F., Costa-Comelles, J. & Laborda, R. (1987) Influence of food and temperature on development and oviposition of Euseius stipulatus and Typhlodromus phialatus (Acari: Phytoseiidae). Experimental and Applied Acarology 3, 317–329.Google Scholar
Galán-Soldevilla, C., Cariñanos González, P., Alcázar Teno, P. & Domínguez Vilches, E. (2007) Manual de Calidad y Gestión de la Re Española de Aerobiología. 39 pp. Córdoba, Spain, Universidad de Córdoba.Google Scholar
Garcia-Marí, F., Ferragut, F., Costa-Comelles, J. & Marzal, C. (1984) Population dynamics of the citrus red mite Panonychus citri (McGr.) and its predators in Spanish citrus orchards. pp. 459–465 in Proceedings of the International Society of Citriculture, 5th International Citrus Congress 1984, São Paulo, Brazil.Google Scholar
García-Marí, F., Ferragut, F., Costa-Comelles, J., Roca, D., Laborda, R. & Marzal, C. (1987) Cursillo de Acarología Agrícola. 362 pp. Valencia, Spain, Universidad Politécnica de Valencia.Google Scholar
González-Fernández, J. & Hermoso, J.M. (2005) Control del ácaro cristalino del aguacate. La Caña 10, 18–20.Google Scholar
Gratton, C. & Denno, R.F. (2003) Seasonal shift from bottom-up to top-down impact in phytophagous insect populations. Oecologia 134, 487–495.CrossRefGoogle ScholarPubMed
Gutierrez, J. (1985) Mounting techniques. pp. 351–353in Helle, W. & Sabelis, M.W.(Eds) Spider Mites, Their Biology, Natural Enemies and Control, vol. 1. Amsterdam, The Netherlands, Elsevier Science Ltd.Google Scholar
Hairston, N.G., Smith, F.E. & Slobodkin, L.B. (1960) Community structure, population control, and competition. American Naturalist XCIV, 421–425.Google Scholar
Hatherly, I.S., Bale, J.S. & Walters, K.F.A. (2005) Intraguild predation and feeding preferences in three species of phytoseiid mite used for biological control. Experimental and Applied Acarology 37, 43–55.CrossRefGoogle ScholarPubMed
Holt, R.D. (1977) Predation, apparent competition, and the structure of prey communities. Theoretical Population Biology 12, 197–229.Google Scholar
Holt, R.D. & Lawton, J.H. (1994) The ecological consecuences of shared natural enemies. Anuual Review of Ecology and Systematics 25, 495–520.CrossRefGoogle Scholar
Holt, R.D. & Polis, G.A. (1997) A theoretical framework for intraguild predation. American Naturalist 149, 745–764.CrossRefGoogle Scholar
Huang, C.F. & Sih, A. (1990) Experimental studies on behaviourally mediated, indirect interactions through a shared predator. Ecology 71, 1515–1522.Google Scholar
Hunter, M.D. & Price, P.W. (1992) Playing chutes and ladders – Heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73, 724–732.Google Scholar
Hutchins, S.H. (1994) Techniques for sampling arthropods in integrated pest management. pp. 73–97in Pedigo, P. & Buntin, G.D.(Eds) Handbook of Sampling Methods for Arthropods in Agriculture. Boca Raton, FL, USA, CRC Press.Google Scholar
Janssen, A., Montserrat, M., HilleRisLambers, R., de Roos, A.M., Pallini, A. & Sabelis, M.W. (2006) Intraguild predation usually does not disrupt biological control. pp. 21–44in Boivin, G. & Brodeur, J.(Eds) Trophic and Guild Interactions in Biological Control. Dordrecht, Holland, Springer Verlag.CrossRefGoogle Scholar
Janssen, A., Sabelis, M.W., Magalhães, S., Montserrat, M. & van der Hammen, T. (2007) Habitat structure affects intraguild predation. Ecology 88, 2713–2719.CrossRefGoogle ScholarPubMed
Judge, G.G., Griffith, W.E., Hill, R.C., Luetkepohl, H. & Lee, T.S. (1985) The Theory and Practice of Econometrics. 1056 pp.New York, USA, Wiley & Sons.Google Scholar
Karban, R., Hougeneitzmann, D. & Englishloeb, G. (1994). Predator-mediated apparent competition between 2 herbivores that feed on grapevines. Oecologia 97, 508–511.CrossRefGoogle Scholar
Lawler, S.P. & Morin, P.J. (1993) Food web architecture and population dynamics in laboratory microcosms of protists. American Naturalist 141, 675–686.CrossRefGoogle ScholarPubMed
Lima, S.L. (1998) Nonlethal effects in the ecology of predator-prey interactions. BioScience 48, 25–34.Google Scholar
Lima, S.L. & Dill, L.M. (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68, 619–640.CrossRefGoogle Scholar
Liu, C.Z., Yan, L., Li, H.R. & Wang, G. (2006) Effects of predator-mediated apparent competition on the population dynamics of Tetranichus urticae on apples. BioControl 51, 453–463.CrossRefGoogle Scholar
Magalhães, S., Tudorache, C., Montserrat, M., van Maanen, R., Sabelis, M.W. & Janssen, A. (2005a) Diet of intraguild predators affects antipredator behavior in intraguild prey. Behavioral Ecology 16, 364–370.Google Scholar
Magalhães, S., Janssen, A., Montserrat, M. & Sabelis, M.W. (2005b) Prey attack and predators defend: counterattacking prey trigger parental care in predators. Proceedings of the Royal Society of London Series B 272, 1929–1933.Google Scholar
McMurtry, J.A. & Croft, B.A. (1997) Life-styles of phytoseiid mites and their roles in biological control. Annual Review of Entomology 42, 291–321.Google Scholar
McMurtry, J.A. & Scriven, G.T. (1965) Studies on predator-prey interactions between Amblyseius hibisci and Oligonychus punicae (Acarina: Phytoseiidae, Tetranichidae) under greenhouse conditions. Annals of the Entomological Society of America 59, 793–800.Google Scholar
Montserrat, M., Janssen, A., Magalhães, S. & Sabelis, M.W. (2006) To be an intra-guild predator or a cannibal: is prey quality decisive? Ecological entomology 31, 430–436.Google Scholar
Montserrat, M., Magalhães, S., Sabelis, M.W., de Roos, A.M. & Janssen, A. (2008a) Patterns of exclusion in an intraguild predator-prey system strongly depend on initial conditions. Journal of Animal Ecology 77, 624–630.CrossRefGoogle Scholar
Montserrat, M., de la Peña, F., Hormaza, J.I. & González-Fernández, J.J. (2008b) How do Neoseiulus californicus (Acari: Phytoseiidae) females penetrate densely webbed spider mite nests? Experimental and Applied Acarology 44, 101–106.CrossRefGoogle ScholarPubMed
Mori, K., Saito, Y. & Sakagami, T. (1999) Efects of the nest web and female attendance on survival of young in a subsocial spider mite, Schizotetranychus longus (Acari: Tetranychidae). Experimental and Applied Acarology 23, 411–418.Google Scholar
Morin, P.J. (1999) Productivity, intraguild predation, and population dynamics in experimental food webs. Ecology 80, 752–760.CrossRefGoogle Scholar
Morris, R.J., Lewis, O.T. & Godfray, H.C.J. (2004) Experimental evidence of apparent competition in a tropical forest food web. Nature 428, 310–313.Google Scholar
Muller, C.B. & Godfray, H.C.J. (1997) Apparent competition between two aphid species. Journal of Animal Ecology 66, 57–64.Google Scholar
Mylius, S.D., Klumpers, K., de Roos, A.M. & Persson, L. (2001) Impact of omnivory and stage structure on food web composition along a productivity gradient. American Naturalist 158, 259–276.Google Scholar
Nelder, J.A. & Wedderburn, R.W.M. (1972) Generalized linear models. Journal of the Royal Statistical Society, Series A 135, 370–384.Google Scholar
Oksanen, L., Fretwell, S.D., Arruda, J. & Niemela, P. (1981) Exploitation ecosystems in gradients of primary productivity. American Naturalist 118(2), 240–261.Google Scholar
Onzo, A., Hanna, R., Negloh, K., Toko, M. & Sabelis, M.W. (2005) Biological control of cassava green mite with exotic and indigenous phytoseiid predators – Effects of intraguild predation and supplementary food. Biological Control 33, 143–152.Google Scholar
Ovadia, O. & Schmitz, O.J. (2004) Weather variation and trophic interaction strength: sorting the signal from the noise. Oecologia 140, 398–406.Google Scholar
Parker, K.R. & Wiens, J.A. (2005) Assessing recovery following environmental accidents: Environmental variation, ecological assumptions, and strategies. Ecological Applications 15, 2037–2051.Google Scholar
Platt, K.A. & Thompson, W.W. (1992) Idioblast oil cells of avocado: Distribution, isolation, ultraestructure, histiochemistry, and biochemistry. International Journal of Plant Sciences 153, 301–310.Google Scholar
Platt-Aloia, K.A., Oross, J.W. & Thompson, W.W. (1983) Ultraestructure and development of oil cells in mesocarp of avocado fruit. Botanical Gazette 144, 49–55.Google Scholar
Polis, G.A. & Strong, D.R. (1996) Food web complexity and community dynamics. American Naturalist 147, 813–846.Google Scholar
Polis, G.A., Myers, C.A. & Holt, R.D. (1989) The ecology and evolution of intraguild predation – potential competitors that eat each other. Annual Review of Ecology and Systematics 20, 297–330.Google Scholar
Rodriguez-Soana, C. & Trumble, J.T. (2000) Secretory avocado idioblast oil cells: evidence of their defensive role against non-adapted insect herbivore. Entomologia Experimentalis et Applicatta 94, 183–194.Google Scholar
Rodriguez-Soana, C., Millar, J.G. & Trumble, J.T. (1997) Growth inhibitory, insecticidal, and feeding deterrent effects of (12Z,15Z)-1-acetoxy-2-hydroxy-4-oxo-heneicosa-12,15,-dienne, a compound from avocado fruit, to Spodoptera exigua. Journal of Chemical Ecology 23, 1819–1831.Google Scholar
Rodriguez-Soana, C., Millar, J.G., Maynard, D.F. & Trumble, J.T. (1998) Novel antifeedant and insecticidal compounds from avocado idioblast cell oil. Journal of Chemical Ecology 24, 867–889.Google Scholar
Rosenheim, J.A., Kaya, H.K., Ehler, L.E., Marois, J.J. & Jaffee, B.A. (1995) Intraguild predation among biological control agents – theory and evidence. Biological Control 5, 303–335.Google Scholar
Schausberger, P. (2003) Cannibalism among phytoseiid mites: A review. Experimental and Applied Acarology 29, 173–191.Google Scholar
Southwood, T.R.E. (1978) Ecological Methods with Particyular Reference to the Study of Insect Populations, 2nd edn.524 pp. London, UK, Chapman & Hall.Google Scholar
Summerville, K.S., Bonte, A.C. & Fox, L.C. (2007) Short-term temporal effects on community structure of Lepidoptera in restored and remnant tallgrass prairies. Restoration Ecology 15, 179–188.CrossRefGoogle Scholar
van Rijn, P.C.J. & Tanigoshi, L.K. (1999) Pollen as food source for the predatory mites Iphiseius degenerans and Neoseiulus cucumeris (Acari: Phytoseiidae): dietary range and life history. Experimental and Applied Acarology 23, 785–802.Google Scholar
Vela, J.M., González-Fernández, J., Wong, E., Montserrat, M., Farré, J.M. & Boyero, J.R. (2007) El ácaro del aguacate (Oligonychus perseae): Estado actual del problema e investigación en Andalucía. Agrícola Vergel 306, 301–308.Google Scholar
Zannou, I.D., Hanna, R., de MoRaes, G.J. & Kreiter, S. (2005) Cannibalism and interspecific predation in a phytoseiid predator guild from cassava fields in Africa: evidence from the laboratory. Experimental and Applied Acarology 37, 27–42.Google Scholar