Hostname: page-component-8448b6f56d-c4f8m Total loading time: 0 Render date: 2024-04-25T01:39:34.581Z Has data issue: false hasContentIssue false

Impact of natural control agents of the citrus leafminer Phyllocnistis citrella on lemon trees varies among seasons

Published online by Cambridge University Press:  07 September 2015

L. Goane*
Affiliation:
Facultad de Agronomía y Zootecnia, Consejo Nacional de Investigaciones Científicas y Técnicas – CONICET, Tucumán, Argentina
A. Casmuz
Affiliation:
Estación Experimental Agroindustrial Obispo Colombres, Sección Zoología Agrícola – EEAOC, Tucumán, Argentina
H. Salas
Affiliation:
Estación Experimental Agroindustrial Obispo Colombres, Sección Zoología Agrícola – EEAOC, Tucumán, Argentina
E. Willink
Affiliation:
Estación Experimental Agroindustrial Obispo Colombres, Sección Zoología Agrícola – EEAOC, Tucumán, Argentina
A. Mangeaud
Affiliation:
Facultad de Ciencias Exactas, Físicas y Naturales – FCEFN, Córdoba, Argentina
G. Valladares
Affiliation:
Facultad de Ciencias Exactas, Físicas y Naturales – FCEFN, Córdoba, Argentina Instituto Multidisciplinario de Biología Vegetal – IMBIV (CONICET), Córdoba, Argentina
*
*Author for correspondence Phone: (54) 381-439-0003 E-mail: lugoane@gmail.com

Abstract

Studies on insect natural enemies and their effects on host populations are of immense practical value in pest management. Predation and parasitism on a citrus pest, the leafminer Phyllocnistis citrella Stainton, were evaluated by sampling over 3 years in four locations within a world leading lemon producing area in Northwest Argentina. Both mortality factors showed seasonal trends consistent across locations, with predation exerting earlier and more sustained pressure than parasitism, which showed wider seasonal variations. The dominant parasitoids, native Cirrospilus neotropicus and introduced Ageniaspis citricola, showed different seasonal trends: C. neotropicus was dominant in spring whereas A. citricola superseded it in autumn and winter. Although parasitism rates were relatively low, the native C. neotropicus revealed favourable features as potential control agent, by showing density-dependence, parasitism rates comparable with those of the specific A. citricola during part of the cycle, and earlier synchronization with the host. The study provides highly relevant information for a sustainable management of this worldwide pest, for which biological control is considered the best long-term option.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2015 

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

Amalin, D.M., Peña, J.E., Duncan, R.E., Browning, H.W. & McSorley, R. (2002) Natural mortality factors acting on citrus leafminer, Phyllocnistis citrella, in lime orchards in South Florida. BioControl 47, 327347.CrossRefGoogle Scholar
Ateyyat, M.A. (2002) Parasitoid complex of citrus leafminer, Phyllocnistis citrella on lemon in the Central Jordan Valley. BioControl 47, 3343.CrossRefGoogle Scholar
Auerbach, M.J., Connor, E.F. & Mopper, S. (1995) Minor miners and major miners: population dynamics of leaf-mining insects. pp. 83110 in Cappuccino, N. & Price, P.W. (Eds) Population Dynamics, Novel Approaches and Synthesis. San Diego, California, Academic Press.Google Scholar
Berti Filho, I. & Ciociola, A.I. (2002) Parasitóides ou predadores? Vantagens e desvantagens. pp. 2941 in Parra, J.R., Botelho, P.S., Corrêa-Ferreira, B.S. & Bento, J.M.S. (Eds) Controle biológico no Brasil: parasitóides e predadores. São Paulo, Brasil, Manole.Google Scholar
Calabuig, A., Garcia-Marí, F., Pekas, A. (2014) Ants affect the infestation levels but not the parasitism of honeydew and non-honeydew producing pests in citrus. Bulletin of Entomological Research 104, 405417.CrossRefGoogle Scholar
Christiano, R.S.C., Dalla Pria, M., Jesus Junior, W.C., Parra, J.R.P., Amorim, L. & Bergamin Filho, A. (2007) Effect of citrus leaf-miner damage, mechanical damage and inoculum concentration on severity of symptoms of Asiatic citrus canker in Tahiti lime. Crop Protection 26, 5965.CrossRefGoogle Scholar
Colloff, M.J., Lindsay, E.A., Cook, D.C. (2013) Natural pest control in citrus as an ecosystem service: integrating ecology, economics and management at the farm scale. Biological Control 67, 170177.CrossRefGoogle Scholar
Diez, P.A., Peña, J.E. & Fidalgo, P. (2006) Population dynamics of Phyllocnistis citrella (Lepidoptera: Gracillariidae) and its parasitoids in Tafí Viejo, Tucumán, Argentina. Florida Entomologist 89, 328335.CrossRefGoogle Scholar
Eber, S. (2004) Bottom-up density regulation in the holly leaf-miner Phytomyza ilicis . Journal of Animal Ecology 73, 948958.CrossRefGoogle Scholar
Ehler, L.E. (1998) Invasion biology and biological control. Biological Control 13, 127133.CrossRefGoogle Scholar
Elekçioğlu, N.Z. & Uygun, N. (2013) Population fluctuation of citrus leafminer, Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) and its parasitoids in the eastern Mediterranean region of Turkey. Pakistan Journal of Zoology 45, 13931403.Google Scholar
FAO (2012) Citrus Fruit, Fresh and Processed, Annual Statistics 2012. [www document]. URL http://www.fao.org/fileadmin/templates/est/COMM_MARKETS_MONITORING/Citrus/Documents/CITRUS_BULLETIN_2012.pdf Google Scholar
Foelkel, E., Redaelli, L.R., Jahnke, S.M. & Losekann, P.B. (2009) Predation and parasitism of Cirrospilus neotropicus (Hymenoptera: Eulophidae) on Phyllocnistis citrella (Lepidoptera: Gracillariidae) in laboratory. Revista Colombiana Entomología 35, 156162.CrossRefGoogle Scholar
Garcia-Mari, F., Vercher, R., Costa-Comelles, J., Marzal, C. & Villalba, M. (2004) Establishment of Citrostichus phyllocnistoides (Hymenoptera: Eulophidae) as a biological control agent for the citrus leafminer Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Spain. Biological Control 29, 215226.CrossRefGoogle Scholar
Girardoz, S., Quicke, D.L.J. & Kenis, M. (2007) Factors favouring the development and maintenance of outbreaks in an invasive leaf miner Cameraria ohridella (Lepidoptera: Gracillariidae): a life table study. Agricultural and Forest Entomology 9, 141158.CrossRefGoogle Scholar
Goane, L., Valladares, G. & Willink, E. (2008) Preference and performance of Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) on three citrus hosts: laboratory and field assessment. Environmental Entomology 37, 10251034.CrossRefGoogle ScholarPubMed
Grabenweger, G., Kehrli, P., Schlick-Steiner, B., Steiner, F., Stolz, M. & Bacher, S. (2005) Predator complex of the horse chestnut leafminer Cameraria ohridella: identification and impact assessment. Journal of Applied Entomology 129, 353362.CrossRefGoogle Scholar
Graham, J.H., Gottwald, T.R., Cubero, J. & Achor, D.S. (2004) Xanthomonas axonopodis pv. citri: factors affecting successful eradication of citrus canker. Molecular Plant Pathology 5, 115.CrossRefGoogle ScholarPubMed
Gratton, C. & Denno, R.F. (2003) Seasonal shift from bottom-up to top-down impact in phytophagous insect populations. Oecologia 134, 487495.CrossRefGoogle ScholarPubMed
Gripenberg, S. & Roslin, T. (2008) Neither the devil nor the deep blue sea: larval mortality factors fail to explain the abundance and distribution of Tischeria ekebladella . Ecological Entomology 33, 346356.CrossRefGoogle Scholar
Hawkins, B.A. (1994) Pattern and Process in Host-parasitoid Interactions. Cambridge, UK, Cambridge University Press.CrossRefGoogle Scholar
Hawkins, B.A. (2001) Top-down and bottom-up forces in the population and community ecology of insects. Basic Applied Ecology 2, 293294.CrossRefGoogle Scholar
Hixon, M.A., Pacala, S.W. & Sandin, S.A. (2002) Population regulation: historical context and contemporary challenges of open vs. closed systems. Ecology 83, 14901508.CrossRefGoogle Scholar
Hoy, M.A. & Jessey, C. (2004) Ageniaspis citricola (Hymenoptera: Encyrtidae) established in Bermuda. Florida Entomologist 87, 229230.CrossRefGoogle Scholar
Hoy, M.A. & Nguyen, R. (1997) Classical biological control of the citrus leafminer Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae): theory, practice, art and science. Tropical Lepidoptera 8, 19.Google Scholar
Karamaouna, F., Pascual-Ruiz, S., Aguilar-Fenollosa, E., Verdú, M.J., Urbaneja, A. & Jacas, J.Á. (2010) Changes in predation and parasitism of the citrus leafminer Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) populations in Spain following establishment of Citrostichus phyllocnistoides (Hymenoptera: Eulophidae). Biological Control 52, 3745.CrossRefGoogle Scholar
Kidd, N.A.C. & Jervis, M.A. (1996) Population dynamics. pp. 293374 in Jervis, M. & Kidd, N. (Eds) Insect Natural Enemies. London, UK, Chapman & Hall.CrossRefGoogle Scholar
Langor, D.W., Digweed, S.C., Williams, D.J.M., Spence, J.R. & Saunders, C. (2000) Establishment and spread of two introduced parasitoids (Ichneumonidae) of the birch leafminer, Fenusa pusilla (Lepeletier) (Tenthredinidae). BioControl 45, 415423.CrossRefGoogle Scholar
Legaspi, J.C., French, J.V., Zuniga, A.G.& Legaspi, B.C. Jr. (2001) Population dynamics of the citrus leafminer, Phyllocnistis citrella (Lepidoptera: Gracillariidae), and its natural enemies in Texas and Mexico. Biological Control 21, 8490.CrossRefGoogle Scholar
Lioni, A.S.R. & Cividanes, F.J. (2004) Tabela de vida ecológica do minador-do-citros, Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae). Neotropical Entomology 33, 407415.CrossRefGoogle Scholar
Lomeli-Flores, J.R., Barrera, J.F. & Bernal, J.S. (2009) Impact of natural enemies on coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) population dynamics in Chiapas, Mexico. Biological control 51, 5160.CrossRefGoogle Scholar
Mafi, S.A. & Ohbayashi, N. (2004) Seasonal prevalence of the citrus leafminer, Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) and its parasitoids in controlled and uncontrolled Citrus iyo groves in Ehime Prefecture. Applied Entomology and Zoology 39, 597601.CrossRefGoogle Scholar
Matsumoto, T., Itioka, T. & Nishida, T. (2004) Is spatial density-dependent parasitism necessary for successful biological control? Testing a stable host–parasitoid system. Entomologia Experimentalis et Applicata 110, 191200.CrossRefGoogle Scholar
Miller, T.E.X. (2008) Bottom-up, top-down, and within-trophic level pressures on a cactus-feeding insect. Ecological Entomology 33, 261268.CrossRefGoogle Scholar
Mustafa, I., Arshad, M., Ghani, A., Ahmad, I., Raza, A.B.M., Saddique, F., Asif, S., Khan, M.R. & Ahmed, H. (2014) Population dynamics of citrus leaf miner on different varieties of citrus in correlation with abiotic environmental factors in Sargodha District, Punjab, Pakistan. Phytoparasitica 42, 341348.CrossRefGoogle Scholar
Naranjo, S.E., Ellsworth, P.C. & Frisvold, G.B. (2015) Economic value of biological control in integrated pest management of managed plant systems. Annual Review of Entomology 60, 621645.CrossRefGoogle ScholarPubMed
Peña, J.E., Duncan, R. & Browning, H. (1996) Seasonal abundance of Phyllocnistis citrella (Lepidoptera: Gracillariidae) and its parasitoids in South Florida citrus. Environmental Entomology 25, 698702.CrossRefGoogle Scholar
Pomerinke, M.A. & Stansly, P.A. (1998) Establishment of Ageniaspis citricola (Hymenopera: Encyrtidae) for biological control of Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Florida. Florida Entomologist 81, 361372.CrossRefGoogle Scholar
Queiroz, J.M. (2002) Distribution, survivorship and mortality sources in immature stages of the neotropical leaf miner Pachyschelus coeruleipennis Kerremans (Coleoptera: Buprestidae). Brazilian Journal of Biology 62, 6976.CrossRefGoogle ScholarPubMed
Rott, A.S. & Ponsonby, D.J. (2000) The effects of temperature, relative humidity and host plant on the behavior of Stethorus punctillum as a predator of the two-spotted spider mite, Tetranychus urticae . BioControl 45, 155164.CrossRefGoogle Scholar
Salvo, A. & Valladares, G.R. (2007) Leafminer parasitoids and pest management. Ciencia e Investigación Agrícola 34, 125142.CrossRefGoogle Scholar
Santolamazza-Carbone, S., Velasco, P., Soengas, P. & Cartea, M.E. (2014) Bottom-up and top-down herbivore regulation mediated by glucosinolates in Brassica oleracea var. acephala. Oecologia 174, 893907.CrossRefGoogle ScholarPubMed
Sarada, G., Gopal, K., Gouri Sankar, T., Mukunda Lakshmi, L., Gopi, V., Nagalakshmi, T. & Ramana, K.T.V. (2014) Citrus leaf miner (Phyllocnistis citrella Stainton, Lepidoptera: Gracillariidae): biology and management: a review. Journal of Agriculture and Allied Sciences 3, 3948.Google Scholar
Schowalter, T.D. (2006) Insect Ecology: An Ecosystem Approach. Louisiana, Academic Press.Google Scholar
Smith, D., Beattie, G.A.C. & Broadley, R.H. (1997) Citrus Pests and Their Natural Enemies; Integrated Pest Management in Australia. Brisbane, Australia, Queensland Department of Primary Industries.Google Scholar
Speight, M.R., Hunter, M.D. & Watt, A.D. (2008) Ecology of Insects: Concepts and Applications. London, Wiley-Backwell.Google Scholar
Symondson, W.O.C., Sunderland, K.D. & Greenstone, M.H. (2002) Can generalist predators be effective biocontrol agents? Annual Review of Entomology 47, 561594.CrossRefGoogle ScholarPubMed
Tsagkarakis, A.E., Perdikis, D.C. & Lykouressis, D.P. (2013) Introduced and native parasitoids of Phyllocnistis citrella Station in Greece: short term post-release evaluation. Phytoparasitica 41, 417428.CrossRefGoogle Scholar
Urbaneja, A. & Jacas, J.A. (2003). Predación de Phyllocnistis citrella: importancia de la fauna auxiliar generalista y su conservación en cítricos. Phytoma España 153, 171172.Google Scholar
Urbaneja, A., Llácer, E., Tomás, Ó., Garrido, A. & Jacas, J.A. (2000) Indigenous natural enemies associated with Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Eastern Spain. Biological Control 18, 199207.CrossRefGoogle Scholar
Van der Walt, A., du Plessis, H. & Van den Berg, J. (2009) Infestation of groundnut by the groundnut leafminer, Aproaerema modicella (Deventer) (Lepidoptera: Gelechiidae) and rates of parasitization of this pest in South Africa. Crop Protection 28, 5356.CrossRefGoogle Scholar
van Lenteren, J.C. (2011) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57, 120.CrossRefGoogle Scholar
Vivan, L.M., Torres, J.B. & Veiga, A.F.S.L. (2003) Development and reproduction of a predatory stinkbug, Podisus nigrispinus, in relation to two different prey types and environmental conditions. BioControl 48, 155168.CrossRefGoogle Scholar
Walker, M. & Jones, T.H. (2001) Relative role of top-down and bottom-up forces in terrestrial tritrophic plant–insect herbivore–natural enemy systems. Oikos 93, 177187.CrossRefGoogle Scholar
Willink, E., Zaia, G., Gastaminza, G., Zamudio, M.P., Salas, H., Casmuz, A., Medina, S. & Jaldo, H. (2002) Introducción de Citrostichus phyllocnistoides para el control biológico del minador de los cítricos en el NOA. Avance Agroindustrial 23, 1719.Google Scholar
Xiao, Y. & Fadamiro, H.Y. (2010) Exclusion experiments reveal relative contributions of natural enemies to mortality of citrus leafminer, Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Alabama satsuma orchards. Biological Control 54, 189196.CrossRefGoogle Scholar
Xiao, Y., Qureshi, J.A. & Stansly, P. (2007) Contribution of predation and parasitism to mortality of citrus leafminer Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) populations in Florida. Biological Control 40, 396404.CrossRefGoogle Scholar
Zaia, G.D., Willink, E., Gastaminza, G., Salas, H., Villagrán, M.E., Augier, L. & Figueroa, D. (2006) Control biológico clásico del ‘minador de la hoja de los cítricos’: balance de lo realizado en la EEAOC. Avance Agroindustrial 27, 2934.Google Scholar
Zappalà, L. & Hoy, M.A. (2004) Reproductive strategies and parasitization behavior of Ageniaspis citricola, a parasitoid of the citrus leafminer Phyllocnistis citrella . Entomologia Experimentalis et Applicata 113, 135143.CrossRefGoogle Scholar
Zappalà, L., Hoy, M.A. & Cave, R.D. (2007) Interaction between the red imported fire ant, the citrus leafminer, and its parasitoid Ageniaspis citricola (Hymenoptera: Encyrtidae): laboratory and field evaluations. Biocontrol Science and Technology 17, 353363.CrossRefGoogle Scholar
Zhang, L.S. & Liu, T.X. (2008) Host-feeding of three parasitoid species on Bemisia tabaci biotype B and implications for whitefly biological control. Entomologia Experimentalis et Applicata 127, 5563.CrossRefGoogle Scholar
Zuccardi, R.B. & Fadda, G.S. (1985) Bosquejo agroecológico de la provincia de Tucumán. Miscelánea No 86, Argentina, Universidad Nacional de Tucumán.Google Scholar