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The invasive coconut mite Aceria guerreronis (Acari: Eriophyidae): origin and invasion sources inferred from mitochondrial (16S) and nuclear (ITS) sequences

Published online by Cambridge University Press:  09 March 2007

D. Navia
Affiliation:
Embrapa Recursos Genéticos e Biotecnologia, Caixa Postal 02372, 70.770-900 Brasília, DF, Brazil
G.J. de Moraes
Affiliation:
Departamento de Entomologia, Fitopatologia e Zoologia Agrícola, ESALQ-Universidade de São Paulo, Caixa Postal 09, 13.418-900 Piracicaba, SP, Brazil
G. Roderick
Affiliation:
Department of Environmental Sciences, Policy and Management, Division of Insect Biology, University of California, Berkeley, CA 94720-3112, USA
M. Navajas*
Affiliation:
Institut National de la Recherche Agronomique, Centre de Biologie et Gestion des Populations, Campus International de Baillarguet, CS 30016, 34988 Montferrier-sur-Lez, France
*
*Fax: +33 (0)4 99 62 33 45 E-mail: [email protected]

Abstract

Over the past 30 years the coconut mite Aceria guerreronis Keifer has emerged as one of the most important pests of coconut and has recently spread to most coconut production areas worldwide. The mite has not been recorded in the Indo-Pacific region, the area of origin of coconut, suggesting that it has infested coconut only recently. To investigate the geographical origin, ancestral host associations, and colonization history of the mite, DNA sequence data from two mitochondrial and one nuclear region were obtained from samples of 29 populations from the Americas, Africa and the Indo-ocean region. Mitochondrial DNA 16S ribosomal sequences were most diverse in Brazil, which contained six of a total of seven haplotypes. A single haplotype was shared by non-American mites. Patterns of nuclear ribosomal internal transcribed spacer (ITS) variation were similar, again with the highest nucleotide diversity found in Brazil. These results suggest an American origin of the mite and lend evidence to a previous hypothesis that the original host of the mite is a non-coconut palm. In contrast to the diversity in the Americas, all samples from Africa and Asia were identical or very similar, consistent with the hypothesis that the mite invaded these regions recently from a common source. Although the invasion routes of this mite are still only partially reconstructed, the study rules out coconut as the ancestral host of A. guerreronis, thus prompting a reassessment of efforts using quarantine and biological control to check the spread of the pest.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2005

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References

Ansaloni, T. & Perring, T.M. (2002) Biology of Aceria guerreronis Keifer on queen palms. p. 145 in Program and Abstract Book. International Congress of Acarology, 11. Universidad Nacional Autónoma de México, México.Google Scholar
Aquino, M.L.N. & Arruda, G.P. (1967) O agente causal da ‘necrose do olho do coqueiro’ em Pernambuco. 33 pp. Recife, IPA.Google Scholar
Bain, T.M. (1948) Informe de la visita praticada a algunas zonas cultivadas de cocotero en la Republica de Colombia. 18 pp. Division de Agricultura y Ganadería, Ministerio de Agricultura, Bogotá.Google Scholar
Baliraine, F., Bonizzoni, M., Osir, E.O., Lux, S.A., Mulaa, F.J., Zheng, L., Gomulski, L.M., Gasperi, G. & Malacrida, A.R. (2003) Comparative analysis of microsatellite loci in four fruit fly species of the genus Ceratitis (Diptera: Tephritidae). Bulletin of Entomological Research 93, 110CrossRefGoogle Scholar
Bandelt, H.J., Forster, P. & Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 3748CrossRefGoogle ScholarPubMed
Baudoin, L., Rao, V.R. & Batugal, P. (1998) International movement of coconut cultivars. 3440Proceedings. COGENT regional coconut genebank planning workshop 1, Serdang, IPGRI.Google Scholar
Bellotti, A.C., Smith, L. & Lapointe, S.L. (1999) Recent advances in cassava pest management. Annual Review of Entomology 44, 343370CrossRefGoogle ScholarPubMed
Ben, Ali, Z., Boursot, P., Said, K., Lagnel, J., Chatti, N. & Navajas, M. (2000) Comparison of ribosomal ITS regions among Androctonus spp. scorpions (Scorpionida/Buthidae) from Tunisia. Journal of Medical Entomology 37, 787790CrossRefGoogle Scholar
Birungi, J. & Munstermann, L.E. (2002) Genetic structure of Aedes albopictus (Diptera: Culicidae) populations based on mitochondrial ND5 sequences: evidence for an independent invasion into Brazil and United States. Genetics 95, 125132Google Scholar
Bohonak, A.J., Davies, N., Villablanca, X. & Roderick, G.K. (2001) Invasion genetics of New World medflies: testing alternative colonization scenarios. Biological Invasions 3, 103111CrossRefGoogle Scholar
Bonizzoni, M., Zheng, L., Guglielmino, C.R., Haymer, D.S., Gasperi, G., Gomulski, L.M. & Malacrida, A.R. (2001) Microsatellite analysis of medfly bioinfestations in California. Molecular Ecology 10, 25152524CrossRefGoogle ScholarPubMed
Briones, M.L. & Sill, Jr W.H. (1963) Habitat, gross morphology and geographical distribution of four new species of eriophyid mites from coconuts in the Philippines. FAO Plant Protection Bulletin 11, 2530Google Scholar
Cabral, R.V.G. & Carmona, M.M. (1969) Aceria guerreronis Keifer (Acarina: Eriophyidae), uma espécie nova para S. Tomé e Príncipe. Portugaliae Acta Biológica 10, 353358Google Scholar
Caterino, M.S., Cho, S. & Sperling, F.A.H. (2000) The current state of insect molecular systematics: a thriving tower of babel. Annual Review of Entomology 45, 154CrossRefGoogle ScholarPubMed
Crooks, J.A. & Soule, M. (1999) Lag times in population explosions of invasive species: causes and implications. pp. 103125in Sandlund, O., Schei, P., Viken, A. (Eds) Invasive species and biodiversity management. Dordrecht The Netherlands, Kluwer.CrossRefGoogle Scholar
Davies, N., Villablanca, F.X. & Roderick, G.K. (1999) Bioinvasions of the medfly Ceratitis capitata: source estimation using DNA sequences at multiple intron loci. Genetics 153, 351360CrossRefGoogle ScholarPubMed
Doreste, S.E. (1968) El ácaro de la flor del cocotero (Aceria guerreronis Keifer) en Venezuela. Agronomia Tropical 18, 370386Google Scholar
Elton, C. (1958) The ecology of invasions by animals and plants. 181 pp. London, Chapman and Hall.CrossRefGoogle Scholar
Estrada, J. & Gonzalez, M. (1975) Daños causados en coco por Aceria guerreronis (Acarina: Eriophyidae) en Cuba. Revista de la Agricultura 8, 3034Google Scholar
Fenton, B., Jones, A.T., Malloch, G. & Thomas, W.P. (1996) Molecular ecology of some Cecidophyopsis mites (Acari: Eriophyidae) on Ribes species and evidence for their natural cross colonisation of blackcurrant (R. nigrum). Annals of Applied Biology 128, 405414CrossRefGoogle Scholar
Fenton, B., Birch, A.N.E., Malloch, G., Lanham, P.G. & Brennan, R.M. (2000) Gall mite molecular phylogeny and its relationship to the evolution of plant host specificity. Experimental and Applied Acarology 24, 831861CrossRefGoogle Scholar
Fernando, L.C.P., Wickramananda, I.R. & Aratchige, N.S. (2002) Status of coconut mite, Aceria guerreronis in Sri Lanka. pp. 18in Fernando, L.C.P., Moraes, G.J. & Wickramananda, I.R. (Eds) Proceedings of the International Workshop on Coconut Mite (Aceria guerreronis), Lunuwila, 6–8 January 2000. Lunuwila, Coconut Research Institute.Google Scholar
Fimiani, P. (1989) Mediterranean region. pp. 3950in Robinson, A. & Hooper, G. (Eds) Fruit flies: their biology, natural enemies and control. Amsterdam, Elsevier Science.Google Scholar
Flechtmann, C.H.W. (1989) Cocos weddelliana H. Wendl. (Palmae: Arecaceae), a new host plant for Eriophyes guerreronis (Keifer, 1965) (Acari: Eriophyidae) in Brazil. International Journal of Acarology 15, 241CrossRefGoogle Scholar
Flechtmann, C.H.W. (1998) Mite (Arthropoda: Acari) associates of palms (Arecaceae) in Brasil. IV. Description of two new species in the family Eriophyidae. International Journal of Acarology 24, 113117CrossRefGoogle Scholar
Gasparich, G.E., Silva, J.G., Han, H.Y., McPheron, B.A., Steck, G.J. & Sheppard, W.S. (1997) Population genetic structure of Mediterranean fruit fly (Diptera: Tephritidae) and implications for world wide colonization patterns. Annals of the Entomological Society of America 90, 790797CrossRefGoogle Scholar
Gasperi, G., Bonizzoni, M., Gomulski, L.M., Murelli, V., Torti, C., Malacrida, A.R. & Guglielmino, C.R. (2002) Genetic differentiation, gene flow and the origin of infestations of the medfly, Ceratitis capitata. Genetica 116, 125135CrossRefGoogle ScholarPubMed
Gondim, Jr M.G.C., Flechtmann, C.H.W. & Moraes, G.J. (2000) Mite (Arthropoda: Acari) associates of palms (Arecaceae) in Brazil. V. Descriptions of four new species in the Eriophyoidea. Systematic and Applied Acarology 5, 99110CrossRefGoogle Scholar
Griffith, R. (1984) The problem of the coconut mite, Eriophyes guerreronis, in the coconut groves of Trinidad and Tobago. pp. 128–132 in Proceedings of the Annual Meeting of the Caribbean Food Crops Society 20, St Croix, Caribbean Food Crops Society.Google Scholar
Haq, M.A. (2001) Culture and rearing of Aceria guerreronis and its predators. Entomon 26, 34Google Scholar
Haq, M.A., Sumangala, K. & Ramani, N. (2002) Coconut mite invasion, injury and distribution. pp. 41–49 in Fernando, L.C.P., Moraes, G.J., Wickramananda, I.R. (Eds) Proceedings of the International Workshop on Coconut Mite (Aceriaguerreronis), Lunuwila, 6–8 January 2000. Lunuwila, Coconut Research Institute.Google Scholar
Harpending, H. (1994) Signature of ancient population growth in a low resolution mitochondrial DNA mismatch distribution. Heredity Human Biology 66, 591600Google Scholar
Harries, H.C. (1978) The evolution, dissemination and classification of Cocos nucifera. Botanical Review44, 265320.CrossRefGoogle Scholar
Hernández, Roque F. (1977) Combate químico del eriófido del cocotero Aceria (Eriophyes) guerreronis (K.) en la Costa de Guerrero. Agricultura Técnica en México4, 2338.Google Scholar
Howard, F.W., Abreu-Rodriguez, E. & Denmark, H.A. (1990) Geographical and seasonal distribution of the coconut mite, Aceria guerreronis (Acari: Eriophyidae), in Puerto Rico and Florida, USA. Journal of Agriculture of the University of Puerto Rico 74, 237251CrossRefGoogle Scholar
Julia, J.F. & Mariau, D. (1979) Nouvelle recherches en Côte-d'Ivoire sur Eriophyes guerreronis K., acarien ravageur des noix du cocotier. Oléagineux 34, 181187Google Scholar
Kang, S.M. (1981) Malaysian eriophyid and tarsonemid mites on coconut. FAO Plant Protection Bulletin 29, 79Google Scholar
Keifer, H.H. (1965) Eriophyid studies B-14 Sacramento California Department of Agriculture, Bureau of EntomologyGoogle Scholar
Kolbe, J.J., Glor, R.E., Schettino, L.R., Lara, A.C., Larson, A. & Losos, J.B. (2004) Genetic variation increases during biologial invasion by a Cuban lizard. Nature 431, 177181CrossRefGoogle Scholar
Lande, R. & Barrowclough, G.F. (1987) Effective population size, genetic variation, and their use in population management. pp. 87123in Soule, M.E. (Ed.) Viable populations for conservation. Cambridge, Cambridge University Press.CrossRefGoogle Scholar
Lebrun, P., Grivet, L. & Baudoin, L. (1998) Dissemination et domestication du cocotier a la lumière des marqueurs RFLP. Plantations Recherche Developpement 5, 233245Google Scholar
Lindquist, E.E., Sabelis, M.W. & Bruin, J. (1996) Eriophyoid mites: their biology, natural enemies and control. 790 pp. Amsterdam, Elsevier.Google Scholar
Mariau, D. (1969) Aceria guerreronis Keifer: récent ravageur de la cocoteraie Dahoméenne. Oléagineux 32, 101111Google Scholar
Mohanasundaram, M. (1984) New eriophyid mites from India (Acarina: Eriophyoidea). Oriental Insects 18, 251283CrossRefGoogle Scholar
Mooney, H.A. & Cleland, E.E. (2001) The evolutionary impact of invasive species. Proceedings of the National Academy of Sciences, USA 98, 54465451CrossRefGoogle ScholarPubMed
Moore, D. (1986) Bract arrangement in the coconut fruit in relation to attack by the coconut mite Eriophyes guerreronis Keifer. Tropical Agriculture 63, 285288Google Scholar
Moore, D. & Howard, F.W. (1996) Coconuts. pp. 561570in Lindquist, E.E., Sabelis, M.W.Bruin, J.Eriophyoid mites: their biology, natural enemies and control. Amsterdam, Elsevier.CrossRefGoogle Scholar
Moore, D., Alexander, L. & Hall, R.A. (1989) The coconut mite, Eriophyes guerreronis Keifer in St Lucia: yield losses and attempts to control it with acaricide, polybutene and Hirsutella fungus. Tropical Pest Management 35, 8389CrossRefGoogle Scholar
Moraes, G.J. & Zacarias, M.S. (2002) Use of predatory mites for the control of eriophyid mites. pp. 7888 in Fernando, L.C.P., Moraes, G.J., Wickramananda, I.R (Eds) Proceedings of the International Workshop on Coconut Mite (Aceriaguerreronis), Lunuwila, 6–8 January 2000. Lunuwila, Coconut Research Institute.Google Scholar
Mun, J.H., Bohonak, A.J. & Roderick, G.K. (2003) Population structure of the pumpkin fruit fly Bactrocera depressa (Tephritidae) in Korea and Japan: Pliocene allopatry or recent invasion. Molecular Ecology 12, 29412951CrossRefGoogle ScholarPubMed
Muthiah, C. & Bhaskaran, R. (2000) Major outbreak of eriophyid mite of coconut in India. Planter 76, 243246Google Scholar
Nair, C.P.R. & Koshy, P.K. (2000) Studies on coconut eriophyid mite, Aceria guerreronis Keifer in India. p. 7 in Programme of the International Workshop on Coconut Mite, (Aceriaguerreronis) 1, Lunuwilla, Coconut Research Institute.Google Scholar
Navajas, M. & Navia, D (2005) Evolutionary genetics of invasive species using molecules and morphological variation to trace the origin and dissemination of exotic pests. pp. 107112 in Symposium Proceedings, Plant Protection and Plant Health in Europe–Introduction and Spread of Invasive Species, 81. Alton, British Crop Production Council.Google Scholar
Navajas, M., Lagnel, J., Fauvel, G. & Moraes, G.J. (1999) Sequence variation of ribosomal internal transcribed spacers (ITS) in commercially important Phytoseiidae mites. Experimental and Applied Acarology 23, 851859CrossRefGoogle ScholarPubMed
Navia, D. (2004) Ácaros Eriophyoidea (Prostigmata) associados a palmeiras (Arecaceae), com ênfase no ácaro do coqueiro, Aceria guerreronis Keifer–espectro de hospedeiros e àspectos biogeográficos. Piracicaba, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo. 435 pp. Thesis (PhD) available in http://www.teses.usp.br/teses/disponiveis/11/11146/tde-02072004-142301/Google Scholar
Navia, D. & Flechtmann, C.H.W. (2002) Mite (Arthropoda: Acari) associates of palms (Arecaceae) in Brazil: VI. New genera and new species of Eriophyidae and Phytoptidae (Prostigmata: Eriophyoidea). International Journal of Acarology 28, 121146CrossRefGoogle Scholar
Nei, M. (1987) Molecular evolutionary genetics. pp. 512 1st edn. 512 New York, Columbia University Press.CrossRefGoogle Scholar
Oldfield, G.N. (1996) Diversity and host plant specificity. pp. 199–216. in Lindquist, E.E., Sabelis, M.W., Bruin, J. (Eds) Eriophyoid mites: their biology, natural enemies and control. Amsterdam, Elsevier.Google Scholar
Persley, G.J. (1992) Replanting the tree of life: towards an international agenda for coconut palm research 156 pp. Wallingford, Oxon CAB International.Google Scholar
Pimentel, D. (2000) Environmental and economic costs of nonindigenous species in the United States. BioScience 50, 5365CrossRefGoogle Scholar
Pimentel, D. (2002) Introduction: non-native species in the world. pp. 381in Pimentel, D. (Ed.) Biological invasions: economic and environmental costs of alien plant, animal, and microbe species. Boca Raton, Florida, CRC Press.Google Scholar
Pimm, S. (1996) The balance of nature? Ecological issues in the conservation of species and communities. American Scientist 84, 468Google Scholar
Purseglove, J.W. (1975) Tropical crops: monocotyledons. 607 pp. London, Longmans.Google Scholar
Ramaraju, K. & Rabindra, R.J. (2002) Palmyra, Borassus flabellifer Linn. (Palmae): a host of the coconut eriophyid mite Aceria guerreronis Keifer. Pest Management in Horticulture Ecosystems 7, 149151Google Scholar
Ramaraju, K., Natarajan, K., Sundara, P.C., Palanisamy, S. & Rabindra, R.J. (2002) Studies on coconut eriophyid mite, Aceria guerreronis Keifer in Tamil Nadu, Índia. pp. 1331in Fernando, L.C.P., Moraes, G.J., Wickramananda, I.R. (Eds) Proceedings of the International Workshop on Coconut Mite (Aceria guerreronis), Lunuwila, 6–8 January 2000. Lunuwila, Coconut Research Institute.Google Scholar
Robbs, C.F. & Peracchi, A.L. (1965) Sobre a ocorrência de um ácaro prejudicial ao coqueiro (Cocos nucifera L.). pp. 6570in Anais da Reunião Fitossanitária, 9, Rio de Janeiro, Ministério da Agricultura, SDSV.Google Scholar
Roderick, G. & Navajas, M. (2003) Genes in new environments: genetics and evolution in biological control. Nature Reviews Genetics 4, 889899CrossRefGoogle ScholarPubMed
Rogers, A. (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49, 608615CrossRefGoogle ScholarPubMed
Rogers, A. & Harpending, H. (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552569Google ScholarPubMed
Salomone, N., Emerson, B.C., Hewitt, G.M. & Bernini, F. (2002) Phylogenetic relationship among the Canary Island Steganacaridae (Acari, Oribatida) inferred from mitochondrial DNA sequence data. Molecular Ecology 11, 7989CrossRefGoogle ScholarPubMed
Santana, D.L.Q. & Flechtmann, C.H.W. (1998) Mite (Arthropoda: Acari) associates of palms (Arecaceae) in Brazil. I. Present status and new records. Revista Brasileira de Zoologia 15, 959963CrossRefGoogle Scholar
Sathiamma, B. (1981) Mite fauna associated with coconut palm in Kerala. pp. 11–14. in Channabasavanna, G.P. (Ed.) Contribution to acarology in India. Bangalore, Acarological Society of India.Google Scholar
Sathiamma, B. & Radhakrishnan, C.P.R. & Koshi, P.K. (1998) Outbreak of a nut infesting eriophyid mite, Eriophyes guerreronis (K.) in coconut plantations in India. Indian Coconut Journal 29, 13Google Scholar
Schiliesske, J. (1988) On the gall mite fauna (Acari: Eriophyoidea) of Cocos nucifera L. in Costa Rica. Nachrichtenblatt des deutschen Pflanzenschutzdienstes 40, 124127Google Scholar
Schneider, S., Roesli, D. & Excoffier, L. (2000) A software for population genetics data analysis. Geneva, University of Geneva, Genetics and Biometry Laboratory.Google Scholar
Seguni, Z. (2002) Incidence, distribution and economic importance of the coconut eriophyid mite, Aceria guerreronis Keifer in Tanzanian coconut based cropping systems. pp. 5457 in Fernando, L.C.P., Moraes, G.J. & Wickramananda, I.R. (Eds) Proceedings of the International Workshop on Coconut Mite (Aceria guerreronis), Lunuwila, 6–8 January 2000. Lunuwila, Coconut Research Institute.Google Scholar
Sembene, M.A.D. (1998) Genetic differentiation of groundnut seed-beetle populations in Senegal. Entomologia Experimentalis et Applicata 87, 171180CrossRefGoogle Scholar
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651701CrossRefGoogle Scholar
Solignac, M., Cornuet, J., Vautrin, D., Le Conte, Y., Anderson, D., Evans, J., Cros-Arteil, S. & Navajas, M. (2005) The invasive Russian and Japanese types of Varroa destructor, ectoparasite mite of the Western honey bee (Apis mellifera), are two partially isolated clones. Proceedings of the Royal Society of London B 272, 411419Google Scholar
Stepien, C.A., Taylor, C.D. & Dabrowska, K.A. (2002) Genetic variability and phylogeographical patterns of a nonindigenous species invasion: a comparison of exotic vs. native zebra and quaga mussel populations. Journal of Evolutionary Biology 15, 314328CrossRefGoogle Scholar
Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics123, 585595.CrossRefGoogle ScholarPubMed
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through weighting position-specific gap penalties and weight matrix. Nucleic Acids Research 22, 46734680CrossRefGoogle ScholarPubMed
Tsutsui, N.D., Suarez, A.V., Holway, D.A. & Case, T.J. (2000) Reduced genetic variation and the success of an invasive species. Proceedings of the National Academy of Sciences, USA 97, 59485953CrossRefGoogle ScholarPubMed
Van Driesche, R.G. & Bellows, T.S. (1996) Biological control. 539 pp. New York, Chapman and Hall.CrossRefGoogle Scholar
Vietmeyer, N.D. (1986) Lesser-known plants of potential use in agriculture and forestry. Science 232, 13791384CrossRefGoogle ScholarPubMed
Villablanca, F.X., Roderick, G.K. & Palumbi, S.R. (1998) Invasion genetics of the Mediterranean fruit fly: variation in multiple nuclear introns. Molecular Ecology 7, 547560CrossRefGoogle ScholarPubMed
Wesson, D.M. & Collins, F.H. (1992) Sequence and secondary structure of 5.8S rRNA in the tick, Ixodes scapularis. Nucleic Acids Research 20, 1139CrossRefGoogle ScholarPubMed
White, I. & Elson-Harris, M. (1992) Fruit flies of economic significance: their identification and bionomics. 600 pp. Wallingford, Oxon, CAB International.CrossRefGoogle Scholar
Wittenberg, R. & Cock, M.J.W. (2001) Invasive alien species: a toolkit of best prevention and management practices. 240 pp. Wallingford, Oxon, CAB International.CrossRefGoogle Scholar
Zuluaga, C.I. & Sánchez, P.A. (1971) La roña o escoriación de los frutos del cocotero (Cocos nucifera L.) en Colombia. Acta Agronomica 21, 133139Google Scholar