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Ophelimus mediterraneus sp. n. (Hymenoptera, Eulophidae): a new Eucalyptus gall wasp in the Mediterranean region

Published online by Cambridge University Press:  07 February 2019

N. Borowiec*
Affiliation:
UMR INRA-CNRS-Université Côte d'Azur ‘Sophia Agrobiotech Institute’, 400 Route des Chappes, 06903 Sophia Antipolis, France
J. La Salle
Affiliation:
Atlas of Living Australia, CSIRO Ecosystem Sciences, GPO Box 1700, Canberra, ACT 2601, Australia
L. Brancaccio
Affiliation:
UMR INRA-CNRS-Université Côte d'Azur ‘Sophia Agrobiotech Institute’, 400 Route des Chappes, 06903 Sophia Antipolis, France Atlas of Living Australia, CSIRO Ecosystem Sciences, GPO Box 1700, Canberra, ACT 2601, Australia Bioline Agroscience, R&D Division, 1306 route de Biot, 06560 Valbonne, France
M. Thaon
Affiliation:
UMR INRA-CNRS-Université Côte d'Azur ‘Sophia Agrobiotech Institute’, 400 Route des Chappes, 06903 Sophia Antipolis, France
S. Warot
Affiliation:
UMR INRA-CNRS-Université Côte d'Azur ‘Sophia Agrobiotech Institute’, 400 Route des Chappes, 06903 Sophia Antipolis, France
M. Branco
Affiliation:
Forest Research Center, Institute Superior of Agronomy, Technical University of Lisbon, Tapada da Ajuda 1349-017 Lisbon, Portugal
N. Ris
Affiliation:
UMR INRA-CNRS-Université Côte d'Azur ‘Sophia Agrobiotech Institute’, 400 Route des Chappes, 06903 Sophia Antipolis, France
J.-C. Malausa
Affiliation:
UMR INRA-CNRS-Université Côte d'Azur ‘Sophia Agrobiotech Institute’, 400 Route des Chappes, 06903 Sophia Antipolis, France
R. Burks
Affiliation:
University of California, Riverside, CA 92521, USA
*
*Author for correspondence Phone: (+33)4 92 38 65 00 Fax: (+33)4 92 38 64 01 E-mail: nicolas.borowiec@inra.fr

Abstract

We report here for the first time the presence of Ophelimus mediterraneus sp. n. in Mediterranean Europe. This species appears to be closely related to Ophelimus maskelli, a well-known invasive pest of Eucalyptus. Based on molecular (cytochrome oxidase I, 28S), morphological (multivariate ratio analysis) and bio-ecological investigations, our study gives unambiguous relevant criteria that allow the discrimination between these two species. A full description of O. mediterraneus sp. n. is also provided. The geographic distribution of O. mediterraneus sp. n. as well as its impact on Eucalyptus species needs to be more widely assessed since its presence may have been confused with O. maskelli in their sympatric introduced areas. Further investigations of potential parasitoids in the native area may thus be welcomed to evaluate classical biological control achievability.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2019 

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References

Al Khatib, F., Fusu, L., Cruaud, A., Gibson, G., Borowiec, N., Rasplus, J.Y., Ris, N. & Delvare, G. (2014) An integrative approach to species discrimination in the Eupelmus urozonus complex (Hymenoptera, Eupelmidae), with the description of 11 new species from the Western Palaearctic. Systematic Entomology 39, 806862.Google Scholar
Arzone, A. & Alma, A. (2000) A gall Eulophid of Eucalyptus in Italy. Informatore Fitopatologico 50, 4346.Google Scholar
Ashmead, W.H. (1900) Notes on some New Zealand and Australian parasitic Hymenoptera, with descriptions of new genera and species. Proceedings of the Linnean Society of New South Wales 25, 327360.Google Scholar
Austin, D.A., Yeates, D.K., Cassis, G., Fletcher, M.J., La Salle, J., Lawrence, J.F., McQuillan, P.B., Mound, L.A., Bickel, D.J., Gullan, P.J., Hales, D.F. & Taylor, G.S. (2004) Insects ‘Down Under’ – Diversity, endemism and evolution of the Australian insect fauna: examples from select orders. Australian Journal of Entomology 43, 216234.Google Scholar
Baur, H. & Leuenberger, C. (2011) Analysis of ratios in multivariate morphometry. Systematic Biology 60, 813825.Google Scholar
Baur, H., Kranz-Baltensperger, Y., Cruaud, A., Rasplus, J.Y., Timokhov, A.V. & Gokhman, V.E. (2014) Morphometric analysis and taxonomic revision of Anisopteromalus Ruschka (Hymenoptera: Chalcidoidea: Pteromalidae) – an integrative approach. Systematic Entomology 39, 691709.Google Scholar
Borowiec, N., Thaon, M., Brancaccio, L., Warot, S., Ris, N. & Malausa, J.C. (2012) L'eucalyptus menacé par une nouvelle espèce d’Ophelimus en France. Phytoma 656, 4244.Google Scholar
Borowiec, N., Brancaccio, L., Thaon, M., Warot, S., Branco, M., La Salle, J., Ris, N. & Malausa, J.C. (2013) Gall wasps in France and neighbouring countries: a new Ophelimus (Hymenoptera, Eulophidae) threatens Eucalyptus plantations. p. 54 in Proceedings of the 6th International Symposium on the Biology and Ecology of Gall Inducing Arthropods, Lamington National Park 4–8 August 2013, Australia.Google Scholar
Borrajo, P., Lopez, M.A., Ocete, R., Lopez, G. & Ruiz, F. (2008) First report of Closterocerus chamaeleon Girault (Hymenoptera, Eulophidae), parasitoid of Ophelimus maskelli Ashmead (Hymenoptera, Eulophidae) in Huelva (SW Spain). Boletin de Sanidad Vegetal Plagas 34, 383385.Google Scholar
Bouček, Z. (1988) Australasian Chalcidoidea (Hymenoptera). A biosystematics revision of genera of fourteen families, with a reclassification of species. Wallingford, UK, CAB International.Google Scholar
Branco, M., Boavida, C., Durand, N., Franco, J.C. & Mendel, Z. (2009) Presence of the Eucalyptus gall wasp Ophelimus maskelli and its parasitoid Closterocerus chamaeleon in Portugal: first record, geographic distribution and host preference. Phytoparasitica 37, 5154.Google Scholar
Branco, M., Dhahri, S., Santos, M. & Ben Jamaa, M.L. (2014) Biological control reduces herbivore's host range. Biological Control 69, 5964.Google Scholar
Burks, R.A., Heraty, J.M., Gebiola, M. & Hansson, C. (2011) Combined molecular and morphological phylogeny of Eulophidae (Hymenoptera: Chalcidoidea), with focus on the subfamily Entedoninae. Cladistics 27, 125.Google Scholar
Burks, R.A., Mottern, J.L., Waterworth, R. & Paine, T.D. (2015 a) First report of the Eucalyptus gall wasp, Ophelimus maskelli (Hymenoptera: Eulophidae), an invasive pest on Eucalyptus, from the Western Hemisphere. Zootaxa 3926, 448450.Google Scholar
Burks, R.A., Mottern, J.L., Pownall, N.G., Waterworth, R. & Paine, T.D. (2015 b) First record of Closterocerus chamaeleon, parasitoid of the Eucalyptus gall wasp Ophelimus maskelli (Hymenoptera, Chalcidoidea, Eulophidae), in the New World. Zookeys 504, 149152.Google Scholar
Caleca, V. (2010) First record in Algeria of two Eulophid wasps: Closterocerus chamaeleon (Girault) and its host, the Eucalyptus gall wasp Ophelimus maskelli (Ashmead) (Hymenoptera Eulophidae). Naturalista Siciliano 34, 201206.Google Scholar
Caleca, V., Lo Verde, G., Rizzo, M.C. & Rizzo, R. (2011) Dispersal rate and parasitism by Closterocerus chamaeleon (Girault) after its release in Sicily to control Ophelimus maskelli (Ashmead) (Hymenoptera, Eulophidae). Biological Control 57, 6673.Google Scholar
Colautti, R.I., Ricciardi, A., Grigorovich, I.A. & Maclsaac, H.J. (2004) Is invasion success explained by the enemy release hypothesis? Ecology Letters 7, 721733.Google Scholar
Cruaud, A., Jabbour-Zahab, R., Genson, G., Cruaud, C., Couloux, A., Kjellberg, F., van Noort, S. & Raspus, J.Y. (2010) Laying the foundations for a new classification of Agaonidae (Hymenoptera: Chalcidoidea), a multilocus phylogenetic approach. Cladistics 26, 359387.Google Scholar
Csoka, G., Stone, G.N. & Melika, G. (2005) Biology, ecology and evolution of gall-inducing Cynipidae. pp. 573642 in Raman, A., Schaefer, C.W. & Withers, T.M. (Eds) Biology, Ecology and Evolution of Gall-Inducing Arthropods. Vol. 2. Enfield, Science Publishers.Google Scholar
Dhahri, S., Ben Jamaa, M.L. & Lo Verde, G. (2010) First record of Leptocybe invasa and Ophelimus maskelli Eucalyptus gall wasps in Tunisia. Tunisian Journal of Plant Protection 5, 229234.Google Scholar
Doğanlar, M. & Mendel, Z. (2007) First record of the Eucalyptus gall wasp Ophelimus maskelli and its parasitoid, Closterocerus chamaeleon, in Turkey. Phytoparasitica 35, 333335.Google Scholar
Doughty, R.W. (2000) The Eucalypts: A Natural and Commercial History of the gum Tree. Baltimore, MD, USA, John Hopkins University Press.Google Scholar
Eilenberg, J., Hajek, A. & Lomer, C. (2001) Suggestions for unifying the terminology in biological control. BioControl 46, 387400.Google Scholar
European Plant Protection Organization (2006) First report of two new Eucalyptus pests in the South of France. Ophelimus maskelli and Leptocybe invasa. EPPO Reporting Service 189, p. 9.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google Scholar
Fusu, L. (2017) An integrative taxonomic study of European Eupelmus (macroneura) (Hymenoptera: Chalcidoidea: Eupelmidae), with a molecular and cytogenetic analysis of Eupelmus (macroneura) vesicularis: several species hiding under one name for 240 years. Zoological Journal of the Linnean Society 181, 519603.Google Scholar
Garcia, A., Goncalves, H., Borowiec, N., Franco, J.C. & Branco, M. (submitted) Ophelimus sp., a new invasive gall wasp of Eucalyptus globulus in Europe, escapes the parasitism by Closterocerus chamaeleon due to an asynchronous life cycle. Biological Control. doi: 10.1016/j.biocontrol.2018.12.006.Google Scholar
Gebiola, M., Monti, M.M., Johnson, R.C., Wooley, J.B., Hunter, M.S., Giorgini, M. & Pedata, P.A. (2017) A revision of the Encarsia pergandiella species complex (Hymenoptera: Aphelinidae) shows cryptic diversity in parasitoids of whitefly pests. Systematic Entomology 42, 3159.Google Scholar
Gibson, G.A.P., Huber, J.T. & Woolley, J.B. (1997) Annotated keys to the genera of Nearctic Chalcidoidea (Hymenoptera). Ottawa, NRC Research Press.Google Scholar
Gillespie, J.J., Munro, J.B., Heraty, J.M., Yoder, M.J., Owen, A.K. & Carmichael, A.E. (2005) A secondary structural model of the 28S rRNA expansion segments D2 and D3 for chalcidoid wasps (Hymenoptera: Chalcidoidea). Molecular Biology and Evolution 22, 15931608.Google Scholar
Girault, A.A. (1913 a) Some new genera and species of Chalcidoid Hymenoptera of the family Eulophidae from Australia. Journal of Entomology and Zoology 5, 103112.Google Scholar
Girault, A.A. (1913 b) Some chalcidoid Hymenoptera from North Queensland. Archiv für Naturgeschichte 79, 7090.Google Scholar
Girault, A.A. (1913 c) Australian hymenoptera Chalcidoidea IV. The family Eulophidae with descriptions of new genera and species. Memoirs Queensland Museum 2, 140296.Google Scholar
Girault, A.A. (1915) Australian hymenoptera Chalcidoidea IV – Supplement. Memoirs Queensland Museum 3, 180299.Google Scholar
Girault, A.A. (1925) Notes and descriptions of Australian chalcid flies – III (Hymenoptera). Insecutor Inscit. Menstr. 13, 91100.Google Scholar
Gordon, D.R., Flory, S.L., Cooper, A.L. & Morris, S.K. (2012) Assessing the invasion risk of Eucalyptus in the United States using the Australian weed risk assessment. International Journal of Forestry Research, 10.1155/2012/203768.Google Scholar
Haliday, A.H. (1844) Contributions toward the classification of the Chalcididae. Transations of the Royal Entomological Society of London 3, 295301.Google Scholar
Hurley, B.P., Garnas, J., Wingfield, M.J., Branco, M., Richardson, D.M. & Slippers, B. (2016) Increasing numbers and intercontinental spread of invasive insects on eucalypts. Biological Invasions 18, 921933.Google Scholar
Iglesias Trabado, G. & Wilstermann, D. (2008) Eucalyptus universalis. Global cultivated eucalypt forests map 2008, in GIT Forestry Consulting's Eucalyptologics: Information resources on Eucalyptus cultivation worldwide. Available at http://www.git-forestry-blog.blogspot.com (last access 2018-07).Google Scholar
Kavallieratos, N.G., Kontomidas, D.C., Anagnou-Veroniki, M. & Emmanuel, N.G. (2006) First record of the gall inducing insect Ophelimus eucalypti (Gahan) (Hymenoptera: Chalcidoidea: Eulophidae) in Greece. Annals of the Benaki Phytopatology Institute, 20, 125128.Google Scholar
Kenis, M. & Branco, M. (2010) Impact of alien terrestrial arthropods in Europe. BioRisk 4, 5171.Google Scholar
Kenis, M., Auger-Rozenberg, M.A., Roques, A., Timms, L., Péré, C., Cock, M.J.W., Settele, J., Augustin, S. & Lopez-Vaamonde, C. (2009) Ecological effects of invasive alien insects. Biological Invasions 11, 2145.Google Scholar
Kim, I.K. & La Salle, J. (2008) A new genus and species of Tetrastichinae (Hymenoptera: Eulophidae) inducing galls in seed capsules of Eucalyptus. Zootaxa 1745, 6368.Google Scholar
Kim, I.K., McDonald, M. & La Salle, J. (2005) Moona, a new genus of tetrastichine gall inducers (Hymenoptera: Eulophidae) on seeds of Corymbia (myrtaceae) in Australia. Zootaxa 989, 110.Google Scholar
Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.Google Scholar
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.Google Scholar
Ladiges, P.Y., Udovicic, F. & Nelson, G. (2003) Australian biogeographical connections and the phylogeny of large general in the plant family Myrtaceae. Journal of Biogeography 30, 989998.Google Scholar
La Salle, J. (2005) Biology of gall inducers and evolution of gall induction in Chalcidoidea (Hymenoptera: Eulophidae, Eurytomidae, Pteromalidae, Tanaostigmatidae, Torymidae). pp. 503533 in Raman, A., Schaefer, C.W. & Withers, T.M. (Eds) Biology, Ecology and Evolution of Gall-Inducing Arthropods. Vol. 2, Enfield, Science Publishers.Google Scholar
La Salle, J., Arakelian, G., Garrison, R.W. & Gates, M.W. (2009) A new species of invasive gall wasp (Hymenoptera: Eulophidae: Tetrastichinae) on blue gum (Eucalyptus globulus) in California. Zootaxa 2121, 3543.Google Scholar
Laszlo, Z., Baur, H. & Tothmeresz, B. (2013) Multivariate ratio analysis reveals Trigonoderus pedicellaris Thomson (Hymenoptera, Chalcidoidea, Pteromalidae) as a valid species. Systematic Entomology 38, 753762.Google Scholar
Lawson, S., Griffiths, M., Nahrung, H., Noack, A., Wingfield, M., Wilcken, C., Slippers, B., Lo, N., Thu, P.Q., Lee, S.S., Lelana, N.E., Ketphanh, S., Zhou, X. & Eungwijarnpanya, S. (2012) Biological control of eucalypt pests overseas and in Australia. ACIAR final report number FR2012-26. Australian Centre for International Agricultural Research. Available at https://www.aciar.gov.au/node/10901 (last access 2018-07).Google Scholar
Leica Microsystems GmbH. Microscope software platform – Leica Application Suite. Available at https://www.leica-microsystems.com/products/microscope-software/details/product/leica-application-suite/ (last access 2018 07).Google Scholar
Lo Verde, G., Dhahri, S. & Ben Jamaa, M.L. (2010) First record in Tunisia of Closterocerus chamaeleon (Girault) parasitoid of the Eucalyptus gall wasp Ophelimus maskelli (Ashmead) (Hymenoptera Eulophidae). Naturalista Siciliano 24, 207210.Google Scholar
Majer, J.D., Recher, H.F., Wellington, A.B., Woinarski, J.C.Z. & Yen, A.L. (1997) Invertebrates of eucalypt formations. pp. 278302 in Williams, J.E. & Woinarski, J.C.Z. (Eds) Eucalypt Ecology: Individuals to Ecosystems. Cambridge, Cambridge University Press.Google Scholar
Mendel, Z., Protasov, A., Fisher, N. & La Salle, J. (2004) Taxonomy and biology of Leptocybe invasa gen. & sp. n. (Hymenoptera: Eulophidae), an invasive gall inducer on Eucalyptus. Australian Journal of Entomology 43, 101113.Google Scholar
Mendel, Z., Protasov, A., Saphir, N., Brand, D., Assale, F., Blumberg, D. & La Salle, J. (2005) Insect plant interactions of two invasive Eucalyptus gall inducers, Leptocybe invasa Fisher & LaSalle and Ophelimus maskelli (Ashmead) (Hymenoptera: Eulophidae), and management possibilities. pp. 1721 in Bento, A., Miranda-Arabolaza, M.J. & Pereira, J.A. (Eds) IV Congreso Nacional de Entomologia Aplicada. Braganca, Portugal, Instituto Politecnico de Braganca.Google Scholar
Mendel, Z., Protasov, A., Blumberg, D., Brand, D., Saphir, N., Madar, Z. & La Salle, J. (2007) Release and recovery of parasitoids of the Eucalyptus gall wasp Ophelimus maskelli in Israel. Phytoparasitica 35, 330332.Google Scholar
Mendel, Z., Protasov, A., La Salle, J., Blumberg, D., Brand, D. & Branco, M. (2017) Classical biological control of two Eucalyptus gall wasps; main outcome and conclusions. Biological Control 105, 6678.Google Scholar
Mifsud, D. (2012) Leptocybe invasa Fisher & LaSalle, 2004 and Ophelimus maskelli Haliday, 1844 – two new records of gall forming Eulophidae from Malta (Hymenoptera, Chalcidoidea). Bulletin of the Entomological Society of Malta 5, 189193.Google Scholar
Noyes, J.S. (2002) Interactive Catalogue of World Chalcidoidea. Lexington, KY, Taxapad, Scientific Names for Information Management (CD-ROM).Google Scholar
Noyes, J.S. (2018) Universal Chalcidoidea Database. The Natural History Museum. Available at http://www.nhm.ac.uk/research-curation/projects/chalcidoids/ (last access 2018-07).Google Scholar
Paine, T.D., Steinbauer, M.J. & Lawson, S.A. (2011) Native and exotic pests of Eucalyptus: a worldwide perspective. Annual Review of Entomology 56, 181201.Google Scholar
Potts, B.M., Vaillancourt, R.E., Jordan, G., Dutkowski, G., Da Costa e Silva, J., McKinnon, G., Steane, D., Volker, P., Lopez, G., Apiolaza, L., Li, Y., Marques, C. & Borralho, N. (2004) Exploration of the Eucalyptus globulus gene pool. in Borralho, N., Pereira, J.S., Marques, C., Coutinho, J., Madeira, M. & Tomé, M. (Eds) Proceedings of the International IUFRO Conference, 11–15 October 2004, Aveiro, Portugal. Instituto de Investigacao da Floresta e Papel.Google Scholar
Protasov, A., Blumberg, D., Brand, D., La Salle, J. & Mendel, Z. (2007 a) Biological control of the Eucalyptus gall wasp Ophelimus maskelli (Ashmead): Taxonomy and biology of the parasitoid species Closterocerus chamaeleon (Girault), with information on its establishment in Israel. Biological Control 42, 196206.Google Scholar
Protasov, A., La Salle, J., Blumberg, D., Brand, D., Saphir, N., Assael, F., Fisher, N. & Mendel, Z. (2007 b) Biology, revised taxonomy and impact on host plants of Ophelimus maskelli, an invasive gall inducer on Eucalyptus spp. in the Mediterranean area. Phytoparasitica 35, 5076.Google Scholar
Pujade-Villar, J. & Riba-Flinch, J.M. (2004) Two Australian eulophids, very harmful to Eucalyptus spp., introduced into the northeast of the Iberian Peninsula (Hymenoptera: Eulophidae). Boletin of the Sociedad Entomologica Aragonesa 35, 299301.Google Scholar
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/.Google Scholar
Rosen, D. & DeBach, P. (1973) Systematics, morphology and biological control. Entomophaga 18, 215222.Google Scholar
Schauff, M.E. & Garrison, R. (2000) An introduced species of Epichrysocharis (hymenoptera: Eulophidae) producing galls on Eucalyptus in California with notes on the described species and placement of the genus. Journal of Hymenoptera Research 9, 176181.Google Scholar
Simberloff, D. (2009) We can eliminate invasions of live with them. Successful management projects. Biological Invasions 11, 149157.Google Scholar
Tilbury, C. & Jukes, M. (2006) Ophelimus? maskelli: a new gall-causing eulophid wasp (Hymenoptera: Chalcidoidea) on Eucalyptus in London. Cecidology 21, 9091.Google Scholar
Torchin, M.E., Lafferty, K.D., Dobson, A.P., McKenzie, V.J. & Kuris, A.M. (2003) Introduced species and their missing parasites. Nature 421, 628630.Google Scholar
Withers, M. (2001) Colonization of eucalypts in New Zealand by Australian insects. Austral Ecology 26, 467476.Google Scholar
Withers, T.M., Raman, A. & Berry, J.A. (2000) Host range and biology of Ophelimus eucalypti (Gahan) (Hym.: Eulophidae), a pest of New Zealand eucalypts. New Zealand Plant Protection 53, 339344.Google Scholar
Yukawa, J. & Rohfritsch, O. (2005) Biology and ecology of gall-inducing Cecidomyiidae (Diptera). pp. 273304 in Raman, A., Schaefer, C.W. & Withers, T.M. (Eds) Biology, Ecology and Evolution of Gall-Inducing Arthropods. Vol. 1. Enfield, Science Publishers.Google Scholar
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