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A survey of entomopathogenic nematode species in continental Portugal

Published online by Cambridge University Press:  16 April 2013

V. Valadas
Affiliation:
NemaLab-ICAAM (Instituto de Ciências Agrárias e Ambientais Meditterrânicas) and Departamento de Biologia, Universidade de Évora, Évora, Portugal
M. Laranjo
Affiliation:
Lab. Microbiologia do Solo-ICAAM (Instituto de Ciências Agrárias e Ambientais Meditterrânicas) and Departamento de Biologia, Universidade de Évora, Évora, Portugal IIFA (Instituto de Investigação e Formação Avançada), Universidade de Évora, Évora, Portugal
M. Mota
Affiliation:
NemaLab-ICAAM (Instituto de Ciências Agrárias e Ambientais Meditterrânicas) and Departamento de Biologia, Universidade de Évora, Évora, Portugal
S. Oliveira*
Affiliation:
Lab. Microbiologia do Solo-ICAAM (Instituto de Ciências Agrárias e Ambientais Meditterrânicas) and Departamento de Biologia, Universidade de Évora, Évora, Portugal
*

Abstract

Entomopathogenic nematodes (EPN) are lethal parasites of insects, used as biocontrol agents. The objectives of this work were to survey the presence of EPN in continental Portugal and to characterize the different species. Of the 791 soil samples collected throughout continental Portugal, 53 were positive for EPN. Steinernema feltiae and Heterorhabditis bacteriophora were the two most abundant species. Analysis of EPN geographical distribution revealed an association between nematode species and vegetation type. Heterorhabditis bacteriophora was mostly found in the Alentejo region while S. feltiae was present in land occupied by agriculture with natural vegetation, broadleaved forest, mixed forest and transitional woodland-shrub, agro-forestry areas, complex cultivated patterns and non-irrigated arable land. Although no clear association was found between species and soil type, S. feltiae was typically recovered from cambisols and H. bacteriophora was more abundant in lithosols. Sequencing of the internal transcribed spacer (ITS) region indicated that S. feltiae was the most abundant species, followed by H. bacteriophora. Steinernema intermedium and S. kraussei were each isolated from one site and Steinernema sp. from two sites. Phylogenetic analyses of ITS, D2D3 expansion region of the 28S rRNA gene, as well as mitochondrial cytochrome c oxidase subunit I (COXI) and cytochrome b (cytb) genes, was performed to evaluate the genetic diversity of S. feltiae and H. bacteriophora. No significant genetic diversity was found among H. bacteriophora isolates. However, COXI seems to be the best marker to study genetic diversity of S. feltiae. This survey contributes to the understanding of EPN distribution in Europe.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2013 

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References

Adams, B.J., Peat, S.M. & Dillman, A.R. (2007) Phylogeny and evolution. pp. 693733 in Nguyen, K.B. & Hunt, D.J. (Eds) Entomopathogenic nematodes: systematics, phylogeny and bacterial symbionts. Nematology Monographs and Perspectives 5 . Leiden, The Netherlands, Brill.Google Scholar
Bedding, R.A. & Akhurst, R.J. (1975) A simple technique for the detection of insect parasitic nematodes in soil. Nematologica 21, 109110.Google Scholar
Bednarek, A. (1998) The agricultural system, as a complex factor, effects the population of entomopathogenic nematodes (Rhabditida: Steinernematidae) in the soil. IOBC Bulletin 21, 155216.Google Scholar
Boag, B., Nielson, R. & Gordon, S. (1992) Distribution and prevalence of the entomopathogenic nematode Steinernema feltiae in Scotland. Annals of Applied Biology 121, 355360.CrossRefGoogle Scholar
Boemare, N. (2002) Biology, taxonomy and systematics of Photorhabdus and Xenorhabdus . pp. 3556 in Gaugler, R. (Ed.) Entomopathogenic nematology. Wallingford, UK, CABI Publishing.CrossRefGoogle Scholar
Bruck, D.J. (2004) Natural occurrence of entomopathogens in Pacific Northwest nursery soil and their virulence to the black vine weevil, Otiorhynchus sulcatus (F.) (Coleoptera: Curculionidae). Environmental Entomology 33, 13351343.Google Scholar
Burman, M., Abrahamsson, K., Ascard, J., Sjoberg, A. & Erikson, B. (1986) Distribution of insect parasitic nematodes in Sweden. p. 312 in Samson, R.A., Vlak, J.M. & Peters, D. (Eds) Fundamentals and applied aspects of invertebrate pathology. Wageningen, The Netherlands, Foundation of the 4th International Colloquium on Invertebrate Pathology.Google Scholar
Caetano, M., Araújo, A., Nunes, A., Nunes, V. & Pereira, M. (2009) Accuracy assessment of the CORINE Land Cover 2006 map of Continental Portugal. 47 pp. Lisbon, Relatório Técnico, Instituto Geográfico Português.Google Scholar
Campos-Herrera, R., Escuer, M., Labrador, S., Robertson, L., Barrios, L. & Gutiérrez, C. (2007) Distribution of the entomopathogenic nematodes from La Rioja (Northern Spain). Journal of Invertebrate Pathology 95, 125139.Google Scholar
Campos-Herrera, R., Johnson, E.G., El-Borai, F.E., Stuart, R.J., Graham, J.H. & Duncan, L.W. (2011) Long-term stability of entomopathogenic nematode spatial patterns measured by sentinel insects and real-time PCR assays. Annals of Applied Biology 158, 5568.Google Scholar
De Doucet, M.M.A. & Gabarra, R. (1994) On the occurrence of Steinernema glasseri (Steiner, 1929) (Steinernematidae) and Heterorhabditis bacteriophora Poinar, 1976 (Heterorhabditidae) in Catalogne, Spain. Fundamental Applied Nematology 17, 441443.Google Scholar
Downes, M.J. & Griffin, C.T. (1991) Recovery of heterorhabditid nematodes from Irish and Scottish soils. pp. 216218 in Smits, P.H. (Ed.) Proceedings of the Third European Meeting Microbial Control of Pests. IOBC/WPRS Bulletin, Wageningen, The Netherlands.Google Scholar
Edgington, S., Buddie, A.G., Moore, D., France, A., Merino, L., Tymo, L.M. & Hunt, D.J. (2010) Diversity and distribution of entomopathogenic nematodes in Chile. Nematology 12, 915928.Google Scholar
Ehlers, R.U., Deseo, K.V. & Stackebrandt, E. (1991) Identification of Steinernema spp. from Italian and German soils. Nematologica 37, 360366.Google Scholar
El-Borai, F., Stuart, R.J., Campos-Herrera, R., Pathak, E. & Duncan, L.W. (2012) Entomopathogenic nematodes, root weevil larvae, and dynamic interactions among soil texture, plant growth, herbivory, and predation. Journal of Invertebrate Pathology 109, 134142.Google Scholar
Emelianoff, V., Le Brun, N., Pages, S., Stock, P., Tailliez, P., Moulia, C. & Sicard, M. (2008) Isolation and identification of entomopathogenic nematodes and their symbiotic bacteria from Herault and Gard (Southern France). Journal of Invertebrate Pathology 98, 211217.CrossRefGoogle ScholarPubMed
FAO, (2006) World reference base for soil resources 2006. A framework for international classification, correlation and communication. 145 pp. Rome, FAO.Google Scholar
Felsenstein, J. (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 34, 783791.CrossRefGoogle Scholar
García del Pino, F. (1994) Los nematodos entomopatógenos (Rhabditida: Steinernematidae y Heterorhabditidae) presentes en Cataluna y su utilizacion para el control biológico de insectos. PhD thesis, Universidad Autónoma de Barcelona, Barcelona.Google Scholar
García del Pino, F. (2005) Natural occurrence of entomopathogenic nematodes in Spain. MC-Meeting and Working Group 4th Meeting: Natural occurrence and evolution of entomopathogenic nematodes and Management Committee Meeting, Ceske Budejovice, The Czech Republic, 14–17 January.Google Scholar
García del Pino, F. & Palomo, A. (1996) Natural occurrence of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in Spanish soils. Journal of Invertebrate Pathology 68, 8490.CrossRefGoogle Scholar
Georgis, R., Koppenhöfer, A.M., Lacey, L.A., Bélair, G., Duncan, L.M., Grewal, P.S., Samish, M., Tan, L., Torr, P. & van Tol, R.W.H.M. (2006) Successes and failures in the use of parasitic nematodes for pest control. Biological Control 38, 103123.Google Scholar
Glazer, I., Liran, N. & Steinberger, Y. (1991) A survey of entomopathogenic nematodes (Rhabditida) in the Negev desert. Phytoparasitica 19, 291300.Google Scholar
Griffin, C.T., Moore, J.F. & Downes, M.J. (1991) Occurrence of insect parasitic nematodes (Steinernematidae, Heterorhabditidae) in the Republic of Ireland. Nematologica 37, 92100.Google Scholar
Gwynn, R.L. & Richardson, P.N. (1996) Incidence of entomopathogenic nematodes in soil samples collected from Scotland, England and Wales. Fundamental and Applied Nematology 19, 427431.Google Scholar
Hall, T.A. (1999) BioEdit: a user-friendly biological sequences alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Research 41, 9598.Google Scholar
Hasegawa, M., Kishino, H. & Yano, T.A. (1985) Dating of the human shape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160174.Google Scholar
Hazir, S., Keskin, N., Stock, S.P., Kaya, H. & Özcan, S. (2003) Diversity and distribution of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in Turkey. Biodiversity and Conservation 12, 375386.Google Scholar
Hominick, W.M. (2002) Biogeography. pp. 115143 in Gaugler, R. (Ed.) Entomopathogenic nematology. Wallingford, UK, CABI Publishing.Google Scholar
Hominick, W.M. & Briscoe, B.R. (1990) Occurrence of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in British soils. Parasitology 100, 295302.Google Scholar
Hominick, W.M., Reid, A.P., Bohan, D.A. & Briscoe, B.R. (1996) Entomopathogenic nematodes: biodiversity, geographical distribution and the Convention on Biological Diversity. Biocontrol Science and Technology 6, 317331.Google Scholar
Hozzank, A., Wegensteiner, R., Waitzbauer, W., Burnell, A., Mráček, Z. & Zimmermann, G. (2003) Investigations on the occurrence of entomopathogenic fungi and entomoparasitic nematodes in soils from lower Austria. Bulletin OILB/SROP 26, 7780.Google Scholar
Iraki, N., Salah, N., Sansour, M.A., Segal, D., Glazer, I., Johnigk, S.A., Hussei, M.A. & Ehlers, R.U. (2003) Isolation and characterization of two entomopathogenic nematode strains, Heterorhabditis indica (Nematoda, Rhabditida), from the West Bank, Palestinian Territories. Journal of Applied Entomology 124, 375380.Google Scholar
Ishibashi, N. (2002) Behaviour of entomopathogenic nematodes. pp. 511520 in Lee, D.L. (Ed.) The biology of nematodes. London, Taylor & Francis.Google Scholar
Ivanova, T.I., Danilov, L. & Ivakhnenko, O.A. (2000) Distribution of entomopathogenic nematodes of the families Steinernematidae and Heterorhabditidae in Russia and their morphological characteristics. Parazitologiya 34, 323334.Google Scholar
Joyce, S.A., Burnell, A.M. & Powers, T.O. (1994) Characterisation of Heterorhabditis isolates by PCR amplification of segments of mtDNA and rDNA gene. Journal of Nematology 26, 260270.Google Scholar
Kary, N.E., Niknam, G., Griffin, C.T., Mohammadi, S.A. & Moghaddam, M. (2009) A survey of entomopathogenic nematodes of the families Steinernematidae and Heterorhabditidae (Nematoda: Rhabditida) in the north-west of Iran. Nematology 11, 107116.Google Scholar
Kaya, H.K. & Gaugler, R. (1993) Entomopathogenic nematodes. Annual Review of Entomology 38, 181206.Google Scholar
Kaya, H.K. & Stock, S.P. (1997) Techniques in insect nematology. pp. 281324 in Lacey, L.A. (Ed.) Manual of techniques in insect pathology. London, Academic Press.Google Scholar
Kepenekci, I. (2002) Entomopathogenic nematodes (Rhabditida) in the Mediterranean region of Turkey. Nematologia Mediterranea 30, 1315.Google Scholar
Khatri-Chhetri, H.B., Waeyenberge, L., Spiridonov, S., Manandhar, H.K. & Moens, M. (2010) Two new species of Steinernema Travassos, 1927 with short infective juveniles from Nepal. Russian Journal of Nematology 19, 5374.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.CrossRefGoogle ScholarPubMed
Köppen, W. & Geiger, R. (1928) Klimate der Erde. Gotha, Verlag Justus Perthes (wall-map 150 cm × 200 cm).Google Scholar
Koppenhöfer, A.M. (2000) Nematodes. pp. 283301 in Lacey, L.A. & Kaya, H.K. (Eds) Field manual of techniques in invertebrate pathology. Dordrecht, The Netherlands, Kluwer.Google Scholar
Liu, J. & Berry, R.E. (1996) Steinernema oregonensis n. sp. (Rhabditida: Steinernematidae) from Oregon, USA. Fundamental and Applied Nematology 19, 375380.Google Scholar
Ma, J., Shulong, C., Zou, Y., Xiuhua, L., Richou, H., De Clercq, P. & Moean, M. (2010) Natural occurrence of entomopathogenic nematodes in North China. Russian Journal of Nematology 18, 117126.Google Scholar
Menti, H., Wright, D.J. & Perry, R.N. (1997) Desiccation survival of populations of nematodes Steinernema feltiae and Heterorhabditis megidis from Greece and the UK. Journal of Helminthology 71, 4146.Google Scholar
Midituri, J.S., Waeyenberge, L. & Moens, M. (1997) Natural distribution of entomopathogenic nematodes (Heterorhabditidae and Steinernematidae) in Belgian soils. Russian Journal of Nematology 5, 5565.Google Scholar
Mráček, Z. (1980) The use of ‘Galleria traps’ for obtaining nematode parasites of insects in Czechoslovakia (Lepidoptera: Nematoda, Steinernematidae). Acta Entomologica Bohemoslovaca 77, 378382.Google Scholar
Mráček, Z. & Becvár, S. (2000) Insect aggregations and entomopathogenic nematode occurrence. Nematology 2, 297301.Google Scholar
Mráček, Z., Bečvár, S. & Kindlmann, P. (1999) Survey of entomopathogenic nematodes from the families Steinernematidae and Heterorhabditidae (Nematoda: Rhabditida) in the Czech Republic. Folia Parasitologica 46, 145148.Google Scholar
Mráček, Z., Bečvár, S., Kindlmann, P. & Jersáková, J. (2005) Habitat preference for entomopathogenic nematodes, their insect hosts and new faunistic records for the Czech Republic. Biological Control 34, 2737.Google Scholar
Nadler, S.A., Bolotin, E. & Stock, S.P. (2006) Phylogenetic relationships of Steinernema Travassos, 1927 (Nematoda: Cephalobine: Steinernematidae) based on nuclear, mitochondrial and morphological data. Systematic Parasitology 63, 161181.CrossRefGoogle ScholarPubMed
Nguyen, K.B. & Hunt, D. (2007) Entomopathogenic nematodes: Systematics, phylogeny and bacterial symbionts. 816 pp. Leiden, E.J. Brill.Google Scholar
Nguyen, K.B., Maruniak, J. & Adams, B.J. (2001) The diagnostic and phylogenetic utility of the rDNA internal transcribed spacer sequences of Steinernema . Journal of Nematology 33, 7382.Google ScholarPubMed
Nielsen, O. & Philipsen, H. (2003) Danish surveys on insects naturally infected with entomopathogenic nematodes. Bulletin OILB/SROP 26, 131136.Google Scholar
Püza, V. & Mráček, Z. (2005) Seasonal dynamics of entomopathogenic nematodes of the genera Steinernema and Heterorhabditis as a response to abiotic factors and abundance of insect hosts. Journal of Invertebrate Pathology 89, 116122.Google Scholar
Reid, A.P., Hominick, W.M. & Briscoe, B.R. (1997) Molecular taxonomy and phylogeny of entomopathogenic nematode species (Rhabditida: Steinernematidae) by RFLP analysis of ITS region of the ribosomal DNA repeat unit. Systematic Parasitology 37, 187193.Google Scholar
Rosa, J.S. & Simões, N. (2004) Evaluation of twenty-eight strains of Heterorhabditis bacteriophora isolated in Azores for biocontrol of the armyworm, Pseudaletia unipuncta (Lepidoptera: Noctuidae). Biological Control 29, 409417.Google Scholar
Rosa, J.S., Bonifassi, E., Amaral, J., Lacey, L.A., Simões, N. & Laumond, C. (2000) Natural occurrence of entomopathogenic nematodes (Rhabditida: Steinernema, Heterorhabditis) in Azores. Journal of Nematology 32, 215222.Google Scholar
Saitou, N. & Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406425.Google Scholar
Shamseldean, M.M. & Abd-Elgawad, M.M. (1994) Natural occurrence of insect pathogenic nematodes (Rhabditida: Heterorhabditidae) in Egyptian soils. Afro-Asian Journal of Nematology 4, 151154.Google Scholar
Shishiniova, M., Budurova, L. & Gradinarov, D. (2000) Entomopathogenic nematodes from Steinernematidae and Heterorhabditidae (Nematoda: Rhabditida) in Bulgaria. Bulletin OILB/SROP 23, 7578.Google Scholar
Simões, N., Laumond, C. & Bonifassi, E. (1994) Effectiveness of Steinernema spp. and Heterorhabditis bacteriophora against Popillia japonica in Azores. Journal of Nematology 25, 480485.Google Scholar
Spiridonov, S., Krasomil-Osterfeld, K. & Moens, M. (2004) Steinernema jollieti sp. n. (Rhabditida: Steinernematidae), a new entomopathogenic nematode from the American Midwest. Russian Journal of Nematology 12, 8595.Google Scholar
Steiner, W. (1996) Distribution of entomopathogenic nematodes in the Swiss Alps. Review Suisse Zoology 103, 439452.Google Scholar
Stock, S.P. (2009) Molecular approaches and the taxonomy of insect-parasitic and pathogenic nematodes. pp. 71100 in Stock, S.P., Vandenburg, J., Glazer, I. & Boemare, N. (Eds) Insect pathogens: molecular approaches and techniques. Wallingford, Oxon, UK, CAB International Press.Google Scholar
Stock, S.P., Campbell, J.F. & Nadler, S.A. (2001) Phylogeny of Steinernema Travassos, 1927 (Cephalobina: Steinernematidae) inferred from ribosomal DNA sequences and morphological characters. Journal of Parasitology 87, 877889.Google Scholar
Stock, S.P., Al Banna, L., Darwish, R. & Katbeh, A. (2008) Diversity and distribution of entomopathogenic nematodes (Nematoda: Steinernematidae, Heterorhabditidae) and their bacterial symbionts (c-Proteobacteria: Enterobacteriaceae) in Jordan. Journal of Invertebrate Pathology 98, 228234.Google Scholar
Sturhan, D. & Liskova, M. (1999) Occurrence and distribution of entomopathogenic nematodes in the Slovak Republic. Nematology 1, 273277.Google Scholar
Sturhan, D. & Ruess, L. (1999) An undescribed Steinernema sp. (Nematoda: Steimernematidae) from Germany and the Scandinavian Subartic. Russian Journal of Nematology 7, 4347.Google Scholar
Tamura, K. (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Molecular Biology and Evolution 9, 678687.Google Scholar
Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512526.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739.Google Scholar
Tarasco, E. & Triggiani, O. (1997) Survey of Steinernema and Heterorhabditis (Rhabditida: Nematoda) in southern Italian soils. Entomologica 31, 117123.Google Scholar
Triggiani, O. & Tarasco, E. (2000) Occurrence of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in pine and oak woods in Southern Italy. Entomologica 34, 2332.Google Scholar
Valadas, V., Boyle, S., Vieira, P., Kakouli-Duarte, T. & Mota, M. (2007) First report of an entomopathogenic nematode from continental Portugal. Helminthologia 44, 226229.Google Scholar
Valadas, V., Vieira, P., Oliveira, S. & Mota, M. (2009) First report of the genus Heterorhabditis (Nematoda: Heterorhabditidae) from continental Portugal. Helminthologia 46, 4548.Google Scholar
Valadas, V., Mráček, Z., Oliveira, S. & Mota, M. (2011) Three species of entomopathogenic nematodes of the family Steinernematidae (Nematoda: Rhabditida) new to Continental Portugal. Nematologia Mediterranea 39, 169178.Google Scholar
Vänninen, I., Husberg, G.B. & Hokkanen, H.M.T. (1989) Occurrence of entomopathogenic fungi and entomoparasitic nematodes in cultivated soils in Finland. Acta Entomologica Fennica 53, 6571.Google Scholar
White, G.F. (1927) A method for obtaining infective juveniles from cultures. Science 66, 302303.Google Scholar
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