Molecular phylogenetic analysis and comparative morphology resolve two new species of olive-tree soil related dagger nematodes of the genus Xiphinema (Dorylaimida : Longidoridae) from Spain
Antonio Archidona-Yuste A , Juan A. Navas-Cortés A , Carolina Cantalapiedra-Navarrete A , Juan E. Palomares-Rius A and Pablo Castillo A BA Institute for Sustainable Agriculture (IAS), Spanish National Research Council (CSIC), Campus de Excelencia Internacional Agroalimentario, ceiA3, Avda. Menéndez Pidal s/n, 14004 Córdoba, Spain.
B Corresponding author. Email: p.castillo@csic.es
Invertebrate Systematics 30(6) 547-565 https://doi.org/10.1071/IS16002
Submitted: 5 January 2016 Accepted: 19 April 2016 Published: 13 December 2016
Abstract
The genus Xiphinema constitutes a large group of ~275 species of polyphagous, plant-ectoparasitic nematodes that are distributed almost worldwide. Some species affect agricultural crops by feeding directly on root cells as well as by transmitting nepoviruses. Despite their agricultural importance, species discrimination in Xiphinema is difficult, leading to potential misidentification. Integrative taxonomy, based on the combination of molecular analyses and morphology, constitutes a new insight into Xiphinema species identification. In this study we describe two new species of Xiphinema from the Iberian Peninsula (X. macrodora, sp. nov. and X. oleae, sp. nov.) associated with cultivated and wild olive trees. Both species have specific rRNA sequences. Morphologically, Xiphinema macrodora, sp. nov. is characterised by a very long body (7.2–8.7 mm), a very long odontostyle and odontophore (190–206 and 105–120 µm, respectively), and a well developed pseudo-Z-organ, comprising 8 to 12 sclerotised bodies. Xiphinema oleae, sp. nov. is characterised by an odontostyle and an odontophore 136–149 and 65–80 µm long, respectively, and a well developed Z-organ with refractive inclusions (3–5), variable in shape. Additionally, X. macrodora, sp. nov. has the longest body size, and the longest odontostyle and odontophore of any Xiphinema, whereas X. oleae, sp. nov. is the first species with a well developed Z-organ from the Iberian Peninsula.
http://zoobank.org/urn:lsid:zoobank.org:pub:E4CE8711-22EF-40E4-9D39-6FE962F25225
Additional keywords: Bayesian inference, D2–D3 rRNA, integrative taxonomy, ITS1.
References
Archidona-Yuste, A., Navas-Cortés, J. A., Cantalapiedra-Navarrete, C., Palomares-Rius, J. E., and Castillo, P. (2016a). Cryptic diversity and species delimitation in the Xiphinema americanum-group complex (Nematoda: Longidoridae) as inferred from morphometrics and molecular markers. Zoological Journal of the Linnean Society 176, 231–265.| Cryptic diversity and species delimitation in the Xiphinema americanum-group complex (Nematoda: Longidoridae) as inferred from morphometrics and molecular markers.Crossref | GoogleScholarGoogle Scholar |
Archidona-Yuste, A., Navas-Cortés, J. A., Cantalapiedra-Navarrete, C., Palomares-Rius, J. E., and Castillo, P. (2016b). Unravelling the biodiversity and molecular phylogeny of needle nematodes of the genus Longidorus (Nematoda: Longidoridae) in olive and a description of six new species. PLoS One 11, e0147689.
| Unravelling the biodiversity and molecular phylogeny of needle nematodes of the genus Longidorus (Nematoda: Longidoridae) in olive and a description of six new species.Crossref | GoogleScholarGoogle Scholar |
Barsi, L., and De Luca, F. (2008). Morphological and molecular characterisation of two putative Xiphinema americanum-group species, X. parasimile and X. simile (Nematoda: Dorylaimida) from Serbia. Nematology 10, 15–25.
| Morphological and molecular characterisation of two putative Xiphinema americanum-group species, X. parasimile and X. simile (Nematoda: Dorylaimida) from Serbia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVeqtbs%3D&md5=b1e61fe44ffc8db0c48ffc34a1e199cfCAS |
Blaxter, M. L., De Ley, P., Garey, J. R., Liu, L. X., Scheldeman, P., Vierstraete, A., Vanfleteren, J. R., Mackey, L. Y., Dorris, M., Frisse, L. M., Vida, J. T., and Thomas, W. K. (1998). A molecular evolutionary framework for the Phylum Nematoda. Nature 392, 71–75.
| A molecular evolutionary framework for the Phylum Nematoda.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhvVOgtb4%3D&md5=84c5582ec6740ae4004ce896f624e2e4CAS |
Bongers, T., and Bongers, M. (1998). Functional diversity of nematodes. Applied Soil Ecology 10, 239–251.
| Functional diversity of nematodes.Crossref | GoogleScholarGoogle Scholar |
Boucher, G., and Lambshead, P. J. D. (1995). Ecological biodiversity of marine nematodes in samples from temperate, tropical, and deep sea regions. Conservation Biology 9, 1594–1604.
| Ecological biodiversity of marine nematodes in samples from temperate, tropical, and deep sea regions.Crossref | GoogleScholarGoogle Scholar |
Bravo, M. A., and Roca, F. (1995). Xiphinema cadavalense sp. n. (Nemata: Longidoridae) from Portugal. Fundamental and Applied Nematology 18, 17–20.
Cantalapiedra-Navarrete, C., Navas-Cortés, J. A., Liébanas, G., Vovlas, N., Subbotin, S. A., Palomares-Rius, J. E., and Castillo, P. (2013). Comparative molecular and morphological characterisations in the genus Rotylenchus: Rotylenchus paravitis n. sp., an example of cryptic speciation. Zoologischer Anzeiger 252, 246–268.
| Comparative molecular and morphological characterisations in the genus Rotylenchus: Rotylenchus paravitis n. sp., an example of cryptic speciation.Crossref | GoogleScholarGoogle Scholar |
Castillo, P., Vovlas, N., Subbotin, S., and Troccoli, A. (2003). A new root-knot nematode, Meloidogyne baetica n. sp. (Nematoda: Heteroderidae), parasitizing wild olive in southern Spain. Phytopathology 93, 1093–1102.
| A new root-knot nematode, Meloidogyne baetica n. sp. (Nematoda: Heteroderidae), parasitizing wild olive in southern Spain.Crossref | GoogleScholarGoogle Scholar |
Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.
| Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVSgt7g%3D&md5=7270e7b94b46ec4a30ad5328609b8552CAS |
Cherry, T., Szalanski, A. L., Todd, T. C., and Powers, T. O. (1997). The internal transcribed spacer region of Belonolaimus (Nemata: Belonolaimidae). Journal of Nematology 29, 23–29.
| 1:CAS:528:DyaK1cXksFOjsLg%3D&md5=cd2fdd7da0b5818371b19cb8503f0306CAS |
Coolen, W. A. (1979). Methods for extraction of Meloidogyne spp. and other nematodes from roots and soil. In ‘Root-knot Nematodes (Meloidogyne species). Systematics, Biology, and Control’. (Eds F. Lamberti and C. E. Taylor.) pp. 317–329. (Academic Press: London.)
Coomans, A. (1996). Phylogeny of the Longidoridae. Russian Journal of Nematology 4, 51–60.
Coomans, A. (2000). Nematode systematics: past, present and future. Nematology 2, 3–7.
| Nematode systematics: past, present and future.Crossref | GoogleScholarGoogle Scholar |
Coomans, A., Huys, R., Heyns, J., and Luc, M. (2001). Character analysis, phylogeny, and biogeography of the genus Xiphinema Cobb, 1973 (Nematoda, Longidoridae). Vol. 287, Annales du Musée Royal de l’Afrique Centrale (Zoologie), Tervuren, Belgique.
Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
| jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=b326576d8549dc5561e70b14d1339c77CAS |
De Luca, F., Archidona-Yuste, A., Troccoli, A., Fanelli, E., Vovlas, N., Trisciuzzi, N., and Castillo, P. (2014). Redescription and molecular characterisation of Xiphinema barense Lamberti et al., 1986 (Nematoda: Longidoridae) from wild olive trees in southern Italy. Nematology 16, 1079–1089.
| Redescription and molecular characterisation of Xiphinema barense Lamberti et al., 1986 (Nematoda: Longidoridae) from wild olive trees in southern Italy.Crossref | GoogleScholarGoogle Scholar |
Decraemer, W., and Robbins, R. T. (2007). The who, what and where of Longidoridae and Trichodoridae. Journal of Nematology 39, 295–297.
Decraemer, W., Palomares-Rius, J. E., Cantalapiedra-Navarrete, C., Landa, B. B., Duarte, I., Almeida, T., Vovlas, N., and Castillo, P. (2013). Seven new species of Trichodorus (Diphtherophorina, Trichodoridae) from Spain, an apparent centre of speciation. Nematology 15, 57–100.
| Seven new species of Trichodorus (Diphtherophorina, Trichodoridae) from Spain, an apparent centre of speciation.Crossref | GoogleScholarGoogle Scholar |
Ferris, H., Bongers, T., and Goedec, R. G. M. (2001). A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Applied Soil Ecology 18, 13–29.
| A framework for soil food web diagnostics: extension of the nematode faunal analysis concept.Crossref | GoogleScholarGoogle Scholar |
Flegg, J. J. M. (1967). Extraction of Xiphinema and Longidorus species from soil by a modification of Cobb’s decanting and sieving technique. Annals of Applied Biology 60, 429–437.
| Extraction of Xiphinema and Longidorus species from soil by a modification of Cobb’s decanting and sieving technique.Crossref | GoogleScholarGoogle Scholar |
Geraert, E. (1968). Morphometric relations in nematodes. Nematologica 14, 171–183.
| Morphometric relations in nematodes.Crossref | GoogleScholarGoogle Scholar |
Gutiérrez-Gutiérrez, C., Palomares-Rius, J. E., Cantalapiedra-Navarrete, C., Landa, B. B., Esmenjaud, D., and Castillo, P. (2010). Molecular analysis and comparative morphology to resolve a complex of cryptic Xiphinema species. Zoologica Scripta 39, 483–498.
| Molecular analysis and comparative morphology to resolve a complex of cryptic Xiphinema species.Crossref | GoogleScholarGoogle Scholar |
Gutiérrez-Gutiérrez, C., Palomares-Rius, J., Cantalapiedra-Navarrete, C., Landa, B. B., and Castillo, P. (2011). Prevalence, polyphasic identification, and molecular phylogeny of dagger and needle nematodes infesting vineyards in southern Spain. European Journal of Plant Pathology 129, 427–453.
| Prevalence, polyphasic identification, and molecular phylogeny of dagger and needle nematodes infesting vineyards in southern Spain.Crossref | GoogleScholarGoogle Scholar |
Gutiérrez-Gutiérrez, C., Cantalapiedra-Navarrete, C., Decraemer, W., Vovlas, N., Prior, T., Palomares-Rius, J. E., and Castillo, P. (2012). Phylogeny, diversity, and species delimitation in some species of the Xiphinema americanum-group complex (Nematoda: Longidoridae), as inferred from nuclear and mitochondrial DNA sequences and morphology. European Journal of Plant Pathology 134, 561–597.
| Phylogeny, diversity, and species delimitation in some species of the Xiphinema americanum-group complex (Nematoda: Longidoridae), as inferred from nuclear and mitochondrial DNA sequences and morphology.Crossref | GoogleScholarGoogle Scholar |
Gutiérrez-Gutiérrez, C., Cantalapiedra-Navarrete, C., Montes Borrego, M., Palomares-Rius, J. E., and Castillo, P. (2013a). Molecular phylogeny of the nematode genus Longidorus (Nematoda: Longidoridae) with description of three new species. Zoological Journal of the Linnean Society 167, 473–500.
| Molecular phylogeny of the nematode genus Longidorus (Nematoda: Longidoridae) with description of three new species.Crossref | GoogleScholarGoogle Scholar |
Gutiérrez-Gutiérrez, C., Cantalapiedra-Navarrete, C., Remesal, E., Palomares-Rius, J. E., Navas-Cortés, J. A., and Castillo, P. (2013b). New insight into the identification and molecular phylogeny of dagger nematodes of the genus Xiphinema (Nematoda: Longidoridae) with description of two new species. Zoological Journal of the Linnean Society 169, 548–579.
| New insight into the identification and molecular phylogeny of dagger nematodes of the genus Xiphinema (Nematoda: Longidoridae) with description of two new species.Crossref | GoogleScholarGoogle Scholar |
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
| 1:CAS:528:DC%2BD3cXhtVyjs7Y%3D&md5=a7029faf93326ae9b57891e1e59a49afCAS |
He, Y., Subbotin, S. A., Rubtsova, T. V., Lamberti, F., Brown, D. J. F., and Moens, M. (2005). A molecular phylogenetic approach to Longidoridae (Nematoda: Dorylaimida). Nematology 7, 111–124.
| A molecular phylogenetic approach to Longidoridae (Nematoda: Dorylaimida).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnvFyhsr4%3D&md5=8f529bb58b8ffac5c43ed15f2f14cb96CAS |
Holterman, M., Van Der Wurff, A., Van Den Elsen, S., Van Megen, H., Bongers, T., Holovachov, O., Bakker, J., and Helder, J. (2006). Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Phylogenetics and Evolution 23, 1792–1800.
| 1:CAS:528:DC%2BD28XovVWhurw%3D&md5=a2c56f980f90947b1350b3252b7c1728CAS |
Hugot, J. P., Baujard, P., and Morand, S. (2001). Biodiversity in helminths and nematodes as a field of study: an overview. Nematology 3, 199–208.
| Biodiversity in helminths and nematodes as a field of study: an overview.Crossref | GoogleScholarGoogle Scholar |
Jairajpuri, M. S., and Ahmad, W. (1992). ‘Dorylaimida. Freeliving, Predaceous and Plant-parasitic Nematodes.’ (Oxford & IBH Publishing Co: New Delhi.)
Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment 542 software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
| MAFFT multiple sequence alignment 542 software version 7: improvements in performance and usability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFWisLc%3D&md5=367c17fe8bfe9a8b8cd9ac1c424a7903CAS |
Lamberti, F., Molinari, S., Moens, M., and Brown, D. J. F. (2000). The Xiphinema americanum group. I. Putative species, their geographical occurrence and distribution, and regional polytomous identification keys for the group. Russian Journal of Nematology 8, 65–84.
Lambshead, P. J. D. (1993). Recent developments in marine benthic biodiversity research. Oceanics 6, 5–24.
Lazarova, S. S., Malloch, G., Oliveira, C. M. G., Hübschen, J., and Neilson, R. (2006). Ribosomal and mitochondrial DNA analyses of Xiphinema americanum-group populations. Journal of Nematology 38, 404–410.
| 1:CAS:528:DC%2BD2sXjvFKqt7s%3D&md5=e1057e4bc4b511ac56096b8a4e656084CAS |
Loof, P. A. A., and Coomans, A. (1972). The oesophageal gland nuclei of Longidoridae (Dorylaimida). Nematologica 18, 213–233.
| The oesophageal gland nuclei of Longidoridae (Dorylaimida).Crossref | GoogleScholarGoogle Scholar |
Loof, P. A. A., and Luc, M. (1990). A revised polytomous key for the identification of species of the genus Xiphinema Cobb, 1913 (Nematoda: Longidoridae) with exclusion of the X. americanum-group. Systematic Parasitology 16, 35–66.
| A revised polytomous key for the identification of species of the genus Xiphinema Cobb, 1913 (Nematoda: Longidoridae) with exclusion of the X. americanum-group.Crossref | GoogleScholarGoogle Scholar |
Loof, P. A. A., Luc, M., and Baujard, P. (1996). A revised polytomous key for the identification of species of the genus Xiphinema Cobb, 1913 (Nematoda: Longidoridae) with exclusion of the X. americanum-group: Supplement 2. Systematic Parasitology 33, 23–29.
Luc, M., and Kostadinov, A. (1982). Xiphinema algeriense n. sp. (Nematoda: Longidoridae). Bulletin Museum national Historie naturelle, Paris, 4eme séries, 3, section A, 777–781.
Luc, M., Coomans, A., Loof, P. A. A., and Baujard, P. (1998). The Xiphinema americanum group (Nematoda: Longidoridae). 2. Observations on Xiphinema brevicollum Lordello & Da Costa, 1961 and comments on the group. Fundamental and Applied Nematology 21, 475–490.
Neilson, R., Ye, W., Oliveira, C. M. G., Hübschen, J., Robbins, R. T., Brown, D. J. F., and Szalanski, A. L. (2004). Phylogenetic relationships of Longidoridae species (Nematoda: Dorylaimida) from North America inferred from 18S rDNA sequence data. Helminthologia 41, 209–215.
| 1:CAS:528:DC%2BD2MXitFOjtbc%3D&md5=26e1ce42bd8e72d22def95b45e7f9a13CAS |
Nunn, G. B. (1992). Nematode molecular evolution. Ph.D. Thesis, University of Nottingham.
Oliveira, C. M. G., Ferraz, L. C. C. B., and Neilson, R. (2006). Xiphinema krugi, species complex or complex of cryptic species? Journal of Nematology 38, 418–428.
| 1:CAS:528:DC%2BD2sXjvFKqt7g%3D&md5=ac3e5b101187cd21bca4294b38a1501fCAS |
Page, R. D. (1996). TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357–358.
| 1:STN:280:DyaK2s%2FlvVSgtg%3D%3D&md5=0b115f1c34d59a6279f7f1ccf2b946f9CAS |
Palomares-Rius, J. E., Subbotin, S. A., Landa, B. B., Vovlas, N., and Castillo, P. (2008). Description and molecular characterisation of Paralongidorus litoralis sp. n. and P. paramaximus Heyns, 1965 (Nematoda: Longidoridae) from Spain. Nematology 10, 87–101.
| Description and molecular characterisation of Paralongidorus litoralis sp. n. and P. paramaximus Heyns, 1965 (Nematoda: Longidoridae) from Spain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVeqtbc%3D&md5=626ba2e465ebad6d0f0078032011c6b0CAS |
Palomares-Rius, J. E., Cantalapiedra-Navarrete, C., Gutiérrez-Gutiérrez, C., Liébanas, G., and Castillo, P. (2013). Morphological and molecular characterisation of Paralongidorus plesioepimikis n. sp. (Nematoda: Longidoridae) from southern Spain. Nematology 15, 363–378.
| Morphological and molecular characterisation of Paralongidorus plesioepimikis n. sp. (Nematoda: Longidoridae) from southern Spain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlslShsLw%3D&md5=05f63d35819153ec26da48715baff1fdCAS |
Palomares-Rius, J. E., Cantalapiedra-Navarrete, C., and Castillo, P. (2014). Cryptic species in plant-parasitic nematodes. Nematology 16, 1105–1118.
| Cryptic species in plant-parasitic nematodes.Crossref | GoogleScholarGoogle Scholar |
Robbins, R. T., Brown, D. J., Halbrendt, J. M., and Vrain, T. C. (1996). Compendium of juvenile stages of Xiphinema species (Nematoda: Longidoridae). Russian Journal of Nematology 4, 163–171.
Roca, F. (1991). Xiphinema coronatum sp. n. (Nematoda: Longidoridae) from Italy. Revue de Nématologie 14, 597–601.
Ronquist, F., and Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MRBAYES 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=eb4d9b9211c4f59088b8e30c23025081CAS |
Roshan-Bakhsh, A., Pourjam, E., Pedram, M., Robbins, R. T., and Decraemer, W. (2014). Description of Xiphinema castilloi sp. n. (Dorylaimida: Longidoridae) from Iran and its phylogenetic relationships. Nematology 16, 359–368.
| Description of Xiphinema castilloi sp. n. (Dorylaimida: Longidoridae) from Iran and its phylogenetic relationships.Crossref | GoogleScholarGoogle Scholar |
Schuurmans Stekhoven Jr, J. H., and Teunissen, R. J. H. (1938). Nématodes libres terrestres. Exploration du Parc National Albert - Mission G. F. De Witte (1933–35), fasc. 22, 229 pp.
Seinhorst, J. W. (1966). Killing nematodes for taxonomic study with hot f.a. 4 : 1. Nematologica 12, 178.
| Killing nematodes for taxonomic study with hot f.a. 4 : 1.Crossref | GoogleScholarGoogle Scholar |
Soetaert, K., Muthumbi, A., and Heip, C. (2002). Size and shape of ocean margin nematodes: morphological diversity and depth-related patterns. Marine Ecology Progress Series 242, 179–193.
| Size and shape of ocean margin nematodes: morphological diversity and depth-related patterns.Crossref | GoogleScholarGoogle Scholar |
Sturhan, D. (1983). Description of two new Xiphinema species from Portugal, with notes on X. pachtaicum and X. opisthohysterum (Nematoda, Longidoridae). Nematologica 29, 270–283.
| Description of two new Xiphinema species from Portugal, with notes on X. pachtaicum and X. opisthohysterum (Nematoda, Longidoridae).Crossref | GoogleScholarGoogle Scholar |
Taylor, C. A., and Brown, D. J. F. (1997). ‘Nematode Vectors of Plant Viruses.’ (CAB International: Wallingford, UK.)
Tzortzakakis, E., Archidona-Yuste, A., Cantalapiedra-Navarrete, C., Nasiou, E., Lazanaki, M., Kabourakis, E., Palomares-Rius, J. E., and Castillo, P. (2014). Integrative diagnosis and molecular phylogeny of dagger and needle nematodes of olives and grapevines in the island of Crete, Greece, with description of Xiphinema cretense n. sp. (Nematoda, Longidoridae). European Journal of Plant Pathology 140, 563–590.
| Integrative diagnosis and molecular phylogeny of dagger and needle nematodes of olives and grapevines in the island of Crete, Greece, with description of Xiphinema cretense n. sp. (Nematoda, Longidoridae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlart7%2FE&md5=8333bdea6951da2cb101481c28e35e45CAS |
Tzortzakakis, E., Archidona-Yuste, A., Cantalapiedra-Navarrete, C., Nasiou, E., Palomares-Rius, J. E., and Castillo, P. (2015). Description and molecular characterisation of Xiphinema herakliense n. sp. (Nematoda: Longidoridae) from wild and cultivated olives in Crete. Nematology 17, 231–245.
| Description and molecular characterisation of Xiphinema herakliense n. sp. (Nematoda: Longidoridae) from wild and cultivated olives in Crete.Crossref | GoogleScholarGoogle Scholar |
Vrain, T. C., Wakarchuk, D. A., Levesque, A. C., and Hamilton, R. I. (1992). Intraspecific rDNA restriction fragment length polymorphism in the Xiphinema americanum group. Fundamental and Applied Nematology 15, 563–573.
Ye, W., Szalanski, A. L., and Robbins, R. T. (2004). Phylogenetic relationships and genetic variation in Longidorus and Xiphinema species (Nematoda: Longidoridae) using ITS1 sequences of nuclear ribosomal DNA. Journal of Nematology 36, 14–19.
| 1:CAS:528:DC%2BD2cXlslGls70%3D&md5=2c125a3e33faabcb25654a7b0ff0b9daCAS |
Yeates, G. W. (1986). Stylet and body lengths as niche dimensions in plant-parasitic nematodes. Zoologischer Anzeiger 216, 327–337.
Zullini, A. (1973). Some soil and freshwater nematodes from Chiapas (Mexico). Academia Nazionale die Lincei. Quaderno 171, 73–96.