Skip to main content
SpringerLink
Log in

Species diversity of ring nematodes of the genus Criconemoides (Nematoda: Criconematidae) based on three new species from China, using integrative taxonomy

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Ring nematodes of the genus Criconemoides are a group of polyphagous, migratory root-ectoparasites of plants. In a nematological survey of Zhejiang Province, three new Criconemoides species were isolated from the rhizosphere of Citrus sp., Euonymus alatus and Pterocarya stenoptera trees. In the present study, the new species characterized using an integrative taxonomic approach and described as Criconemoides parainformis n. sp., C. geraerti n. sp. and C. rotundicaudatus n. sp. Three of the species shares truncated anteriorly flattened lip region comprised of two annuli, body annuli margin smooth with few anastomoses, (except C. rotundicaudatus n. sp. it has crenated annuli margins and numerous anastomoses), excretory pore 1–2 annuli posterior to pharyngeal bulb base, (except C. geraerti n. sp. it has excretory pore at the same level, or 1–2 annuli anterior to pharyngeal bulb base), vulva closed, anus hardly visible 1–3 annuli posterior to vulva. The new species can be distinguished based on their en face view pattern under scanning electron microscope (SEM) and the tail shapes. i.e. C. parainformis n. sp. has an ellipsoid oral disc, slightly fused pseudolips and tail ending in a bilobed terminus. C. geraerti n. sp. has a hexagonal oral disc, separated pseudolips, and a bluntly conoid tail. C. rotundicaudatus n. sp. has a rounded oral disc, well developed pseudolips, and a short broadly rounded tail. Besides detailed morphological studies using SEM, genomic and mitochondrial molecular data were obtained for the three described new species. In inferred phylogenies, these three species clustered with known Criconemoides species in 18S, 28S, ITS and coxI trees. Currently, only four known Criconemoides species occur in China and the discovery of the three new Criconemoides species in present study has increased our knowledge on the diversity of Criconemoides in China.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Similar content being viewed by others

Notes

  1. Specific epithet formed from the Latin word para = beside or near, and the species epithet informis, thereby reflecting its close similarity to C. informis.

  2. Specific epithet is named in honour of Professor Etienne Geraert for his extraordinary contribution to our knowledge of nematode taxonomy.

  3. Specific epithet is based on the specific tail morphology, rotundum = round and cauda = tail.

References

  • Andrássy, I. (1965). Verzeichnis und Bestimmungsschlüssel der Arten der Nematoden-Gattungen Criconemoides Taylor, 1936 und Mesocriconema n. gen. Opuscula Zoologica Instituti Zoosystematici Universitatis Budapestinensis, 5, 153–171.

    Google Scholar 

  • Armenteros, M., Rojas-Corzo, A., Ruiz-Abierno, A., Derycke, S., Backeljau, T., & Decraemer, W. (2014). Systematics and DNA barcoding of free-living marine nematodes with emphasis on tropical desmodorids using nuclear SSU rDNA and mitochondrial COI sequences. Nematology, 16(8), 979–989.

    Article  Google Scholar 

  • Brzeski, W., Choi, Y. E., & Loof, P. A. A. (2002). Compendium of the genus Criconemoides Taylor, 1936 (Nematoda: Criconematidae). Nematology, 4(3), 325–339.

    Article  Google Scholar 

  • Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17(4), 540–552.

    Article  CAS  PubMed  Google Scholar 

  • Choi, Y. E., & Geraert, E. (1975). Criconematids from Korea with the description of eight new species (Nematoda: Tylenchida). Nematologica, 21(1), 35–52.

    Article  Google Scholar 

  • Choi, Y. E., & Geraert, E. (1995). Systematic study of Criconematoidea from Korea. 3. Two new and one known species of Criconematoidea from Korea (Nematoda: Tylenchida). Korean Journal of Applied Entomology, 34(4), 350–359.

    Google Scholar 

  • Cordero, M. A., Robbins, R. T., & Szalanski, A. L. (2012). Taxonomic and molecular identification of Mesocriconema and Criconemoides species (Nematoda: Criconematidae). Journal of Nematology, 44(4), 399–426.

    PubMed  PubMed Central  Google Scholar 

  • Darriba, D. T. G., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Grisse, A. (1964). Criconemoides flandriensis n. sp. (Nematoda: Criconematidae). Nematologica, 9(4), 547–552.

    Article  Google Scholar 

  • De Grisse, A. (1967). Description of fourteen new species of Criconematidae with remarks on different species of this family. Biologisch Jaarboek Dodonaea, 35, 66–125.

    Google Scholar 

  • De Grisse, A. T. (1969). Redescription ou modification de quelques techniques utilisées dans l’étude des nematodes phytoparasitaires. Mededelingen van de Rijksfaculteit der Landbouwwetenschappen Gent, 34, 351–369.

    Google Scholar 

  • De Ley, P., Félix, M. A., Frisse, L. M., Nadler, S. A., Sternberg, P. W., & Thomas, W. K. (1999). Molecular and morphological characterisation of two reproductively isolated species with mirror-image anatomy (Nematoda: Cephalobidae). Nematology, 1, 591–612.

    Article  Google Scholar 

  • Eroshenko, A. S. (1981). Crossonemoides n. gen. And three new species of ectoparasitic nematodes of plants (Nematoda: Criconematidae) from the Primorsk zone. Parazitologiya, 15(6), 547–551.

    Google Scholar 

  • Eskandari, A., Karegar, A., Pourjam, E., van der Berg, E., & Tiedt, L. (2010). Additional data on some poorly known species of Criconemoides Taylor, 1936 (Nematoda: Criconematidae). Nematology, 12(4), 505–518.

    Article  Google Scholar 

  • Ferris, H., Zheng, L., & Walker, M. A. (2012). Resistance of grape rootstocks to plant-parasitic nematodes. Journal of Nematology, 44(4), 377–386.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Geraert, E. (2010). The Criconematidae of the world: Identification of the family Criconematidae (Nematoda). Ghent: Academia Press.

    Google 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.

    CAS  Google Scholar 

  • Hoffmann, J. K. (1974). Morphological variation in species of Bakernema, Criconema, and Criconemoides (Criconematidae: Nematoda). Iowa State Journal of Research 49, 137–53.

  • Inserra, R. N., Stanley, J. D., Ochoa, A., Schubert, T. S., Subbotin, S. A., Crow, W. T., & McSorley, R. (2014). Hemicriconemoides species as crop damaging parasitic nematodes in Florida. Nematology Circular 223, 1–6.

  • Jahanshahi Afshar, F., Pourjam, E., & Pedram, M. (2019a). Lobocriconema iranense (Van den Berg, Eskandari, Tiedt & Karegar, 2010) n. comb. and description of L. nokandense n. sp. (Nematoda: Criconematidae) from Iran. Nematology, 21(10), 1043–1061.

    Article  CAS  Google Scholar 

  • Jahanshahi Afshar, F., Pourjam, E., & Pedram, M. (2019b). New morphological observations on Neolobocriconema serratum (Khan & Siddiqi, 1963) Mehta & Raski, 1971 (Rhabditida: Criconematidae). Nematology, 21(4), 419–434.

  • Jenkins, W. R. (1964). A rapid centrifugal-flotation method for separating nematodes from soil. Plant Disease Reporter, 48(9), 692.

    Google Scholar 

  • Joyce, S. A., Burnell, A. M., & Powers, T. O. (1994). Characterization of Heterorhabditis isolates by PCR amplification of segments of mtDNA and rDNA genes. Journal of Nematology, 26(3), 260–270.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh, K., Rozewicki, J., & Yamada, K. D. (2017). MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20, 1160–1166.

    Article  PubMed Central  Google Scholar 

  • Liu, Z. M., & Feng, Z. X. (1995). Six new records of plant nematodes in China. Journal of Guanxi Agricultural University, 14, 121–124.

    Google Scholar 

  • Maria, M., Powers, T. O., Tian, Z., Harris, T., Higgins, R., & Zheng, J. (2018a). Description and distribution of three criconematid nematodes from Hangzhou, Zhejiang Province, China. Journal of Nematology, 50(2), 183–206. https://doi.org/10.21307/jofnem-2018-010.

    Article  Google Scholar 

  • Maria, M., Cai, R., Castillo, P., & Zheng, J. (2018b). Morphological and molecular characterisation of Hemicriconemoides paracamelliae sp. n. (Nematoda: Criconematidae) and two known species of Hemicriconemoides from China. Nematology, 20(5), 403–422. https://doi.org/10.1163/15685411-00003147.

    Article  Google Scholar 

  • Maria, M., Cai, R., Subbotin, S. A., & Zheng, J. (2019). Description of Discocriconemella sinensis n. sp. (Nematoda: Criconematidae) from the rhizosphere of Camellia sinensis in China. Nematology, 21(8), 779–792.

    Article  Google Scholar 

  • Micoletzky, H. (1922). Die freilebenden Erd-Nematoden mitbesonderer Berücksichtigung der Steiermark und der Bukowina, zugleich mit einer Revision sämtlicher nicht mariner, freilebender Nematoden in Form von Genus-Beschreibungen und Bestimmungsschlüsseln. Archiv für Naturgeschichte A, 87, 1–650.

    Google Scholar 

  • Misra, S. L., & Edward, J. C. (1972). Two new species of genus Criconemoides from North India. The Allahabad Farmer, 46(3), 205–208.

    Google Scholar 

  • Nath, R. C., Sinha, B. C., Mukherjee, B., & Dasgupta, M. K. (2008). Occurrence, distribution and importance of plant parasitic nematodes associated with litchi plantations in North Tripura district. Indian Journal of Nematology, 38, 75–80.

    Google Scholar 

  • Olson, M., Harris, T., Higgins, R., Mullin, P., Powers, K., Olson, S., & Powers, T. O. (2017). Species delimitation and description of Mesocriconema nebraskense n. sp. (Nematoda: Criconematidae), a morphologically cryptic, parthenogenetic species from north American grasslands. Journal of Nematology, 49(1), 42–66.

    Article  PubMed  PubMed Central  Google Scholar 

  • Powers, T. O., Harris, T., Higgins, R., Sutton, L., & Powers, K. S. (2010). Morphological and molecular characterization of Discocriconemella inarata, an endemic nematode from north American native tallgrass prairies. Journal of Nematology, 42(1), 35–45.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Powers, T. O., Bernard, E. C., Harris, T., Higgins, R., Olson, M., Lodema, M., Mullin, P., Sutton, L., & Powers, K. S. (2014). COI haplotype groups in Mesocriconema (Nematoda: Criconematidae) and their morphospecies associations. Zootaxa, 3827(2), 101–146.

    Article  CAS  PubMed  Google Scholar 

  • Powers, T., Harris, T., Higgins, R., Mullin, P., & Powers, K. (2017). An 18S rDNA perspective on the classification of criconematoidea. Journal of Nematology, 49(3), 236–244.

    Article  PubMed  PubMed Central  Google Scholar 

  • Raski, D. J. (1952). On the morphology of Criconemoides Taylor, 1936, with descriptions of six new species (Nematoda: Criconematidae). Proceedings of the Helminthological Society of Washington, 19(2), 85–99.

    Google Scholar 

  • Raski, D. J. (1958). Nomenclatorial note on the genus Criconemoides (Nematoda: Criconematidae) with a key to the species. Proceedings of the Helminthological Society of Washington, 25(2), 139–142.

    Google Scholar 

  • Raski, D. J., & Golden, A. M. (1966). Studies on the genus Criconemoides Taylor, 1936 with descriptions of eleven new species and Bakernema variabile n. sp. (Criconematidae: Nematoda). Nematologica, 11(4), 501–565.

    Google Scholar 

  • Raski, D. J., & Riffle, J. W. (1967). Two new species and further notes on Criconemoides Taylor, 1936 (Criconematidae: Nematoda). Proceedings of the Helminthological Society of Washington, 34(2), 212–219.

    Google Scholar 

  • Ronquist, F. H. J. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12), 1572–1574.

    Article  CAS  PubMed  Google Scholar 

  • Ryss, A. Y., McClure, M. A., Nischwitz, C., Dhiman, C., & Subbotin, S. A. (2013). Redescription of Robustodorus megadorus with molecular characterization and analysis of its phylogenetic position within the family Aphelenchoididae. Journal of Nematology, 45(4), 237–252. https://doi.org/10.1017/S0022149X12000533.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seinhorst, J. W. (1959). A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica, 4(1), 67–69.

    Article  Google Scholar 

  • Siddiqi, M. R. (1961). Studies on species of Criconematinae (Nematoda: Tylenchida) from India. Proceedings of the Helminthological Society of Washington, 28(1), 19–34.

    Google Scholar 

  • Siddiqi, M. R. (2000). Tylenchida parasites of plants and insects (2nd ed.). Wallingford: CAB International.

    Book  Google Scholar 

  • Tang, C. Q., Leasi, F., Obertegger, U., Kieneke, A., Barraclough, T. G., & Fontaneto, D. (2012). The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proceedings of the National Academy of Sciences, 10(40), 16208–16212.

    Article  Google Scholar 

  • Taylor, A. L. (1936). The genera and species of the Criconematinae, a sub-family of the Anguillulinidae (Nematoda). Transactions of American Microscopical Society, 45(4), 391–421.

    Article  Google Scholar 

  • Tulaganov, A. (1941). Description of a new species of nematodes of the genus Hoplolaimus. Trudy Uzbekskoi gosudarskoi Universiteta H.S. 16. Biologiya, 11, 21–22.

    Google Scholar 

  • Van den Berg, E., & Tiedt, L. R. (2001). New records of Criconematoidea (Nematoda) from South Africa with the description of Criconema zantene n. sp. Nematology, 3(8), 797–815.

    Article  Google Scholar 

  • Van Den Berg, E., Tiedt, L. R., & Subbotin, S. A. (2012). Morphological and molecular characterisation of Criconemoides brevistylus Singh & Khera, 1976 and C. obtusicaudatus Heyns, 1962 from South Africa (Nematoda: Criconematidae) with first description of a male C. obtusicaudatus and proposal of new synonyms. Nematology, 14(8), 961–976.

    Article  Google Scholar 

  • Van den Berg, E., Tiedt, L. R., Inserra, R. N., Stanley, J. D., Vovlas, N., Palomares Rius, J. E., Castillo, P., & Subbotin, S. A. (2014). Morphological and molecular characterisation of some Hemicriconemoides species (Nematoda: Criconematidae) together with a phylogeny of the genus. Nematology, 16(5), 519–553. https://doi.org/10.1163/15685411-00002786.

    Article  CAS  Google Scholar 

  • Van Den Berg, E., Tiedt, L. R., Liébanas, G., Chitambar, J. J., Stanley, J. D., Inserra, R. N., Castillo, P., & Subbotin, S. A. (2018). Morphological and molecular characterisation of two new Hemicycliophora species (Tylenchida: Hemicycliophoridae) with a revision of the taxonomic status of some known species and a phylogeny of the genus. Nematology, 20(4), 319–354.

    Article  Google Scholar 

  • Westerdahl, B. B., & Duncan, R. A. (2015). Peach nematodes. UC Pest management guidelines (updated 9/15). UCIPM University of California Agriculture and Natural Resources, Statewide Integrated Pest Management Program. http://ipm.ucanr.edu/PMG/r602200111.html

  • Wouts, W. M. (2006). Criconematina (Nematoda: Tylenchida) fauna of New Zealand. 228pp.

  • Ye, W., Giblin-Davis, R. M., Braasch, H., Morris, K., & Thomas, W. K. (2007). Phylogenetic relationships among Bursaphelenchus species (Nematoda: Parasitaphelenchidae) inferred from nuclear ribosomal and mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution, 43(3), 1185–1197.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, J., Subbotin, S. A., He, S., Gu, J., & Moens, M. (2003). Molecular characterisation of some Asian isolates of Bursaphelenchus xylophilus and B. mucronatus using PCR-RFLPs and sequences of ribosomal DNA. Russian Journal of Nematology, 11(1), 17–22.

    Google Scholar 

Download references

Acknowledgements

This research was supported by the National Natural Science Foundation of China (No:31772137). The first author would like to thank Mrs. Carolina Cantalapiedra-Navarrete from Institute for Sustainable Agriculture (IAS), Spanish National Research Council (CSIC), Córdoba, Spain for her tremendous support on sequence editing. The authors thank Mr. Rong N. from the Center of Electron Microscopy, Life Science Division, Zhejiang University, for providing assistance in the preparation of SEM.

Author information

Authors and Affiliations

  1. Labrotory of Plant Nematology, Institute of Biotechnology, College of Agriculture & Biotechnology, Zhejiang University, Hangzhou, 310058, Zhejiang, People’s Republic of China

    Munawar Maria, Wentao Miao, Ruihang Cai, Zhongling Tian & Jingwu Zheng

  2. Institute for Sustainable Agriculture (IAS), Spanish National Research Council (CSIC), Campus de Excelencia Internacional Agroalimentario, ceiA3, Avenida Menéndez Pidal s/n, 14004, Córdoba, Spain

    Pablo Castillo

  3. Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Hangzhou, 310058, People’s Republic of China

    Jingwu Zheng

Authors
  1. Munawar Maria
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wentao Miao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ruihang Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhongling Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pablo Castillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jingwu Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jingwu Zheng.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

No specific permits were required for the described fieldwork studies. The samples from wild plants were obtained in public areas, forests, and other natural areas studied and do not involve any species endangered or protected in China. The sites are not protected in any way.

Informed consent

All the authors certify that the work carried out in this research followed the principles of ethical and professional conduct have been followed. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maria, M., Miao, W., Cai, R. et al. Species diversity of ring nematodes of the genus Criconemoides (Nematoda: Criconematidae) based on three new species from China, using integrative taxonomy. Eur J Plant Pathol 157, 119–139 (2020). https://doi.org/10.1007/s10658-020-01990-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-020-01990-2

Keywords

Search

Navigation