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

in Nematology
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

Summary

Hemicycliophora presently contains 132 valid species of sheath nematodes. Within several samples obtained from surveys in Canada, South Africa, Spain and the USA, we distinguished six valid and six putative unidentified species by integrating the results of morphological and molecular analyses. Valid species included: H. californica, H. gracilis, H. parvana, H. poranga, H. raskii, and H. signata. The putative unidentified species were indicated as Hemicycliophora sp. 10, sp. 12, sp. 15, sp. 16, sp. 17, and sp. 18. Two new species of sheath nematodes from Spain and the USA were described and named as H. onubensis sp. n. and H. robbinsi sp. n., respectively. Hemicycliophora wyei is proposed as a junior synonym of H. parvana and H. ripa is proposed as a junior synonym of H. poranga. Eighteen valid and 13 unidentified species of sheath nematodes were characterised using the partial COI mtDNA gene. A total of 94 new sequences of which 77 were for the COI mtDNA gene were obtained in this study. Phylogenetic relationships within Hemicycliophora, using the D2-D3 expansion segments of 28S rDNA, ITS rRNA and COI gene sequences, are presented as inferred from Bayesian analysis.

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

in Nematology

Sections

References

AbolafiaJ.LiébanasG. & Peña-SantiagoR. (2002). Nematodes of the order Rhabditida from Andalucía Oriental, Spain. The subgenus Pseudacrobeles Steiner, 1938, with description of a new species. Journal of Nematode Morphology and Systematics 4137-154.

BajajH.K. (1998). Criconematids of Kalesar forests and Morni hills of Haryana, India. Indian Journal of Nematology 28150-158.

BrzeskiM.W. (1974). Taxonomy of the Hemicycliophorinae (Nematoda, Tylenchida). Problemowe Postepow Nauk Rolniczych 154237-330.

CastilloP.Gomez-BarcinaA. & LoofP.A.A. (1989). On two species of Hemicycliophora de Man, 1921 (Nematoda: Criconematoidea) found in Spain. Nematologia Mediterranea 1777-82.

CastilloP.VovlasN.SubbotinS. & TroccoliA. (2003). A new root-knot nematode, Meloidogyne baetica n. sp. (Nematoda: Heteroderidae), parasitizing wild olive in southern Spain. Phytopathology 931093-1102. DOI: 10.1094/PHYTO.2003.93.9.1093

ChavesE. (1983). Criconematoidea (Nematoda) from Argentina. Nematologica 29404-424. DOI: 10.1163/187529283X00285

ChitambarJ.J. & SubbotinS.A. (2014). Systematics of the sheath nematodes of the superfamily Hemicycliophoroidea. Nematology Monographs and Perspectives 10 (Series Editors: HuntD.J. & PerryR.N.). Leiden, The NetherlandsBrill.

ColbranR.C. (1960). Studies of plant and soil nematodes. 3. Belonolaimus hastulatus, Psilenchus tumidus and Hemicycliophora labiata, three new species from Queensland. Queensland Journal of Agricultural Science 17175-181.

CoolenW.A. (1979). Methods for extraction of Meloidogyne spp. and other nematodes from roots and soil. In: LambertiF. & TaylorC.E. (Eds). Root-knot nematodes (Meloidogyne species). Systematics biology and control. London, UKAcademic Press pp. 317-329.

Cordero LópezM.A.RobbinsR.T. & SzalanskiA.L. (2013). Taxonomic and molecular identification of Hemicycliophora, Caloosia, Gracilacus and Paratylenchus species (Nematoda: Criconematidae). Journal of Nematology 45145-171.

CurranJ.DriverF.BallardJ.W.O. & MilnerR.J. (1994). Phylogeny of Metarhizium: analysis of ribosomal DNA sequence data. Mycological Research 98547-555. DOI: 10.1016/S0953-7562(09)80478-4

De GrisseA.T. (1969). Redescription ou modification de quelques techniques utilisées dans l’étude des nématodes phytoparasitaires. Mededelingen van de Rijksfaculteit der Landbouwwetenschappen Gent 34351-369.

de ManJ.G. (1921). Nouvelles recherches sur les nématodes libres terricoles de la Hollande. Capita Zoologica 13-62.

DoucetM.E. (1982). Quatre nouvelles espèces du genre Hemicycliophora de Man, 1921 (Nematoda: Tylenchida) provenant d’Argentine. Revue de Nématologie 5309-320.

GoffartH. (1951). Nematoden aus unterirdischen Gewassern. Deutsche Zoologische Zeitschrift 173-78.

GoodeyJ.B. (1963). Soil and freshwater nematodes2nd edition. London, UKMethuen.

HeynsJ. (1962). Two new species of Criconematidae from South Africa. Nematologica 821-24. DOI: 10.1163/187529262X00963

JairajpuriM.S. & BaqriQ.H. (1973). Nematodes of high altitudes in India. I. Four new species of Tylenchida. Nematologica 1919-30. DOI: 10.1163/187529273X00051

KirjanovaE.S. & ShagalinaL.M. (1974). [Hemicycliophora pruni sp. nov. (Nematoda: Hemicycliophoridae) – a parasite of plum tree in central Kopetdagh.] Izvestiya Akademii Nauk Turkmenskoi SSR Serija Biologicheskikh Nauk 635-39.

LoofP.A.A. (1968). Taxonomy of Hemicycliophora species from west and central Europe (Nematoda: Criconematoidea). Mededelingen Landbouwhogeschool Wageningen 68-14 52 pp.

LoofP.A.A. (1984). Hemicycliophora species from Iran (Nematoda: Criconematoidea). Nematologica 3022-41. DOI: 10.1163/187529284X00437

LoofP.A.A. & De GrisseA. (1989). Taxonomic and nomenclatorial observations on the genus Criconemella De Grisse & Loof, 1965, sensu Luc & Raski, 1981. Mededelingen Faculteit Landbouwwetenschappen Rijksuniversiteit Gent 5453-74.

LoofP.A.A. & HeynsJ. (1969). Taxonomy of Hemicycliophora species from South Africa (Nematoda: Criconematoidea). Nematologica 15464-472. DOI: 10.1163/187529269X00795

LoosC.A. (1948). Notes on free-living and plant-parasitic nematodes of Ceylon 3. Ceylon Journal of Science 23119-124.

MaX. & AgudeloP. (2015). First report of Hemicycliophora wyei on bentgrass in Texas. Plant Disease 99732. DOI: 10.1094/PDIS-09-14-0972-PDN

MehtaU.K.RaskiD.J. & ValenzuelaA.A. (1983). Five new species of Criconematidae (Nemata) from southern Chile. Nematologica 28(1982) 398-411. DOI: 10.1163/187529282X00204

MicoletzkyH. (1913). Die freilebenden Süsswassernematoden der Ost-Alpen. 1. Teil der vorlaüfi ge Mitteilung: Die frilebenden Süsswassernematoden des Lunzer Seengebietes. Sitzungsberichte der K. Akademie der Wissenschaften in Wien Mathematisch-Naturwissenschaftliche-Klasse Abt. 1 122(1) 111-122; 122(4) 543-548.

MonteiroA.R. & LordelloL.G.E. (1978). A description of Hemicycliophora poranga n. sp. from Brazil (Nemata). Revista Brasileira de Biologia 38569-571.

NetscherC. & SeinhorstJ.W. (1969). Propionic acid better than acetic acid for killing nematodes. Nematologica 15286.

Orton WilliamsK.J. (1978). Two new species of the genus Hemicycliophora de Man, 1921 (Nematoda: Tylenchida). Revue de Nématologie 1197-205.

PowersT.O.BernardE.C.HarrisT.HigginsR.OlsonM.LodemaM.MullinP.SuttonL. & PowersK.S. (2014). COI haplotype groups in Mesocriconema (Nematoda: Criconematidae) and their morphospecies associations. Zootaxa 3827101-146. DOI: 10.11646/zootaxa.3827.2.1

PowersT.O.BernardE.C.HarrisT.HigginsR.OlsonM.OlsonS.LodemaM.MatczyszynJ.MullinP.SuttonL. et al. (2016a). Species discovery and diversity in Lobocriconema (Criconematidae: Nematoda) and related plant-parasitic nematodes from North American ecoregions. Zootaxa 4085301-344. DOI: 10.11646/zootaxa.4085.3.1

PowersT.O.MullinP.HigginsR.HarrisT. & PowersK.S. (2016b). Description of Mesocriconema ericaceum n. sp. (Nematoda: Criconematidae) and notes on other nematode species discovered in an ericaceous heath bald community in Great Smoky Mountains National Park, USA. Nematology 18879-903. DOI: 10.1163/15685411-00003001

RaskiD.J. (1958). Four new species of Hemicycliophora de Man, 1921, with further observations on H. brevis Thorne, 1955 (Nematoda: Criconematidae). Proceedings of the Helminthological Society of Washington 25125-131.

ReedJ.P. & JenkinsW.R. (1963). Hemicycliophora vaccinium n. sp. (Nematoda: Criconematidae) from cranberry. Proceedings of the Helminthological Society of Washington 30211-212.

RonquistF. & HuelsenbeckJ.P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 191572-1574. DOI: 10.1093/bioinformatics/btg180

SchneiderW. (1925). Freilebende Süsswassernematodes aus ostholsteinischen Seen. Nebst Bemerkungen über die Nematodenfauna des Madu und Schaalsees II. Archiv für Hydrobiologie 15536-310.

SeinhorstJ.W. (1962). On the killing, fixation and transferring to glycerin of nematodes. Nematologica 829-32. DOI: 10.1163/187529262X00981

SeinhorstJ.W. (1966). Killing nematodes for taxonomic study with hot F.A. 4:1. Nematologica 12178. DOI: 10.1163/187529266X00239

SubbotinS.A.VovlasN.CrozzoliR.SturhanD.LambertiF.MoensM. & BaldwinJ.G. (2005). Phylogeny of Criconematina Siddiqi, 1980 (Nematoda: Tylenchida) based on morphology and D2-D3 expansion segments of the 28S rRNA gene sequences with application of a secondary structure model. Nematology 7927-944. DOI: 10.1163/156854105776186307

SubbotinS.A.SturhanD.ChizhovV.N.VovlasN. & BaldwinJ.G. (2006). Phylogenetic analysis of Tylenchida Thorne, 1949 as inferred from D2 and D3 expansion fragments of the 28S rRNA gene sequences. Nematology 8455-474. DOI: 10.1163/156854106778493420

SubbotinS.A.ChitambarJ.J.ChizhovV.N.StanleyJ.D.InserraR.N.DoucetM.E.McClureM.YeW.YeatesG.W.MollovD.S. et al. (2014). Molecular phylogeny, diagnostics, and diversity of plant-parasitic nematodes of the genus Hemicycliophora (Nematoda: Hemicycliophoridae). Zoological Journal of the Linnean Society 171475-506. DOI: 10.1111/zoj.12145

SwoffordD.L. (2003). PAUP*: phylogenetic analysis using parsimony (*and other methods) version 4.0b 10. Sunderland, MA, USASinauer Associates.

Tanha MaafiZ.SubbotinS.A. & MoensM. (2003). Molecular identification of cyst-forming nematodes (Heteroderidae) from Iran and a phylogeny based on ITS-rDNA sequences. Nematology 599-111. DOI: 10.1163/156854102765216731

TarjanA.C. (1952). The nematode genus Hemicycliophora de Man, 1921 (Criconematidae) with a description of a new plant-parasitic species. Proceedings of the Helminthological Society of Washington 1965-77.

TaylorA.L. (1936). The genera and species of the Criconematidae, a subfamily of the Anguillulinidae (Nematoda). Transactions of the American Microscopical Society 55391-421.

ThompsonJ.D.GibsonT.J.PlewniakF.JeanmouginF. & HigginsD.G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 254876-4882.

ThorneG. (1955). Fifteen new species of the genus Hemicycliophora with an emended description of H. typica de Man (Tylenchida, Criconematidae). Proceedings of the Helminthological Society of Washington 221-16.

Van den BergE. (1981). Further studies on the genus Hemicycliophora de Man, 1921 in South Africa (Nematoda: Hemicycliophoroidea) with description of a new species. Phytophylactica 13181-194.

Van den BergE. (1987a). New Hemicycliophora species from the Western Cape Province (Hemicycliophoridae: Nematoda). Phytophylactica 1965-70.

Van den BergE. (1987b). More Hemicycliophora species from South Africa (Hemicycliophoridae: Nematoda). Phytophylactica 19309-314.

Van den BergE.SubbotinS.A. & TiedtL.R. (2010). Morphological and molecular characterisation of Hemicycliophora lutosa Loof & Heyns, 1969 and H. typica, 1921 from South Africa (Nematoda: Hemicycliophoridae). Nematology 12303-308. DOI: 10.1163/138855409X12511010796671

Van den BergE.TiedtL.R.InserraR.N.StanleyJ.D.VovlasN.Palomares-RiusJ.E.CastilloP. & SubbotinS.A. (2015). Characterisation of a topotype and other populations of Hemicriconemoides strictathecatus Esser, 1960 (Nematoda: Criconematidae) from Florida with description of H. phoenicis sp. n. from the USA. Nematology 17265-300. DOI: 10.1163/15685411-00002866

ZengY.YeW.KernsJ.TredwayL.MartinS. & MartinM. (2015). Molecular characterization and phylogenetic relationships of plant-parasitic nematodes associated with turf grasses in North Carolina and South Carolina, United States. Plant Disease 99982-993. DOI: 10.1094/PDIS-10-14-1060-RE

Figures

  • View in gallery

    Hemicycliophora species and populations used in the present study.

  • View in gallery

    (Continued.)

  • View in gallery

    (Continued.)

  • View in gallery

    (Continued.)

  • View in gallery

    Hemicycliophora onubensis sp. n. from Huelva, Spain. Female. A: Anterior region; B: Detail of stylet knobs; C: Detail of lip region; D: Lateral field at mid-body; E. F: Posterior region; G, H: Tail region. (Scale bar = 10 μm.)

  • View in gallery

    Scanning electron microscope micrographs of Hemicycliophora onubensis sp. n. from Huelva, Spain. Female. A: Entire body; B-D: Anterior region; E: En face view; F: Detail of lateral field at mid-body; G-I: Posterior region; J: Tail tip. Abbreviations: a = anus; aa = amphidial aperture; ep = excretory pore; ld = labial disc; lf = lateral field; V = vulva. (Scale bars: A = 50 μm; B-D, F, J = 5μm; E = 2 μm; G-I = 10 μm.)

  • View in gallery

    Morphometrics of Hemicycliophora onubensis sp. n. from Huelva, Spain. All measurements are in μm and in the form: mean ± s.d. (range).

  • View in gallery

    Hemicycliophora robbinsi sp. n. from Florida, USA (CD656). Female. A: Anterior region; B: Lip region; C: Lateral field at mid-body; D: Tail, posterior region; E: Posterior region; F: Lateral field opposite vulva; G: Tail tip of another female. (Scale bar = 30 μm.)

  • View in gallery

    Morphometrics of Hemicycliophora robbinsi sp. n. from Florida, USA. All measurements are in μm and in the form: mean ± s.d. (range).

  • View in gallery

    Photomicrographs of H. parvana from the type slide. Female. A, B: Anterior region; C, D: Posterior region; E, G, H: Lateral field; F: Vulval region. (Scale bars: A-E = 50 μm; F-H = 25 μm.)

  • View in gallery

    Hemicycliophora parvana from Paines Praire, Florida, USA. Female. A: Anterior region; B, C: Posterior region of two specimens; D: Spermatheca; E: Lateral field posterior to vulva; F: Lateral field at mid-body. (Scale bar = 30 μm.)

  • View in gallery

    Photomicrographs of Hemicycliophora species. Female. A-F: Anterior region; G-L: Posterior region. A, G: H. poranga (CD1835, USA, CA); B, H: H. signata (CD1385; Mozambique); C, I: Hemicycliophora sp. 12 (CD2267, Canada); D, J: Hemicycliophora sp. 15 (CD2268, Canada); E, K: Hemicycliophora sp. 16 (CD1823, USA, CA); F, L: Hemicycliophora sp. 17 (CD1627, USA, CA). (Scale bar = 50 μm.)

  • View in gallery

    Hemicycliophora poranga (GP-35) from South Africa. Female. A: Anterior part of body; F: Annuli at mid-body, fourth-stage juvenile. B: Anterior part of body; D: Ovarial primordium; E: Annuli at mid-body, second-stage juvenile. C: Anterior part of body. (Scale bar = 30 μm.)

  • View in gallery

    Hemicycliophora poranga (GP-35) from South Africa. A: Female, posterior part of body; B: Fourth-stage juvenile, posterior part of body; C: Second-stage juvenile, posterior part of body; D: Second-stage juvenile, posterior part of body; E: Second-stage juvenile, ovarial primordium. (Scale bar = 30 μm.)

  • View in gallery

    Scanning electron microscope micrographs of Hemicycliophora poranga from South Africa. Female. A, B: Anterior region; C: En face view; D: Vulva; E: Lateral field; F: Tail.

  • View in gallery

    Measurements of females and juveniles of Hemicycliophora typica and females of H. poranga (GP-35) from South Africa. All measurements are in the form: mean ± s.d. (range).

  • View in gallery

    Measurements of Hemicycliophora poranga juveniles (GP-35) from South Africa. All measurements are in μm in the form: mean ± s.d. (range).

  • View in gallery

    Hemicycliophora signata from Mozambique (Moz18). Female. A: Anterior region; B: Posterior region; C: Lateral field at mid-body; D: Lateral field opposite pharyngeal area; E: Spermatheca. Juvenile. F: Anterior region; G-I: Tail region; J: Lateral field opposite pharyngeal area; K: Lateral field at mid-body. (Scale bar = 30 μm.)

  • View in gallery

    Scanning electron microscope micrographs of Hemicycliophora signata from Mozambique (Moz18). Female. A, B: Lip region, anterior region; C: Lip region, en face view; D: Entire body; E: Vulval region, ventral view; F: Annuli at mid-body; G: Posterior region; H: Lateral field at mid-body; I, J: Lateral and ventral view of tail region; K: Ornamented tail tip as seen from posterior direction.

  • View in gallery

    Measurements of females and juveniles of Hemicycliophora signata from Mozambique. All measurements are in the form: mean ± s.d. (range).

  • View in gallery

    Scanning electron microscope micrographs of Hemicycliophora typica female from South Africa (Tvl2055). A, B: Lip region, en face view; C: Lip region, anterior region; D: Mid-body; E, F: Tail, ventral view; G: Vulval region, ventral view. (Scale bars: A-C = 10 μm; D, G = 20 μm; E, F = 50 μm.)

  • View in gallery

    Phylogenetic relationships within populations and species of Hemicycliophora as inferred from Bayesian analysis using the D2-D3 of 28S rRNA gene sequence data set under the GTR + G + I model. Posterior probabilities of over 70% are given for appropriate clades. Newly obtained sequences are indicated in bold. Clade numbers are given as in Subbotin et al. (2014). 1Identified as H. ripa by Subbotin et al. (2014); 2identified as H. wyei by Subbotin et al. (2014); 3identified as H. italiae by Subbotin et al. (2014) (synonym of H. minora according to Chitambar & Subbotin (2014)); 4identified as Hemicycliophora sp. 4 by Subbotin et al. (2014); 5identified as Hemicycliophora sp. 14 by Subbotin et al. (2014); 6identified as H. vaccinii by Subbotin et al. (2014).

  • View in gallery

    Phylogenetic relationships within populations and species of Hemicycliophora as inferred from Bayesian analysis using the ITS rRNA gene sequence data set under the GTR + G + I model. Posterior probabilities of over 70% are given for appropriate clades. Newly obtained sequences are indicated in bold. Clade numbers are given as in Subbotin et al. (2014). 1Identified as H. ripa by Subbotin et al. (2014); 2identified as H. wyei by Subbotin et al. (2014); 3identified as H. wyei by Zeng et al. (2015) and H. conida in GenBank; 4identified as H. zuckermani by Cordero López et al. (2013); 5identified as H. labiata by Cordero López et al. (2013); 6identified as H. shepherdi by Cordero López et al. (2013); 7identified as H. epicharoides by Cordero López et al. (2013); 8identified as Hemicycliophora sp. 4 by Subbotin et al. (2014).

  • View in gallery

    Phylogenetic relationships within populations and species of Hemicycliophora as inferred from Bayesian analysis using the COI mtDNA gene sequence data set under the GTR + G + I model. Posterior probabilities of over 70% are given for appropriate clades. Newly obtained sequences are indicated in bold. Clade numbers are given as in Subbotin et al. (2014). 1Identified as H. typica by Powers et al. (2014); 2identified as Hemicycliophora sp. by Powers et al. (2014); 3identified as H. thornei by Powers et al. (2014); 4identified as H. macristhmus by Powers et al. (2014) (synonym of H aquatica according to Chitambar & Subbotin (2014)).

Index Card

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 14 14 3
Full Text Views 13 13 13
PDF Downloads 2 2 2
EPUB Downloads 0 0 0