Nematology 2011 Vol 13(4) 381-393

Morphological and molecular characterisation of Caloosialongicaudata (Loos 1948) Siddiqi amp Goodey 1963 (Nematoda

Caloosiidae) from Maui the Hawaiian Islands with noteson some species of the genus

Esther VAN DEN BERG 1lowast Louwrens R TIEDT 2 and Sergei A SUBBOTIN 34

1 National Collection of Nematodes Biosystematics Division ARC-Plant Protection Research InstitutePrivate Bag X 134 Queenswood 0121 South Africa

2 Laboratory for Electron Microscopy North West University Potchefstroom Campus Potchefstroom 2520 South Africa3 Plant Pest Diagnostics Center California Department of Food and Agriculture 3294 Meadowview Road

Sacramento CA 95832-1448 USA4 Centre of Parasitology AN Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences

Leninskii Prospect 33 Moscow 117071 Russia

Received 12 April 2010 revised 19 July 2010Accepted for publication 19 July 2010 available online 1 December 2010

Summary ndash Caloosia longicaudata is described from Maui the Hawaiian Islands for the first time and both sexes are characterisedmorphologically using light and scanning electron microscopy Molecular characterisation of C longicaudata using the D2-D3 domainof 28S rRNA partial 18S rRNA and ITS rRNA gene sequences is also provided The phylogenetic relationships of this species with otherrepresentatives of the suborder Criconematina are presented and discussed A diagnostic PCR-ITS-RFLP profile for C longicaudata isgiven together with an identification table for eight species of Caloosia Caloosia langola n comb is transferred to the genus and Cshorai is synonymised with H psidii

Keywords ndash Caloosia shorai n syn Hemicaloosia Hemicaloosia langola n comb molecular morphology morphometrics newcombination new record new synonym phylogeny SEM taxonomy

During sampling for nematodes in cultivated and nat-ural areas of Maui the Hawaiian Islands several speci-mens of Caloosia Siddiqi amp Goodey 1964 were foundMorphological and morphometric analysis revealed thatthese specimens belong to C longicaudata (Loos 1948)Siddiqi amp Goodey 1964 which is the type species for thegenus This finding is the first record of this genus in theHawaiian Islands and the USA

Siddiqi (2000) listed ten species of Caloosia and sincethen two more species have been described C exiguaVan den Berg Marais amp Tiedt 2003 from water sugarbushin the Gouekrans area South Africa (Van den Berg et al2003) and C langola Pramodini Mohilal amp Ghambir2007 from lemon trees in Manirup India (Pramodiniet al 2007) Most descriptions of Caloosia species areincomplete and based on light microscopic studies only

lowast Corresponding author e-mail VDBergEarcagricza

More detailed redescriptions of species from variouslocations may provide evidence on possible variation insome taxonomic morphological characters and help toconfirm the validity of some species

The position of this genus within the suborder Cricone-matina is subject to some discussion and has never beentested using molecular phylogenetic approaches Siddiqi(1980 2000) placed Caloosia together with HemicaloosiaRay amp Das 1978 as members of the family Caloosiidaein the superfamily Hemicycliophoroidea In the phylo-genetic scheme of the Criconematina presented by Sid-diqi (1980) Caloosiidae and Hemicycliophoridae repre-sent one lineage and Caloosiidae was considered as moreprimitive and originated from a common ancestor withMacroposthoniinae In the cladogram given two decadeslater by Siddiqi (2000) Hemicycliophoroidea (Caloosi-

copy Koninklijke Brill NV Leiden 2011 DOI101163138855410X528947Also available online - wwwbrillnlnemy 381

E van den Berg et al

idae and Hemicycliophoridae) also represent one of thelineages and it has a sister relationship with Criconema-toidea Although Raski and Luc (1987) did not recog-nise the family Caloosiidae they considered Caloosia andHemicycliophora de Man 1921 to be related and placedthese genera in the subfamily Hemicycliophorinae An-other view on Caloosia evolution was proposed by Gan-guly and Khan (1983) who believed that the body shapestraight spicules and relatively thin cuticle in Caloosiidaeshows its closer affinity with tylenchids as well as withparatylenchids rather than with Hemicycliophora Theysuggested that Caloosiidae seems to be quite primitive andmight have derived much earlier than other criconematidsIn this article the classification scheme adopted by De-craemer and Hunt (2006) is used

The major objectives of this work were i) to charac-terise morphologically and morphometrically this Hawai-ian population of C longicaudata and compare it withprevious descriptions ii) to characterise molecularly Clongicaudata using the D2-D3 domain of 28S rRNAITS1-58S-ITS2 rRNA and partial 18S rRNA gene se-quences iii) to reconstruct and test the phylogenetic po-sition of C longicaudata within the suborder Cricone-matina using analysis of the genes and iv) to providean identification table for the known species of the genusCaloosia

Materials and methods

NEMATODE POPULATION LIGHT AND SCANNING

MICROSCOPY

A sample containing this nematode was collected inMaui the Hawaiian Islands from an unknown plant inAugust 2009 Specimens were extracted from the soilusing the Baermann funnel method killed and preservedin 4 formalin On arriving in South Africa they weretransferred to TAF then to pure anhydrous glycerin (DeGrisse 1969) and mounted on permanent slides Forelectron microscopy TAF fixed specimens were hydratedin decreasing concentrations of glycerin and alcohol indistilled water to pure distilled water then dehydratedin increasing concentrations of alcohol in distilled waterand finally into pure alcohol Following conventionalcritical point drying and goldpalladium coating (15 nm)specimens were viewed with a FEI ESEM Quanta 200scanning electron microscope at 10 kV

DNA EXTRACTION PCR PCR AND SEQUENCING

DNA was extracted from several dead specimens usingthe proteinase K protocol Detailed protocols for DNA ex-traction PCR cloning and sequencing were as describedby Tanha Maafi et al (2003) Three rRNA gene frag-ments ITS-rRNA D2-D3 expansion segments of 28SrRNA and partial 18S rRNA were amplified The follow-ing primers were used for amplification in the presentstudy ITS-rRNA ndash TW81 (5prime-GTTTCCGTAGGTGAACCTGC-3prime) and AB28 (5prime-ATATGCTTAAGTTCAGCGGGT-3prime) Tanha Maafi et al (2003) D2-D3 of 28S rRNA ndashD2A (5prime- ACAAGTACCGTGAGGGAAAGTTG-3prime) andD3B (5prime-TCGGAAGGAACCAGCTACTA-3prime) (Subbotinet al 2006) partial 18S rRNA ndash G18SU (5prime-GCTTGTCTCAAAGATTAAGCC-3prime) and R18Tyl1 (5prime-GGTCCAAGAATTTCACCTCTC-3prime) (Chizhov et al 2006) primersThe newly obtained sequences have been submitted tothe GenBank database under the numbers GU989621-GU989627

RFLP-ITS-RRNA

The PCR product of the ITS-rRNA was purified us-ing the QIAquick Gel Extraction Kit (Qiagen ValenciaCA USA) Of the purified product 3 μl was digestedby one of following restriction enzymes AvaI Bsh1236IDraI HinfI Hin6I and MspI in the buffer stipulated by themanufacturer The digested DNA was run on a 1 TAEbuffered agarose gel stained with ethidium bromide vi-sualised on a UV transilluminator and photographed Thelength of each restriction fragment from the PCR productswas obtained by a virtual digestion of the sequences usingWebCutter 20 (wwwfirstmarketcomcuttercut2html)

PHYLOGENETIC ANALYSES

The newly obtained sequences for each gene werealigned using ClustalX 183 (Thompson et al 1997) withdefault parameters with corresponding published gene se-quences (Subbotin et al 2005 2006 Chen et al 20072008a b 2009 Bert et al 2008 Holterman et al 2009Van den Berg et al 2010 De Ley et al unpubl) Out-group taxa for each dataset were chosen according to theresults of previously published data (Subbotin et al 20052006 Bert et al 2008 Holterman et al 2009) Sequencedatasets were analysed with maximum parsimony (MP)maximum likelihood (ML) methods using PAUP4b10(Swofford 2003) and Bayesian inference (BI) using Mr-Bayes 312 (Huelsenbeck amp Ronquist 2001) The bestfit model of DNA evolution for ML was obtained using

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the program MrModeltest 22 (Nylander 2002) with theAkaike Information Criterion in conjunction with PAUPBootstrap (BS) analysis for ML was made using 100pseudo-replicates with tree searches in each replicationperformed using one random-sequence-addition withoutbranch swapping BI analysis under the GTR + I + Gmodel for each gene was initiated with a random start-ing tree and was run with four chains for 10 times 106 gen-erations The Markov chains were sampled at intervalsof 100 generations Two runs were performed for eachanalysis The log-likelihood values of the sample pointsstabilised after approximately 103 generations After dis-carding burn-in samples and evaluating convergence theremaining samples were retained for further analysis Thetopologies were used to generate a 50 majority rule con-sensus tree Posterior probabilities (PP) are given on ap-propriate clades For testing of alternative topologies inML we used the Shimodaira-Hasegawa (SH) test as im-plemented in PAUP

Caloosia longicaudata (Loos 1948) Siddiqi ampGoodey 1963

(Figs 1-3)

MEASUREMENTS

See Table 1

DESCRIPTION

Female

Body slightly arcuate ventrad Cuticular sheath absentLateral field not demarcated Cuticle appearing smoothunder light microscope but SEM showing very faint lon-gitudinal lines Lip region high with two annuli first pro-jecting slightly anteriad or outward second projectingoutward Lip annuli separated from each other and fromfirst body annulus by a slight neck Succeeding body an-nuli rounded First few body annuli very slightly sepa-rated from each other remainder not separated En faceview showing a smooth oblong first lip annulus with awell-raised oval labial disc and two large rectangularamphidial openings Cephalic framework weakly sclero-tised Stylet slender slightly curved dorsad with anteri-orly sloping stylet knobs Opening of dorsal pharyngealgland duct 7plusmn12 (55-75) μm from base of stylet knobsBasal pharyngeal bulb amalgamated with broad isthmusexpanding only very slightly Nerve ring opposite isthmusand basal bulb junction Hemizonid seen in two speci-mens only one body annulus long situated opposite or

one annulus anterior to excretory pore Hemizonion notseen Excretory pore situated from one annulus anterior tofive annuli posterior to base of pharynx Annuli rounded5 plusmn 05 (45-6) μm at mid-body becoming smaller on tailUnder light microscope annuli becoming indistinct on calast third of tail making it difficult to count number of an-nuli SEM showing minute annuli continuing to tail tipVulva a transverse slit with slightly overhanging anteriorlip Vagina slightly sigmoid Oval spermatheca presentfilled with rounded sperm cells Tail tapering becomingfiliform with a finely rounded tip

Male

Body slightly arcuate ventrad more so in last quarterLip region rounded with three annuli with a distinct labialdisc Labial framework distinct Stylet absent and pharynxdegenerate Excretory pore distinct Annuli smooth 3 μmwide at mid-body Lateral field not observed Bursa dis-tinct ca 45 anal body diam or 79 μm long starting oppo-site basal tip of spicules and extending to about middle oftail distinctly annulated margin crenate Spicules almoststraight with proximal part slightly curved ventrad Gu-bernaculum indistinct Tail tapering gradually to a finelyrounded tip annuli distinct to end of bursa after whichthey become smaller and more indistinct towards tail tip

MOLECULAR CHARACTERISATION AND

PHYLOGENETIC RELATIONSHIPS OF CALOOSIA

LONGICAUDATA

Amplification of the ITS-rRNA gene from a C longi-caudata sample yielded a single fragment of ca 800 bp inlength The PCR-ITS-RFLP diagnostic profile for C long-icaudata generated by six restriction enzymes is given inFigure 4 with approximate sizes of the fragments as fol-lows AvaI 800 bp (not restricted) Bsh1236I 306 494 bpDraI 800 bp (not restricted) HinfI 284 516 bp Hin6I291 509 bp and MspI 395 405 bp

Alignment of the D2-D3 of 28S rRNA gene includes35 sequences was 587 bp in the length and contained325 parsimony informative characters The phylogenetictree reconstructed by the BI method is presented in Figure5 Caloosia longicaudata clustered with representativesof the genus Criconemoides Taylor 1936 Alignment ofpartial 18S rRNA gene includes 19 sequences was 807bp in the length and contained 168 parsimony informa-tive characters The phylogenetic tree reconstructed by theML method is presented in Figure 6A Caloosia longicau-data clustered with representatives of the genera Crico-nemoides and Hemicycliophora Alignment of ITS rRNA

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Fig 1 Caloosia longicaudata Female A Anterior region B Lip lateral view C Vulva and anus ventral view D Vulval area lateralview E Tail F Spermatheca G Annuli at mid-body Male H Anterior region I Posterior region (Scale bar = 20 μm)

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Fig 2 Caloosia longicaudata Female and male light microscope photographs A Body posture B Female lip region C Male lipregion D Male posterior region E Female anterior region F Vulva ventral G Vulva lateral H Female tail region The scalebar for D and B-H is the same

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Fig 3 Caloosia longicaudata Female A Anterior regionlateral view B C En face views D Annuli at mid-body EVulva ventral view F Vulva lateral view G Posterior part oftail H Post-vulval region

gene includes 19 sequences and after excluding ambigu-ously aligned regions reached 364 bp in length and con-tained 168 parsimony informative characters The phylo-genetic tree for the ITS-rRNA reconstructed by the ML

method is given in Figure 6B The position of C longi-caudata within Criconematina was not resolved Topolo-gies of the trees reconstructed by different methods forcorresponding genes were congruent and differed in po-sitions of some poorly supported clades The SH testsof these three sequence datasets could not reject a sis-ter relationship of C longicaudata with Hemicycliophoraspecies (P = 009 02 02 respectively) where repre-sentatives of these genera formed a clade Thus the posi-tion of C longicaudata is still not well resolved withinCriconematina and the rRNA sequence datasets cannotambiguously support either of the relationship hypothesesproposed by Siddiqi (1980 2000) or Ganguly and Khan(1983)

TAXONOMY OF CALOOSIA

Siddiqi (2000) listed ten species in Caloosia viz Clongicaudata (Loos 1948) Siddiqi amp Goodey 1963 astype species as well as C brevicaudata Khan Chawla ampSahu 1979 C exilis Mathur Khan Nand amp Prasad 1969C paralongicaudata Siddiqi amp Goodey 1963 C parlonaKhan Chawla amp Sahu 1979 C paxi Mathur Khan Nandamp Prasad 1969 C peculiaris Van den Berg amp Meyer1991 C psidii Ghambir amp Dhanachand 1997 C shoraiGhambir amp Dhanachand 1997 and C triannulata Rayamp Das 1981 Caloosia exigua Van den Berg Maraisamp Tiedt 2003 and C langola Pramodini Mohilal ampGambhir 2007 (langolus in original description should bea female noun thus langola) were added later Khera andChaturvedi (1977) discussed the close relationship of Cparalongicaudata with C longicaudata and subsequentlysynonymised C paralongicaudata with C longicaudataTheir decision is accepted here

When studying the article of Gambhir and Dhanachand(1997) it is clear that the species psidii actually belongs toHemicaloosia not Caloosia as it corresponds well withthe diagnosis of the former genus in such characters ashaving a lip region continuous with the body contour asheath closely adpressed to the cuticle and two incisuresin the lateral field When comparing the characters of thefour females identified for each of H psidii and C shoraifrom the article (Table 2) it is clear that they are very simi-lar According to the illustrations of Gambhir and Dhanac-hand (1997) the two species appear almost identical in lipregion pharynx tail and cuticle No illustration is givenfor the mid-body annuli of C shorai but the lateral field isdescribed as being indistinct Brzeski (1974) in describ-ing H nudata (Colbran 1963) Brzeski 1974 stated thatthe breaks in striae characterising this species were not al-

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Fig 1 Caloosia longicaudata Female A Anterior region B Lip lateral view C Vulva and anus ventral view D Vulval area lateralview E Tail F Spermatheca G Annuli at mid-body Male H Anterior region I Posterior region (Scale bar = 20 μm)

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Fig 2 Caloosia longicaudata Female and male light microscope photographs A Body posture B Female lip region C Male lipregion D Male posterior region E Female anterior region F Vulva ventral G Vulva lateral H Female tail region The scalebar for D and B-H is the same

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Fig 3 Caloosia longicaudata Female A Anterior regionlateral view B C En face views D Annuli at mid-body EVulva ventral view F Vulva lateral view G Posterior part oftail H Post-vulval region

gene includes 19 sequences and after excluding ambigu-ously aligned regions reached 364 bp in length and con-tained 168 parsimony informative characters The phylo-genetic tree for the ITS-rRNA reconstructed by the ML

method is given in Figure 6B The position of C longi-caudata within Criconematina was not resolved Topolo-gies of the trees reconstructed by different methods forcorresponding genes were congruent and differed in po-sitions of some poorly supported clades The SH testsof these three sequence datasets could not reject a sis-ter relationship of C longicaudata with Hemicycliophoraspecies (P = 009 02 02 respectively) where repre-sentatives of these genera formed a clade Thus the posi-tion of C longicaudata is still not well resolved withinCriconematina and the rRNA sequence datasets cannotambiguously support either of the relationship hypothesesproposed by Siddiqi (1980 2000) or Ganguly and Khan(1983)

TAXONOMY OF CALOOSIA

Siddiqi (2000) listed ten species in Caloosia viz Clongicaudata (Loos 1948) Siddiqi amp Goodey 1963 astype species as well as C brevicaudata Khan Chawla ampSahu 1979 C exilis Mathur Khan Nand amp Prasad 1969C paralongicaudata Siddiqi amp Goodey 1963 C parlonaKhan Chawla amp Sahu 1979 C paxi Mathur Khan Nandamp Prasad 1969 C peculiaris Van den Berg amp Meyer1991 C psidii Ghambir amp Dhanachand 1997 C shoraiGhambir amp Dhanachand 1997 and C triannulata Rayamp Das 1981 Caloosia exigua Van den Berg Maraisamp Tiedt 2003 and C langola Pramodini Mohilal ampGambhir 2007 (langolus in original description should bea female noun thus langola) were added later Khera andChaturvedi (1977) discussed the close relationship of Cparalongicaudata with C longicaudata and subsequentlysynonymised C paralongicaudata with C longicaudataTheir decision is accepted here

When studying the article of Gambhir and Dhanachand(1997) it is clear that the species psidii actually belongs toHemicaloosia not Caloosia as it corresponds well withthe diagnosis of the former genus in such characters ashaving a lip region continuous with the body contour asheath closely adpressed to the cuticle and two incisuresin the lateral field When comparing the characters of thefour females identified for each of H psidii and C shoraifrom the article (Table 2) it is clear that they are very simi-lar According to the illustrations of Gambhir and Dhanac-hand (1997) the two species appear almost identical in lipregion pharynx tail and cuticle No illustration is givenfor the mid-body annuli of C shorai but the lateral field isdescribed as being indistinct Brzeski (1974) in describ-ing H nudata (Colbran 1963) Brzeski 1974 stated thatthe breaks in striae characterising this species were not al-

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Fig 2 Caloosia longicaudata Female and male light microscope photographs A Body posture B Female lip region C Male lipregion D Male posterior region E Female anterior region F Vulva ventral G Vulva lateral H Female tail region The scalebar for D and B-H is the same

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Fig 3 Caloosia longicaudata Female A Anterior regionlateral view B C En face views D Annuli at mid-body EVulva ventral view F Vulva lateral view G Posterior part oftail H Post-vulval region

gene includes 19 sequences and after excluding ambigu-ously aligned regions reached 364 bp in length and con-tained 168 parsimony informative characters The phylo-genetic tree for the ITS-rRNA reconstructed by the ML

method is given in Figure 6B The position of C longi-caudata within Criconematina was not resolved Topolo-gies of the trees reconstructed by different methods forcorresponding genes were congruent and differed in po-sitions of some poorly supported clades The SH testsof these three sequence datasets could not reject a sis-ter relationship of C longicaudata with Hemicycliophoraspecies (P = 009 02 02 respectively) where repre-sentatives of these genera formed a clade Thus the posi-tion of C longicaudata is still not well resolved withinCriconematina and the rRNA sequence datasets cannotambiguously support either of the relationship hypothesesproposed by Siddiqi (1980 2000) or Ganguly and Khan(1983)

TAXONOMY OF CALOOSIA

Siddiqi (2000) listed ten species in Caloosia viz Clongicaudata (Loos 1948) Siddiqi amp Goodey 1963 astype species as well as C brevicaudata Khan Chawla ampSahu 1979 C exilis Mathur Khan Nand amp Prasad 1969C paralongicaudata Siddiqi amp Goodey 1963 C parlonaKhan Chawla amp Sahu 1979 C paxi Mathur Khan Nandamp Prasad 1969 C peculiaris Van den Berg amp Meyer1991 C psidii Ghambir amp Dhanachand 1997 C shoraiGhambir amp Dhanachand 1997 and C triannulata Rayamp Das 1981 Caloosia exigua Van den Berg Maraisamp Tiedt 2003 and C langola Pramodini Mohilal ampGambhir 2007 (langolus in original description should bea female noun thus langola) were added later Khera andChaturvedi (1977) discussed the close relationship of Cparalongicaudata with C longicaudata and subsequentlysynonymised C paralongicaudata with C longicaudataTheir decision is accepted here

When studying the article of Gambhir and Dhanachand(1997) it is clear that the species psidii actually belongs toHemicaloosia not Caloosia as it corresponds well withthe diagnosis of the former genus in such characters ashaving a lip region continuous with the body contour asheath closely adpressed to the cuticle and two incisuresin the lateral field When comparing the characters of thefour females identified for each of H psidii and C shoraifrom the article (Table 2) it is clear that they are very simi-lar According to the illustrations of Gambhir and Dhanac-hand (1997) the two species appear almost identical in lipregion pharynx tail and cuticle No illustration is givenfor the mid-body annuli of C shorai but the lateral field isdescribed as being indistinct Brzeski (1974) in describ-ing H nudata (Colbran 1963) Brzeski 1974 stated thatthe breaks in striae characterising this species were not al-

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Fig 3 Caloosia longicaudata Female A Anterior regionlateral view B C En face views D Annuli at mid-body EVulva ventral view F Vulva lateral view G Posterior part oftail H Post-vulval region

gene includes 19 sequences and after excluding ambigu-ously aligned regions reached 364 bp in length and con-tained 168 parsimony informative characters The phylo-genetic tree for the ITS-rRNA reconstructed by the ML

method is given in Figure 6B The position of C longi-caudata within Criconematina was not resolved Topolo-gies of the trees reconstructed by different methods forcorresponding genes were congruent and differed in po-sitions of some poorly supported clades The SH testsof these three sequence datasets could not reject a sis-ter relationship of C longicaudata with Hemicycliophoraspecies (P = 009 02 02 respectively) where repre-sentatives of these genera formed a clade Thus the posi-tion of C longicaudata is still not well resolved withinCriconematina and the rRNA sequence datasets cannotambiguously support either of the relationship hypothesesproposed by Siddiqi (1980 2000) or Ganguly and Khan(1983)

TAXONOMY OF CALOOSIA

Siddiqi (2000) listed ten species in Caloosia viz Clongicaudata (Loos 1948) Siddiqi amp Goodey 1963 astype species as well as C brevicaudata Khan Chawla ampSahu 1979 C exilis Mathur Khan Nand amp Prasad 1969C paralongicaudata Siddiqi amp Goodey 1963 C parlonaKhan Chawla amp Sahu 1979 C paxi Mathur Khan Nandamp Prasad 1969 C peculiaris Van den Berg amp Meyer1991 C psidii Ghambir amp Dhanachand 1997 C shoraiGhambir amp Dhanachand 1997 and C triannulata Rayamp Das 1981 Caloosia exigua Van den Berg Maraisamp Tiedt 2003 and C langola Pramodini Mohilal ampGambhir 2007 (langolus in original description should bea female noun thus langola) were added later Khera andChaturvedi (1977) discussed the close relationship of Cparalongicaudata with C longicaudata and subsequentlysynonymised C paralongicaudata with C longicaudataTheir decision is accepted here

When studying the article of Gambhir and Dhanachand(1997) it is clear that the species psidii actually belongs toHemicaloosia not Caloosia as it corresponds well withthe diagnosis of the former genus in such characters ashaving a lip region continuous with the body contour asheath closely adpressed to the cuticle and two incisuresin the lateral field When comparing the characters of thefour females identified for each of H psidii and C shoraifrom the article (Table 2) it is clear that they are very simi-lar According to the illustrations of Gambhir and Dhanac-hand (1997) the two species appear almost identical in lipregion pharynx tail and cuticle No illustration is givenfor the mid-body annuli of C shorai but the lateral field isdescribed as being indistinct Brzeski (1974) in describ-ing H nudata (Colbran 1963) Brzeski 1974 stated thatthe breaks in striae characterising this species were not al-

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Table 1 Morphometrics of Caloosia longicaudata from the Hawaiian islands All measurements are in μm and in the form mean plusmnsd (range)

Female Male

n 21 1L 943 plusmn 1052 (804-1098) 786 (735-821) (n = 3)

a 249 plusmn 2 (225-273) 311b 69 plusmn 04 (65-75) 52c 53 plusmn 03 (5-57) 84o 95 plusmn 23 (74-119) ndashV 75 plusmn 19 (72-80) ndashOV 51 plusmn 151 (38-755) ndashStylet length 73 plusmn 51 (65-83) ndashMetenchium length 55 plusmn 58 (46-625) ndashTelenchium length 16 plusmn 17 (135-185) ndashm 781 plusmn 19 (749-803) ndashStylet knob height 35 plusmn 05 (3-45) ndashStylet knob width 6 plusmn 04 (6-65) ndashLip region height 8 plusmn 05 (75-9) 55First lip annulus diam 145 plusmn 17 (12-17) ndashSecond lip annulus diam 16 plusmn 13 (155-17) ndashFirst body annulus diam 175 plusmn 11 (16-19) ndashSecond body annulus diam 195 plusmn 1 (185-21) ndashThird body annulus diam 21 plusmn 11 (19-22) ndashPharynx length 139 plusmn 107 (122-156) 154Anterior end to median bulb 95 plusmn 52 (86-103) ndashExcretory pore 140 plusmn 133 (118-173) 146Mid-body diam 33 plusmn 46 (295-48) 24Anal body diam 23 plusmn 13 (22-24) 175Vulva-anus distance (VA) 63 plusmn 115 (375-785) ndashSpermatheca length 21 plusmn 1 (19-215) ndashSpermatheca width 145 plusmn 21 (125-175) ndashTail (T) 172 plusmn 144 (147-191) 90R 205 plusmn 103 (190-222) ndashRSt 16 plusmn 13 (14-18) ndashROes 29 plusmn 21 (25-33) ndashRex 31 plusmn 13 (29-33) ndashRhem 29-30 (n = 2) ndashRV 70 plusmn 125 (50-90) ndashRVan 12 plusmn 22 (7-15) ndashRan 59 plusmn 14 (37-79) ndashPVanal body diam 98 plusmn 06 (92-109) ndashTailanal body diam 75 plusmn 04 (69-79) ndashVA (T) 314 plusmn 68 (288-388) ndashVLVB 76 plusmn 14 (53-10) ndashSt (L) 77 plusmn 06 (69-88) ndashLip region diam ndash 8Spicules ndash 37 (36-39) (n = 3)

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Fig 4 Diagnostic PCR-ITS rRNA-RFLP profile for Caloosialongicaudata Code M = 100 bp DNA marker (Promega)U = unrestricted PCR product 1 = AvaI 2 = Bsh1236I3 = DraI 4 = HinfI 5 = Hin6I 6 = MspI

ways visible in all females Also in the form of the lipregion C shorai does not fit the diagnosis of CaloosiaAs they are so similar we regard C shorai as belongingto the genus Hemicaloosia and then as a synonym of Hpsidii Caloosia langola is described as having a sheathand two lines in the lateral field and also clearly belongsto Hemicaloosia It is herein transferred to that genus asHemicaloosia langola (Pramodini Mohilal amp Gambhir2007) n comb

We now regard Caloosia as having eight species InTable 3 the present specimens from the Hawaiian Islandsare compared with these eight species the measurementsof our specimens being the closest to those for Clongicaudata It can also be seen that some of thesespecies are very close to each other Unfortunately someof the nominal species are very poorly described withvery little information available and we believe that withfurther detailed morphological and molecular studiessome of these species will be synonymised

BIOGEOGRAPHY OF CALOOSIA

Caloosia was considered to be native to the south-eastern states of India and some adjoining countriessuch as Sri Lanka and Bangladesh (Ganguly amp Khan1983) However a description of C exigua from SouthAfrica (Van den Berg et al 2003) and reports of Clongicaudata from Fiji (Bridge 1988) and Maui (presentdata) expanded our knowledge of the distribution ofCaloosia and indicate its occurrence in Indo-African andPolynesian biogeographical regions

Acknowledgements

Mrs NH Buckley is thanked for technical assistanceand Mrs Elsa van Niekerk for scanning the illustrationsSAS acknowledges support from the NSF grant PEETDEB 0731516

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CHEN DY NI HF YEN JH amp TSAY TT (2007)[Identification of Hemicriconemoides karayaensis and Hcalifornianus (Nematoda Criconematoidea Criconematidae)among tea plantations in Taiwan] Plant Pathology Bulletin16 181-192

CHEN DY NI HF TSAY TT amp YEN JH (2008a)[Identification of Gracilacus bilineata and G aculenta (Ne-matoda Criconematoidea Tylenchida)] Plant PathologyBulletin 17 209-220

CHEN DY NI HF TSAY TT amp YEN JH (2008b)[Identification of a new recorded sheath nematode Hemi-criconemoides parasinensis (Nematoda CriconematoideaTylenchida)] Plant Pathology Bulletin 17 315-320

CHEN DY NI HF YEN JH amp TSAY TT (2009) [Iden-tification of a new recorded pin nematode Paratylenchusminutus (Nematoda Criconematoidea Tylenchulidae) in Tai-wan] Plant Pathology Bulletin 18 167-174

CHIZHOV VN CHUMAKOVA OA SUBBOTIN SA ampBALDWIN JG (2006) Morphological and molecular char-acterization of foliar nematodes of the genus AphelenchoidesA fragariae and A ritzemabosi (Nematoda Aphelenchoi-didae) from the Main Botanical Garden of the Russian Acad-emy of Sciences Moscow Russian Journal of Nematology14 179-184

COLBRAN RC (1963) Studies of plant and soil nematodes 6Two new species from citrus orchards Queensland Journalof Agricultural Sciences 20 469-474

DE GRISSE A (1969) Redescription ou modification dequelques techniques utiliseacutees dans lrsquoeacutetude des nematodes

388 Nematology

E van den Berg et al

Fig 4 Diagnostic PCR-ITS rRNA-RFLP profile for Caloosialongicaudata Code M = 100 bp DNA marker (Promega)U = unrestricted PCR product 1 = AvaI 2 = Bsh1236I3 = DraI 4 = HinfI 5 = Hin6I 6 = MspI

ways visible in all females Also in the form of the lipregion C shorai does not fit the diagnosis of CaloosiaAs they are so similar we regard C shorai as belongingto the genus Hemicaloosia and then as a synonym of Hpsidii Caloosia langola is described as having a sheathand two lines in the lateral field and also clearly belongsto Hemicaloosia It is herein transferred to that genus asHemicaloosia langola (Pramodini Mohilal amp Gambhir2007) n comb

We now regard Caloosia as having eight species InTable 3 the present specimens from the Hawaiian Islandsare compared with these eight species the measurementsof our specimens being the closest to those for Clongicaudata It can also be seen that some of thesespecies are very close to each other Unfortunately someof the nominal species are very poorly described withvery little information available and we believe that withfurther detailed morphological and molecular studiessome of these species will be synonymised

BIOGEOGRAPHY OF CALOOSIA

Caloosia was considered to be native to the south-eastern states of India and some adjoining countriessuch as Sri Lanka and Bangladesh (Ganguly amp Khan1983) However a description of C exigua from SouthAfrica (Van den Berg et al 2003) and reports of Clongicaudata from Fiji (Bridge 1988) and Maui (presentdata) expanded our knowledge of the distribution ofCaloosia and indicate its occurrence in Indo-African andPolynesian biogeographical regions

Acknowledgements

Mrs NH Buckley is thanked for technical assistanceand Mrs Elsa van Niekerk for scanning the illustrationsSAS acknowledges support from the NSF grant PEETDEB 0731516

References

BERT W LELIAERT F VIERSTRAETE AR VAN-FLETEREN JR amp BORGONIE G (2008) Molecular phy-logeny of the Tylenchina and evolution of the female gon-oduct (Nematoda Rhabditida) Molecular Phylogenetics andEvolution 48 728-744

BRIDGE J (1988) Plant-parasitic nematode problems in thePacific Islands Journal of Nematology 20 173-183

BRZESKI MW (1974) Taxonomy of Hemicycliophorinae(Nematoda Tylenchida) Zeszyty Problemowa PosteacutepowNauk Rolnizych 154 237-330

CHAWLA ML amp SAMATHANAM GJ (1980) Three newspecies of the superfamily Criconematoidea (TylenchidaNematoda) from Tamil Nadu (India) Indian Journal ofNematology 10 59-68

CHEN DY NI HF YEN JH amp TSAY TT (2007)[Identification of Hemicriconemoides karayaensis and Hcalifornianus (Nematoda Criconematoidea Criconematidae)among tea plantations in Taiwan] Plant Pathology Bulletin16 181-192

CHEN DY NI HF TSAY TT amp YEN JH (2008a)[Identification of Gracilacus bilineata and G aculenta (Ne-matoda Criconematoidea Tylenchida)] Plant PathologyBulletin 17 209-220

CHEN DY NI HF TSAY TT amp YEN JH (2008b)[Identification of a new recorded sheath nematode Hemi-criconemoides parasinensis (Nematoda CriconematoideaTylenchida)] Plant Pathology Bulletin 17 315-320

CHEN DY NI HF YEN JH amp TSAY TT (2009) [Iden-tification of a new recorded pin nematode Paratylenchusminutus (Nematoda Criconematoidea Tylenchulidae) in Tai-wan] Plant Pathology Bulletin 18 167-174

CHIZHOV VN CHUMAKOVA OA SUBBOTIN SA ampBALDWIN JG (2006) Morphological and molecular char-acterization of foliar nematodes of the genus AphelenchoidesA fragariae and A ritzemabosi (Nematoda Aphelenchoi-didae) from the Main Botanical Garden of the Russian Acad-emy of Sciences Moscow Russian Journal of Nematology14 179-184

COLBRAN RC (1963) Studies of plant and soil nematodes 6Two new species from citrus orchards Queensland Journalof Agricultural Sciences 20 469-474

DE GRISSE A (1969) Redescription ou modification dequelques techniques utiliseacutees dans lrsquoeacutetude des nematodes

388 Nematology

Studies on Caloosia longicaudata

Fig 5 Phylogenetic relationships of Caloosia longicaudata with other representatives of the suborder Criconematina as inferred fromBayesian analyses of sequences of the D2-D3 of 28S rRNA using GTR + I + G model of DNA evolution Posterior probability valuesmore than 70 are given on appropriate clades The newly obtained sequence is indicated in bold

Vol 13(4) 2011 389

E van den Berg et al

Fig 6 Phylogenetic relationships of Caloosia longicaudata with other representatives of the suborder Criconematina as inferred frommaximum likelihood analyses of sequences for the partial 18S rRNA (A) and partial ITS1-58S rRNA-ITS2 (B) genes Bootstrap valuesmore than 70 are given on appropriate clades The newly obtained sequence is indicated in bold

phytoparasitaires Mededelingen van de Rijksfaculteit derLandbouwwetenschappen Gent 34 251-369

DECRAEMER W amp HUNT DJ (2006) Structure and classifi-cation In Perry RN amp Moens M (Eds) Plant nematologyWallingford UK CABI Publishing pp 3-32

EROSHENKO AS (1976) [Parasitic root nematodes familyHemicycliophoridae] Leningrad USSR Nauka 80 pp

GAMBHIR RK amp DHANACHAND C (1997) Nematodesof fruit plants in Manipur ndash five new species of tylenchids(Nematoda Tylenchida) Indian Journal of Nematology 26(1996) 197-207

GANGULY S amp KHAN E (1983) Revision of the genusCaloosia Siddiqi amp Goodey 1963 (Caloosiidae Nematoda)Indian Journal of Nematology 13 181-198

HOLTERMAN M KARSSEN G VAN DEN ELSEN S VAN

MEGEN H BAKKER J amp HELDER J (2009) Smallsubunit rDNA-based phylogeny of the tylenchids sheds lighton relationships among some high impact plant-parasiticnematodes and the evolution of plant feeding Phytopathology99 227-235

HUELSENBECK JP amp RONQUIST F (2001) MrBAYESBayesian inference of phylogenetic trees Bioinformatics 17754-755

KHAN E CHAWLA ML amp SAHU SC (1979) Caloosiaparlona n sp from soil around roots of rice and C brevicau-data n sp (Nematoda Hemicycliophoridae) from soil aroundroots of Citrus from Orissa India Nematologica 25 362-367

KHERA S amp CHATURVEDI Y (1977) Systematic statusof Caloosia paralongicaudata Siddiqi amp Goodey 1963(Criconematidae Nematoda) Indian Journal of Helminthol-ogy 1 79-83

LOOS CA (1948) Notes on free-living and plant-parasiticnematodes of Ceylon 3 Ceylon Journal of Science 23 119-124

MATHUR VK KHAN E NAND S amp PRASAD SK(1969) Two new species of Caloosia Siddiqi amp Goodey(Nematoda Hemicycliophoridae) from India Bulletin ofEntomology 10 27-31

NYLANDER JAA (2002) MrModeltest v10b Dept ofSystematic Zoology Uppsala University Available athttpwwwebcuusesystzoostaffnylanderhtml

390 Nematology

E van den Berg et al

Fig 6 Phylogenetic relationships of Caloosia longicaudata with other representatives of the suborder Criconematina as inferred frommaximum likelihood analyses of sequences for the partial 18S rRNA (A) and partial ITS1-58S rRNA-ITS2 (B) genes Bootstrap valuesmore than 70 are given on appropriate clades The newly obtained sequence is indicated in bold

phytoparasitaires Mededelingen van de Rijksfaculteit derLandbouwwetenschappen Gent 34 251-369

DECRAEMER W amp HUNT DJ (2006) Structure and classifi-cation In Perry RN amp Moens M (Eds) Plant nematologyWallingford UK CABI Publishing pp 3-32

EROSHENKO AS (1976) [Parasitic root nematodes familyHemicycliophoridae] Leningrad USSR Nauka 80 pp

GAMBHIR RK amp DHANACHAND C (1997) Nematodesof fruit plants in Manipur ndash five new species of tylenchids(Nematoda Tylenchida) Indian Journal of Nematology 26(1996) 197-207

GANGULY S amp KHAN E (1983) Revision of the genusCaloosia Siddiqi amp Goodey 1963 (Caloosiidae Nematoda)Indian Journal of Nematology 13 181-198

HOLTERMAN M KARSSEN G VAN DEN ELSEN S VAN

MEGEN H BAKKER J amp HELDER J (2009) Smallsubunit rDNA-based phylogeny of the tylenchids sheds lighton relationships among some high impact plant-parasiticnematodes and the evolution of plant feeding Phytopathology99 227-235

HUELSENBECK JP amp RONQUIST F (2001) MrBAYESBayesian inference of phylogenetic trees Bioinformatics 17754-755

KHAN E CHAWLA ML amp SAHU SC (1979) Caloosiaparlona n sp from soil around roots of rice and C brevicau-data n sp (Nematoda Hemicycliophoridae) from soil aroundroots of Citrus from Orissa India Nematologica 25 362-367

KHERA S amp CHATURVEDI Y (1977) Systematic statusof Caloosia paralongicaudata Siddiqi amp Goodey 1963(Criconematidae Nematoda) Indian Journal of Helminthol-ogy 1 79-83

LOOS CA (1948) Notes on free-living and plant-parasiticnematodes of Ceylon 3 Ceylon Journal of Science 23 119-124

MATHUR VK KHAN E NAND S amp PRASAD SK(1969) Two new species of Caloosia Siddiqi amp Goodey(Nematoda Hemicycliophoridae) from India Bulletin ofEntomology 10 27-31

NYLANDER JAA (2002) MrModeltest v10b Dept ofSystematic Zoology Uppsala University Available athttpwwwebcuusesystzoostaffnylanderhtml

390 Nematology

Studies on Caloosia longicaudata

Table 2 Comparison of female Hemicaloosia psidii and Caloosia shorai from original descriptions (Gambhir amp Dhanachand 1997)All measurements are in μm

Character H psidii C shorai

n 4 4L 570-740 560-730a 23-36 27-32b 51-65 54-57c 7-10 6-13cprime 49-64 38-49V 78 80-84VLVB Not given 54 calculated from

illustration6

R 237-266 212-253Rex 45 42-43 (value given in measurements but in

text it says excretory pore not clearly seen)RVan 20-22 17-18Ran 19-23 ( until becoming indistinct

on tail)34-41

RV 217 Not givenStylet length 48-58 46-58Stylet knob width 32 Not givenStylet knob height 16 Not givenSt (L) Not given 7-8DGO 48 48Mid-body diam 23-36 Not givenExcretory pore 1264 Excretory pore not seen but Rex value is

givenLateral field Two incisures illustrated Lines not distinct no illustration given of

mid-body annuliLip region configuration Continuous with body contour with

two annuli diam not givenTwo lip annuli continuous with body con-tour 1st 8-11 2nd 9-13

Vulva from anterior end Not given 6149Tail length 77 calculated from figure 564-864

PRAMODINI M MOHILAL N amp GAMBHIR RK (2007)Criconemella lobella sp n and Caloosia langolus sp n fromlemon plants of Manipur Flora and Fauna 13 433-438

RAY S amp DAS SN (1981) Two new and four knownspecies in the family Hemicycliophoridae (CriconematoideaNematoda) from Orissa India Indian Journal of Nematology10 (1980) 141-147

SIDDIQI MR (1961) Studies on species of Criconematinae(Nematoda Tylenchida) from India Proceedings of theHelminthological Society of Washington 28 19-34

SIDDIQI MR (1980) Taxonomy of the plant nematode su-perfamily Hemicycliophoroidea with a proposal for Cricone-matina new suborder Revue de Neacutematologie 3 179-199

SIDDIQI MR (2000) Tylenchida parasites of plants andinsects 2nd edition Wallingford UK CABI Publishing 833pp

SIDDIQI MR amp GOODEY JB (1963) The status of the

genera and subfamilies of the Criconematidae (Nematoda)

with a comment on the position of Fergusobia Nematologica

9 363-377

SUBBOTIN SA VOVLAS N CROZZOLI R STURHAN

D LAMBERTI F MOENS M amp BALDWIN JG (2005)

Phylogeny of Criconematina Siddiqi 1980 (Nematoda Ty-

lenchida) based on morphology and D2-D3 expansion seg-

ments of the 28S-rRNA gene sequences with application of a

secondary structure model Nematology 7 927-944

SUBBOTIN SA STURHAN D CHIZHOV VN VOVLAS

N amp BALDWIN JG (2006) Phylogenetic analysis of Ty-

lenchida Thorne 1949 as inferred from D2 and D3 expansion

fragments of the 28S rRNA gene sequences Nematology 8

455-474

Vol 13(4) 2011 391

E van den Berg et al

Tabl

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Cb

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Cp

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naC

pax

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pec

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ris

Ct

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nula

taM

aui

Haw

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(1)

(2)

(3)

(4)

(5)

(6)

(7)

(8)

(ori

gina

l)Fe

mal

eL

804-

1098

740-

1100

825-

1185

404-

617

1040

-164

075

0-13

0058

0-93

056

5-69

910

46-1

175

a22

5-2

73

25-3

319

1-2

516

9-2

11

31-4

217

-30

419

-39

145

-22

733

-42

c5-

57

45-

57

92-

1111

1-1

68

4-6

4-7

55-

67

63-

104

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5V

72-8

071

-77

80-8

688

-91

64-8

065

-82

72-8

084

-89

69-7

3R

190-

222

190-

237

197-

205

173-

190

231-

300

202-

280

190-

210

141-

172

211-

241

(RN

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14-1

8ndash

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28-3

326

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235

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724

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No

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athu

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al(

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)G

angu

lyamp

Kha

n(1

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(7)

Van

den

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Mey

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as(1

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a

No

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for

R

bK

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ampC

hatu

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repo

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only

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angu

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men

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orth

ree

annu

lim

aybe

pres

ent

392 Nematology

Studies on Caloosia longicaudata

SWOFFORD DL (2003) PAUP phylogenetic analysis us-ing parsimony (and other methods) version 40b10 Sun-derland MA USA Sinauer Associates

TANHA MAAFI Z SUBBOTIN SA amp MOENS M (2003)Molecular identification of cyst-forming nematodes (Het-eroderidae) from Iran and a phylogeny based on the ITS se-quences of rDNA Nematology 5 99-111

TARJAN AC (1952) The nematode genus Hemicycliophorade Man 1921 (Criconematidae) with a description of a newplant-parasitic species Proceedings of the HelminthologicalSociety of Washington 19 65-77

VAN DEN BERG E amp MEYER AJ (1991) Four newnematode species from the Cederberg Cape Province South

Africa (Criconematidae Nemata) Phytophylactica 23 37-45

VAN DEN BERG E MARAIS M amp TIEDT LR (2003)Plant nematodes in South Africa 5 Plant nematodes fromthe Gouekrans area of the Swartberg Nature Reserve withdescriptions of one new and one known Hemicycliophorinae(Nemata) African Plant Protection 9 43-52

VAN DEN BERG E SUBBOTIN SA amp TIEDT LR (2010)Morphological and molecular characterisation of Hemicyclio-phora lutosa Loof amp Heyns 1969 and H typica de Man 1921from South Africa (Nematoda Hemicycliophoridae) Nema-tology 12 303-308

Vol 13(4) 2011 393

Studies on Caloosia longicaudata

SWOFFORD DL (2003) PAUP phylogenetic analysis us-ing parsimony (and other methods) version 40b10 Sun-derland MA USA Sinauer Associates

TANHA MAAFI Z SUBBOTIN SA amp MOENS M (2003)Molecular identification of cyst-forming nematodes (Het-eroderidae) from Iran and a phylogeny based on the ITS se-quences of rDNA Nematology 5 99-111

TARJAN AC (1952) The nematode genus Hemicycliophorade Man 1921 (Criconematidae) with a description of a newplant-parasitic species Proceedings of the HelminthologicalSociety of Washington 19 65-77

VAN DEN BERG E amp MEYER AJ (1991) Four newnematode species from the Cederberg Cape Province South

Africa (Criconematidae Nemata) Phytophylactica 23 37-45

VAN DEN BERG E MARAIS M amp TIEDT LR (2003)Plant nematodes in South Africa 5 Plant nematodes fromthe Gouekrans area of the Swartberg Nature Reserve withdescriptions of one new and one known Hemicycliophorinae(Nemata) African Plant Protection 9 43-52

VAN DEN BERG E SUBBOTIN SA amp TIEDT LR (2010)Morphological and molecular characterisation of Hemicyclio-phora lutosa Loof amp Heyns 1969 and H typica de Man 1921from South Africa (Nematoda Hemicycliophoridae) Nema-tology 12 303-308

Vol 13(4) 2011 393