Nematoda : Criconematidae)

Hemicriconemoides minor sp. n. with observations on .four other species of the genus (Nematoda : Criconematidae)

Michal W. BRZESKIand Françoise REAY I~z~tytut Warzywnictwa,96-100 Skierniewice, Poland and Plant Pathology Department, Waite Agricultural Research Institufe, University of Adelaide, Glen Osmond, South Australia, 5064.

SUMMARY Hemicriconemoides minor n. sp. is described from Australia. It is differentiated from H. taiwanensis Pinochet & Raski, 1975 by being smaller, with fewer annules, smaller stylet knobs and a slightly offset lip region. The male and two juveniles of H. obtusus Colbran 1962 are described. Additional information onH. nitidus Raski & Pinochet, 1975, H. mangiferae Siddiqi, 1961 and H. insignis Dasgupta, Raski & VanGundy, 1969 is given. Variation in juvenile scales and the retrorse annules of Hemicriconemoides are discussed.

RÉSUMÉ Hemicriconemoides minor n. sp. et observations sur quatre autres espdces du genre (Nematoda : Criconematidae) Hemicriconemoides minor n. sp. est décrit, provenant d’Australie ; il se différencie de H. taiwanensis Pinochet & Raski, 1975par la plus faible longueurdu corps, le nombremoins élevé d’anneaux, les boutons du styletmoins déve- loppés et larégion labiale quelque peu séparée du restedu corps. Le mâleet deux juvéniles appartenantà H. obtusus Colbran, 1962 sont décrits. Des données complémentaires sont fournies concernant H. nitidus Raski & Pinochet, 1975, H. mangiferae Siddiqi, 1961 et H. insignis Dasgupta, Raski & Van Gundy, 1969. Les variations concernant les écailles cuticulaires de juvéniles et la présence d’anneaux retrorses dans le genre Hemicriconemoides sont discutées.

The genus Hemicriconemoides occurs in most parts bygentle heat, then fixed with 2% formalin, or of the world, seven species havinp been recorded in relaxedand fixed in hotFA 4:l. They were then Australia(Khair, 1978). H. obtusus Colbran,1962, processed to glycerol byBaker’s method, or bya H. insignis Dasgupta,Raski , & VanGundy, 1967 method of slow evaporation of glycerol-ethanol at and H. minor sp. n. occur in bushland soils and can 400. Specimens were then mounted in pure glycerol. be considered as being native rather than introduced species. These exhibit some of the variability within the genus. H. obfusus isconsidered to be the most Hemicriconemoides minor sp. n. aberrant species (Dasgupta,Raski & VanGundy (Fig. 1A-G) 1969)and H. .minor sp. n. differs frommost other MEASUREMENTS species in having retrorse annules. Females (paratypes from Kuifpo Forest: n = 16) : L = 0.32 (0.29-0.37) mm ; a = 14 (12-15) ; b = 3.4 Materials and methods (2.8-4.4) ; c = 23 (19-27) ; V = 92 (91-94) ; Stylet = 63 (56-68) km ; m = 90 (87-95) ; VL/VB = 1.3 (1.2- Most of thenematode specimenswere collected 1.5) ; Rex = 37 (32-39) ; Rv = 12 (10-13) ; Rvan = during a study of plant parasite nematodes occuring 4 (2-5) ; Ran = 7 (6-8) ; R = 118 (112-125). in bushland soils in South Australia (Reay& Wallace, Holotype (female; Kuitpo Forest) : L = 0.34 mm ; 1982). Soi1 samples werecollected usjng a 5 cm a = 15 ; b = 3.3 ; c = 26 ; V = 92 ; Stylet = diameterauger to 40 cmdepth. Nematodes were 65 Fm ; m = 90 ; VL/VB = 1.5 ; Rex = 36 ; Rv = extracted by amodified Baerman’s technique, relaxed 135; Rvan = 5 ; Ran = 7 ; R = 117.

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Fig. 1. Hemicriconemoidesminor sp.n. A : female ; B : headand stylet ; C : oesophageal region ; D : posterior region of female ; E-G : variability of tail ; (Scale bars represent 20 Pm).

Females (paratypes from Kyeema; n = 16) : L = riorly ; insome paratypes these projections are 0.36 (0.32-0.42) mm ; a = 15 (13-16) ; b = 2.9 (2.7- barelydiscernible. Spermatheca filled withsperm. 3.1) ; c = 25 (19-29) ; V = 92 (91-94) ; Stylet = 70 Gonadstraight in most specimens seen, but some- (62-75)pm ; m = 89 (87-90) ; VL/VB = 1.4 ( 1.2- times recurved. Vulva open, no lateral vulval mem- 1.7) ; Rex = 39 (37-40) ; Rv = 12 (11-14) ; Rvan = branes. Tai1 endoften dorsally curved, tail tip 5 (4-7) ; Ran = 7 (5-9) ; R = 121 (113-128). variable. Males and juveniles: not found. DESCRIPTION

Pemale: Body of young females slightly ventrally TYPELOCALITY arcuate,older females horse-shoe shaped. Annules retrorse, margins sometimes slightly irregular, occa- Kuitpo Forest, adjacent to Meadows, 30 km south sionallytwo annules on the dorsal side merge to of Adelaide, South Australia.An established planting formone annule on the ventral side. Head with of Eucalyptusmaculata Hook,composed of some three, occasionally two,rounded annules, narrower maturetrees, approximately 45 years old and thanthe followingneck region. Head rounded in numerous saplings. E. maculata has been introduced outline.Stylet thin, straight or ventrallycurved. fromthe eastern states of Australiaand does not Styletknobs with small projections directed ante- occurin virgin South Australian forests. Shrub

328 Revue Nbmatol. 5 (2) : 327-334 (1982) I Hemicriconemoides minor sp. R. layerabsent. Ground species composed mostly of REMARKS nativeorchid species, including Pterostylis spp., Caladenia spp., and Acianthus caudatus R. Br. H. minor sp.n. was alsorecovered from other soils : i) forest soil, under Eucalyptusfasciculosa, near Cape Jervis, South Australia ; ii) Virgin Karri ADDITIONALLOCALITY MarriForest (Eucalyptusdiuersicolor FvM.,and E. calophylla R. Br.), south of Manjimup, Western IiyeemaConservation Park, east of Willunga, Australia ; iii) 'Tasmanianrainforest, (Eucalyptus 18 kmsouth, ofAdelaide, South Australia. This delegatensis R.T. Bak.), near the Hellyer river, 64 km reserveis an area of dense natural bushland, with south of Burnie, Tasmania ; iu) Eucalyptus camaldu- an average annual rainfall of 800-900 mm. Dominant lensis woodland,adjacent to theMurray river, in species are : Eucalyptus cosmophylla FvM., E. fasci- Sunraysia district of Victoria. The Tasmanian females crdosa FVM., and E. obliqua L'Herit.Understorey are similar to those fromKuitpo forest. The West species include Xanthorrhoea semiplana Fvm., Hakea Australian specimens. are also similar, except for a rostrata Fvm., es Meisn., H. ulicina R. Br., Acacia slightly longer stylet (67-69 Pm ; n = 3). The Victo- uerticillaia (L'Herjt) Willd., and A. myrtifolia (Sm). rian females are closest to those from Kyeema. Willd. Hemicriconemoides obtusus Colbran. 1962 (Fig. 2 & 3) TYPESPECIMENS A numberof specimens of H. obtusus were recovered Holotypeand seventeen paratypes in the PoliSh from South Australian soils, from several localities. Collection of Nematodes, Instytut Zoologii PAN, ul. They differin various measurements, including being Wilcza64, , Warszawa,Poland ; tenparatypes in longer, with a longer stylet but generallyfewer body Waite Agricultural Research Iristitute,Glen Osmond, annules.However, most characteristics agree with SouthAustralia 5064 ; 'six paratypesin Instytut the originaldescription and theredescription by Warzywnictwa, 96-100Skierniewice, Poland ; five Dasgupta, Raski and Van Gundy (1969). Two juve- paratypes in Plant Research Institute, Swan Street, nileswere also recovered' from aSouth Australian Burnley, Victoria 3121, Australia ; one paratype in locality,one J, withscaly annules and qthe other, each of the following collections : Laboratorium voor J, witha smooth cuticle. This difference between Nematologie,Binnenhaven 10, Wageningen, the juvenilestages issimilar tothat described for Netherlands ; Rijksuniversiteit Gent, Instituut voor H. chitruoodi Esser, 1960, byDasgupta, Raski and Dierkunde,Ledeganckstraat 35, Gent,Belgium ; VanGundy, (1969). Soi1 receivedfrom Western Nematology Department, Rothamsted Experimental Australiacontained a fewfemales and also four Station, Harpenden, England ; Nematology Division, male specimens which are described, being previously University of California,Davis, California95616, unrecorded. U.S.A. ; NematologyDivision, Indian Agricultural Research Institute, New Delhi 12, India. MEASUREMENTS

DIAGNOSIS Females(from South Australia; n = 16) : L = 0.61(0.51-0.68) mm ; a = 17 (15.1-19.4) ; b = 4.8 By having retrorse annules, H. minor sp. n., shows (3.7-5.3) ; c = 18.7(15.3-24.2) ; stylet = 69(63- some similarity to H. taimanensis Pinochet & Raski, 75) pm ; VL/VB = 2.3(1.8-2.7) ; V = 88 (86-89) ; 1975, but differs in being smaller, with fewer annules, R = 99 (92-111) ; Rex = 25 (22-27) ; Rv = 14 (13- a slightly offset head and smaller- stylet knobs. (H. 16) ; Rvan = 6 (5-7) ; Ran = 8 (7-9) ; m = 80 (78- 81) ; stylet knobs = 8.8 (7.5-9.6) pm in diameter. taimanensis: L '= 0.59-0.61 mm ; R = 146-158 ; Rv = 13-16 ; Rvan = 7-10 ; VL/VB = 2.0-2.3 ; Females(from Western Ausirulia; n = 2) : L = stylet knobs 9-11 Pm across). H:minor sp. n., differs 0.46-0.51 mm ; a = 14.9-16.6 ; b = 4.4-4.7 ; c = 19- from' H. californianus Pinochet & Raski,1975 and 20 ; stylet = 62-72 Pm ; VL/VB = 1.7-2.0 ; V = H. gaddi (Loos,1949) Chitwood & Birchfield,1957 89-91 ; R = 92-99 ; Rex = 23-25 ; Rv = 12-13 ; in having a'somewhat shorter stylet, retrorse annules Rvan = 5-6 ; Ran = 7 ; m = 79 ; stylet knobs = and labial disc not elevated. Information regarding 7.8-8.9 pm in diameter. H. gaddi was talcen from Dasgupta, Raski and Van Males (from Western Australia; n = 4) : L = 0.44 Gundy (1969). (0.41-0.47) mm ; a = 22 (20.7-22.8) ; c = 10.2 (9.7-

Revue Nèmaiol. 5 (2) : 327-334 (1982) 3B A

Fig. 2. Hemicriconemoides oblusus Colbran, 1962. In toto vicms. A : fourth stage juvenilc ; B : femalc ; C : male ; D : second stage juvenile ; (Scale bar represents 20 Pm).

330 Revue Némafol. 5 (2) : 327-334 (1982) Hemicriconemoides minor sp. n.

~ ~

10.9) ; T = 34 (30-36) ; R = 186.(161-199) ; Rex = androunded, continuous with body. No lateral 54 (50-57) ; Ran = 18 (17-29) ; Tail length = 43.5 field visible. (41-48) pm. Pre-adultfemale, juvenile st. 4: Bodyslightly Juvenile,si. 2 (fromMyponga, South Australia; curved ventrally, covered in scales. Scales retrorse, n = 1) : L = 0.222 mm ; a = 12.4 ; b = 2.9 ; c = roundedon their edges, and arranged in twelve 40.8;stylet = 35.7 Pm; R = 127;Rex = 40; rows. The scales appear to be as twelvescales on Ran = 5. each annule. Lip region similar to adult female. Juvenile, si. 4 (fromMyporzga, South Australia) L = 0.50 mm ; a = 12.5 ; b = 4.4 ; c = 31.0 ; stylet = 58.2 pm ; R = 110 ; Rex = 26 ; Rv = 11 ; LOCALITIES Rvan = 5 ; Ran = 6. TheSouth Australian female specimens were recovered from soils of five reserves southof AdeIaide andwere most common at MypongaConservation DESCRIPTION Park, an area of very low bushland with Eucalyptus obliqua and E. cosrnophylla co-dominant.The low Fernales: Thedistinctive lip region is similar to level of vegetation, only one metre high, is probably that described previously (Colbran, 1962 ; Dasgupta, dueto the extremely stony nature of the area. Raski & Van Gundy,1969). Also as previously H. obtusus also occurs at : Cox’s Scrub Conservation mentionedby the latter authors, the outer cuticle Park where Eucalyptuscosmophylla and E. fascicu- is thick and very close to the inner cuticle which is losa areco-dominant ; DeepCreek Conservation verythin. The annules are flattened, but may be Park, bushland of Eucalyptus obliqua; and forest of somewhatretrorse on the post-vulval region. Con- Eucalyptusbaxteri (Benth.)Maiden & Blakely ex flictingcomments by Dasgupta, Raski and Van Black at SpringMount Conservation Park. The Gundy (1969) andSiddiqi and Goodey(1963) can WesternAustralian specimens (female and male) beresolved, as thisappears to be anunreliable were recovered from virgin Kami forest (Eucalyptus characteristic. Of thesixteen South Australian diversicolor) south of Manjimup, Western Australia. females,six show slightly retrorse annules on the post-vulvalregion, in one female they areonly present on the tail, and the remaining nine females havepost-vulval annules which are not retrorse, Hemicriconemoides nitidus being similar to -the rest of the body. The Western Raski & Pinochet, 1975 Australian females displaysimilara variability. (Fig. 4A, B) Colbrandescribed four projections across thetail terminus of the inner cuticle. Most of Our specimens have one or two, occasionally three projections, but MEASUREMENTS not four. Although no males haveso far been recorded fromSouth Australian soils, roundedsperm were Fernales (n = 20). L = 0.43 (0.39-0.46) mm ; a = present in the spermathecae of al1 but one female. 15-16 ; b = 4.3 (4.0-4.6) ; c = 20 (17-24) ; V = 90 Males: Body ventrally curved when relaxed. Lip (89-91) ; stylet = 57 (54-63) pm ; m = 83 (81-85) ; region somewhat truncate, continuous with the body VL/VB = 1.9(1.6-2.1) ; Rex’= 27(25-29) ; Rv = and finely annulated. Seven lip annules are present 11 (10-13) ; Rvan = 5 (4-6) ; Ran = 6 (5-7) ; R = which are narrower than thefollowing body annules. 94 (88-99). Styletabsent, œsophagus reduced and degenerate.. Males (n = 2) : L = 0.34-0.39 mm ; a = 17-19 ; Hemizonid 4-15 annulesanterior to the excretory b = 4.4-5.4 ; c = 10-13 ; spicules = 30-33 pm ; gu- pore. Lateral field with four lateral lines, the inner bernaculum = 6 pm ; Rex = 34-49 ; Ran = 16-18 ; two sometimes less distinct. Spicules slightly curved, R == 107-181. 27-35 pm long(measured along curvature). Guber- naculum curved, 5.4-6.8 pm long. Tail tapering to a bluntlyrounded terminus. Caudal alae reduced, REMARKS margins crenate, extending from four annules anterior to the cloaca to fourteen to sixteen annules posterior. Studiedspecimens correspond tothe description Penialsheath 4.3-5.1 pmlong. Testis packed with of Pinochet and Raski (1975), except for the rudi- rounded sperm. mentarylateral vulval membrane seen on Our Juvenile,st. 2: Bodysmooth, slightly curved specimens. The number of annuleson males seems ventrally with fine annulations.Lip region smooth to be too variable to be usedfor taxonomic purposes.

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Fig. 3. Hemiericonemoides obtusus Colbran, 1962. A : anterior region of female ; B, C : posterior region of male ; D, E : lateral field of male ; (Scale bar represents 20 pm).

H. nitidus was described from Minnesota, and the REMARKS examined specimens were collected from an unknown locality in Indiana, U.S.A. by Dr. V.R.'Ferris. This H. mangiferae was reported from Bowen, Queen- increases the known range of bothvariability and sland by Colbran in 1964, and since then from other distribution of H. nitidus. QueenslandIocalities, namely : Brisbane,Pialba, %Pioneer,Stanley River Crossing, theCrater and Marlborough (Khair1978). However, taxonomic Hemicriconemoides mangiferae studies by Dasgupta, Raski and Van Gundy (1969) Siddiqi, 1961 Germaniand Luc (1970) and Pinochet and Raski (Fig. 4C, D) (1975)suggest the necessity for reconsideration of the distribution of this species. A population studjed MEASUREMENTS fromNew South Wales included males, with four lateral lines, and therefore it is concluded that they Females (n = 20) : L = 0.54(0.46-0.63) mm ; represent t.rue H. mangiferae. Occurrence of this a = 20 (17-22) ; b = 4.6 (3.6-5.9) ; c = 25 [21-31) ; species in Australia confirms that itis a cosmopolitan V = 93 (92-94) ; stylet = 81 (74-90) pm ; m = 89 species. (86-95) ; Rex = 36 (33-39) ; Rv = 12 (10-14) ; Thepopulation of H. mangiferae examinedwas Rvan = 4 (2-6) ; Ran = 7 (6-9) ; R = 135 (127-142). collected from along the banks of the Ana Branch

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E A C

Fig. 4. Hemicriconemoides nitidus Raslti & Pinochet, 1975, A : head and B : tail. H. mangiferae Siddiqi, 1961, C : head, and D : tail. H. insignis Dasgupta, Raski & Van Gundy, 1969, E, F : variability of lip region ; G : tail. (Scale bars represent 20 Pm).

River (Darling river system) beside the Silver City REMARKS highway,about 25 kmnorth of Wentworth, New South Wales. Vegetation in the sampling area includes Eucalyptuscamaldulensis Denh., and E. largiflorens These specimens correspondwell to those described FvM., withoccasional Acaciastenophylla A. Cunn. byDasgupta, Raski and Van Gundy (1969). The ex Benth. above measurements are given to report on the variability and distribution of this species. Although H. insignis has only been reported from Hemicriconemoides insignis Dasgupta, the type locality in New South Wales, it is so far, Raski & Van Gundy, 1969 the most widely distributed species of the genus in (Fig. 4E-G) South Australia. It was collected from five localities MEASUREMENTS inSouth Australia, three south of Adelaide, Alli- gator Gorge in the lower Flinders Ranges and also Fernales (n = 14) : stylet = 73 (60-80) ym ; Ferries-"Donald Conservation Parknear Murray m = 90 (89-91) ; Rex = 31 (28-33) ; Rv = 9 (7- Bridge.Together with an additional locality at 10) ; Rvan = 3-4 : Ran = 6 (4-7) ; R = 112 (99- Nyngan,New South Wales, al1 areareas of Euca- 119). lyptus spp, varying from forest to mallee scrub.

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The annulation in Hemicriconemoides ACIINOWLEDGEMENTS Wethank Mr. D.E.Symon,, Senior Lecturerand Thereare two characteristics of theannules of Botanist,Waite Agricultural Research Institute, Hemicriconemoides described byAndrhssy (1979) University of Adelaide for identification of plant which do not agree with Our observations.Despite specimens. Also theSouth Australian section of thc ageneral lack of information for manyspecies, a NationalParks and WildlifeService for permission study of theliterature shows that arrangement of to take soil samples in their reserves. Thanks are also the spines or scales is more variable than suggested due to Dr. J.W. Warcup, Waite Institute ; Dr. P.D. Podger, of C.S.I.R.O., Hobart,Tasmania ; and Dr. by Andrhssy (1979). Although inhis definition of the P. Christensen and Mr. A.R.Annels of the Forests subfamilyHemicriconemoidinae he stated : “Scales Department(Manjimup) Western Australia for col- generallyarranged in alternating rows” he also lection of some of the soil samples. previouslystated (concerning Hemicriconemoides) “Larvaehave spines not arranged in continuous rowsas in the Ogma groupbut being alternate”. REFERENCES Fassuliotis(1962) showed that H. chitwoodi Esser, 1960juveniles have spiny scales arrangedin an ANDRASSY,1. (1979).Revision of thesubfamily Cri- conematinae Taylor, 1936 (Nematoda). Opusc. zool., imbricatemanner. Those of H. pseudobrachyurum Bpest., 16 : 11-57. De Grisse, 1964are described as six dentate scales COLBRAN, R.C. (1962).Studies of plantand soil on each annule, arranged as twelve rows. Juveniles nematodes 5. Four new species of Tylenchoidca of H. mangiferae Siddiqi, 1961 and H. strictathecatus from Queensland pincapple fields. Qld J. agric. Esser, 1960 are both described with twelve rows of Sci., 19 : 231-239. spines. Studiesof H. cocophilus (Loos, 1949) Chitwood COLBRAN, R.C. (1964).Studies of plantand soil & Birchfield 1957, byGermani and Luc (1970) nematodes 7. Queensland records of the order Tylen- clearly show the juveniles with ten spiny scales on chida and the genera Trichodorus and Xiphinema. each annule, arranged in ten continuous rows. They Qld J. agric. Sci., 21 : 77-123. also describe H. a@is Germani & Luc, 1979 with DASGUPTA,D.R., RASIII, D.J. & VANGUNDY, S.D. apparentlyalternate scales, which are in rows of (1969). Revision of thegenus Hemicriconemoides eleven or thirteen,in a spiral arrangement along Chitwood 62 Birchfield, 1957 (Nematoda : Cricone- the length of the body. Therefore we do not consider matidae). J. Nematol., 1 : 126-145. thearrangement of the juvenile scales to bea DEGRISSE, A. (1964). Hemicri~onemoidespseudobra- distinguishing characteristic for this genus. chyurum n. sp. (Nematoda : Criconematidac). Nema- Andrissy(1979) also described theannules of tologica, 10 : 369-372. adult (female) Hemicriconemoides as “not retrorse”. ESSER,R.P. (1960). Threeadditional specics in the This does notagree with Our observations,as al1 genus Hemicriconemoides Chitwood & Birchfield Our specimens of H. minor sp. n. clearly show retrorse 1957 (Nemata : Tylenchida). Nematologica, 5: 64-71. annules.Although most strongly developed in FASSULIOTIS,G. (1962). Life history of Hemicricone- H. minor sp. n., the annules forming the outer layer moides chitwoodi Esser. Nenzatologica, S : 110-116. of thedouble cuticle of H. taiwanensis are also GERMANI,G. & Luc, M. (1970). Cont,ribution à l’étude retrorse,desc,ribed byPinochet and Raski (1975) du genre Hemicriconemoides Chitwood & Birchfield, 1957 (Nematoda : Criconematidae) Cah. ORSTOM, as“posteriously orientated body annulation”. In Sb. Biol., 11 : 133-150. additionthe stylet knobs of H. taiuranensis are KHAIR,G.T. (197s). List of plant parasitic nematodes massive and rounded, without the anterior projections of Australia. Canberra, Dept.. Health(Plant Qua- characteristic of most species. H. obtusus also does rantine), Commonwcalth of Australia, 98 p. not well into the genus, with its distinctive lip fit PINOCHET,J. 62 RASIII, D.J. (1975). Four new spccies regionand unusual double cuticle. It mightbe of the genus Hemicriconemoides (Nematoda : Criconc- suggestedthat these represent one or morenew matidae). J. Nematol., 7 : 263-270. genera. However there are vast areas of Australia, REAY, F. & WALLACE, H.R. (1952). Plant nematodes particularly Western and Northern Australia where associated with native vegetation in South Austra- the endemic nematode species are unknown. There- lia. Nematologica, 27 (1981) : 319-329. fore we feel that until collections have been obtained SIDDIQI,M.R. (1961). Studieson species of Criconema- fromthese areas, splitting of thisgenus into new tinae(Nematoda : Tylenchida)from India. Proc. genera would be premature. ,helminth. Soc. Wash., 28 : 19-34.

Accepté pour publication le 8 mars 1982.

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