Plant Parasmc NEMATODES of LEGUMES in TURKEY

Nematol. medito(1994). 22: 245-251

Istituto di Nematologia Agraria, C.N.R., 70126 Bari, Italyl; International Centerfar Agricultural Researcbin tbe Dry Areas (ICARDA), P.O. Box 5466 Aleppo, Syria2; Field CropsCentrai ResearcbInstitute, Ulus,Ankara, Turkey3

PlANT PARASmC NEMATODES OF LEGUMES IN TURKEY

by 3 M. DI VITOI,, N. GRECOI, G. ORES 1, M.C. SAXENA2, . K.B. SINGH2and I.KUSMENoGLL

Summary. Surveysundertaken in Turkey, during spring 1991 and summer 1992, revealed that root-lesion nematodes were the most common of the several plant parasitic nematodes associatedwith chickpea and lentil. pratylencbus tbomei, P. penetrans and P. mediterraneus occurred throughout the country and were suspectedto reduce crop yields. P. alleni and P. zeae were also present in a few fields. Among other root-Iesion nematodes, Pratylencboidesleiocauda was widespread, while P. alkani and P. et2'Urumensis,and Zygotylencbusguevarai were present in a few samples only. Heterodera ciceriwas detected in twelve fields of chickpea and two of lentil, although severe damage was observed only on chickpea. Meloidogyne artiellia was observed in one field only. Ditylencbus dipsaci was found in two samples of lentil. Other nematodesfound in the soi! were species of Helicotylencbus, 1Ylencborhyncbus,paratylencbus, Tylencbus,Longidorus, Tropb- urus, Tricbodorus, Criconemoides,Heterodera, Meloidogyne and Xpbinema index, X. pacbtaicum and X. italiae.

Nematodescause severe damage to legumes in several terranean coast (locations 1-33, Fig. 1) and during July Mediterranean countries (Greco, 1985; Greco and Di Vita, 1992 in the Anatolian Plateau (locations 34-56, Fig. 1) 1988;Sikora and Greco, 1990;Greco et al., 1992; Di Vita et when these legumes were in an early podding stage. Soi! al., 1994). Far example, the pea cyst nematode, Heterode- (2 kg) and root (4-5) sampleswere collected tram the rhiz- ra goettingiana Liebscher, causes severe damage to pea osphere of plants in each field sampled. Crops showing (Pisum sativum L.) and faba bean (Vicia faba L.) (Di Vita yellowing and stunting were preferentially sampled; other- and Greco, 1986). Surveys of nematodes in chickpea (Cic- wise, sampling was done at regular distancesalong the en- er arietinum L.) and lentil (Lens culinaris Medik.) fields in tire caute taken far the survey. Syria and North Africa (Algeria, Marocco and Tunisia) re- Nematodeswere extracted tram 500 cm3 soi! using the vealed that the most common nematodes were Pratylen- Cobb's wet sieving and Baermann's tunnel method, fixed chus thornei Sher et Allen, P. penetrans (Cobb) Filipjev et in 5% hot formalin and counted. Roots were incubated in ShuurmansStekhoven and P. mediterraneus Corbett (Gre- jars (Young, 1954) to extract endoparasitic migratory nem- co et al., 1984; 1992; Di Vita et al., 1994). Meloidogyne ar- atodes, which were then preserved in 5% hot formalin. En- tiellia Franklin, although observed in few fields, was doparasitic sedentary and remaining migratory nematodes present in alI the countries surveyed, while Heterodera ci- were extracted later using Coolen's method (1979). They ceri Vovlas, Greco et Di Viro was found only in Syria. AlI were counted and about 20 specimens per sample and these nematodes afe damaging to their host plants (Di Vita species were mounted in glycerine (Seinhorst, 1959). Peri- and Greco, 1988;Greco et al., 1988). neal patterns of fernales of Meloidogyne spp. and cones of Little is known about nematodes of legumes in Turkey, cysts of Heterodera spp. were also prepared. Measure- a country which ranks second in chickpea production and ments were also taken far root-lesion and cyst nematodes. first in lentil production in the world. Therefore, surveys Perrnanent slides were then examined microscopically far were conducted in Turkey during 1991 and 1992 to ascer- species identification. The key given by Handoo and tain the nematodes associatedwith legume crops. The re- Golden (1989) was used to identify pratylenchus spp., and sults of these surveys afe reported in this papero that of Sher (1970), along with the description of Yiiksel (1977), far Pratylenchoidesspp.

Materials and methods Results Two surveys, each of two weeks duration, were undertaken in the rnajor chickpea and lentil growing areas of A total of 151 soil and root samples were collected: Turkey during May 1991 in the South and along the Medi- 136 (90%) from chickpea, Il (7%) from lenti! and 4 (3%)

- 245- Fig. 1 - Map of Turkey showing location numbers, as in Table I, where chickpea, lenti! and vetch were sampled for nematode infestation in 1991 and 1992. from vetch (Vicia sativa L.) fields (Table I; Figs 1; 2; 3); were Pratylenchus thornei (61%), P. penetrans (23%) and the last named crop sharesnematode specieswith the oth- Pratylenchoides leiocauda Sher (18%) (Table I; Figs 2; 3). er two crops. Pratylenchus mediterraneus (7%), P. alleni Ferris (3%), P. Cyst nematodes: Heterodera ciceri was the only cyst brachyurus (Godfrey) Filipjev et Shuurmans Stekhoven nematode found in Turkey. It occurred in 12 chickpea and and P. zeae Graham (2%) (Table I; Fig. 2), and Pratylen- 2 lentil samples collected at Kurtalan, Bismil, Pirinclik, Ki- choides alkani Yiiksel (1%), P. erzurumensis Yiiksel (1%), ziltepe, Siverek, Kirbasi, Suruc, Izmir, Gudul, Esagigab,El- and Zygotylenchus guevarai (Tobar Jimenez) Brawn et azig and Kaiseri (Table I; Fig. 3). Morphometrics of second 1oof (3%) were less common (Table I; Figs. 2; 3). Nema- stage juveniles of the nematode population collected at todes were often numerous in the roots; 136,000 P. pene- Kurtalan, Bissell, Pirinclik, Siverek, Kirbasi, Suruc, Izmir, trans/5 g root were present in chickpea samples collected Gudul, Esagigab, Elazig and Kaiseri were similar to those at Kaman and as many as 14,000 of P. penetrans, P. thor- of the originai description given by Vovlas et al. (1985), nei or P. mediterraneus/5 g root in samples of chickpea while the population from Kiziltepe has a shorter stylet. collected at Kaman, Gudul, Malazgirt, Elazig and Kirik- Heavily infested plants showed poor growth and extensive kale. Morphometrics of these nematodes were within the yellowing. range reported by Handoo and Golden (1989). Root-knot nematodes: only M. artiellia was detected Stem and bulb nematode: Ditylenchus dipsaci (Khuen) and was found in roots of chickpea in one sample collect- Filipjev was extracted from lenti! at Pirinclik and Bespinar. ed at Usak (Table I; Fig. 3). Infested plants were yellowish Symptoms of nematode attack Oeaf and stem necrosis and and stunted. stem and pod distortion) were not obvious in either field. Root-lesion nematodes:a rotai of 150 root samples of Other nematodes: analysis of soi! samples revealed the chickpea, lentil and vetch were infested with these nema- presence of several other plant parasitic nematodes. Spe- todes. Attack was often severe with roots becoming com- cies of Tylenchorhynchus (55%), Helicotylenchus(68%), pletely necrotic and black and aerial plant parts showing paratylenchus (13%), Trophurus (4%), Criconemoides poor growth and yellowing. One hundred and four sam- (2%), Tylenchus (74%), Zygotylenchus guevarai 2%, Dity- ples were infested with a single species of root-lesion lenchus dipsaci 6%, Xiphinema [x. index Thome et Allen nematode and 38 samples were infested with two or more 2%, X. pachtaicum (Tulaganov) Kirjanova 5% and X. itali- species (Table I; Figs 2; 3). The most common species ae Meyl 2%], LonRidorus (1%), Trichodorus (1%). Meloido-

246

gyne (second stage juveniles) (6%) and Heterodera (sec- effect of other root-lesionnematodes on the yield of sam- ond stage juveniles) (5%) were encountered in 151 sampled crops is, however, not known. ples collected. No plant damage was observed associated Although different species of root-lesion nematodes with these nematodes. were present in different parts of the country, P. mediterraneus was dominant in south-eastern Turkey (Silvan, Kurtalan, Pirinclik and Cinar) in an area bordering North- Discussion east Syria, where this was the only root-lesion nematode attacking chickpea and lentil. pratylenchus thomei was The two surveys cannot be considered exhaustive; found throughout Turkey but was dominant in the Anato- however, they demonstrate that several nematodes afe lian Plateau and was the only Pratylenchus species occur- commonly associatedwith chickpea and lentil in Turkey. ring on the Mediterraneancoast. Many of them afe known to be higWy damaging to these The chickpea cyst nematode (H. cicen) is very damag- pulses. Root-lesion nematodes were present in alI sampled ing to chickpea, pea, grasspea (Lathyrns sativus L.) and fields and could cause considerable yield losses.The large lentil. Severeyield losses in chickpea and lentil can be ex- number of P. thomei, P. penetrans and P. mediterraneus pected when population densities of the nematode ex- specimensextracted from roots of chickpea and their asso- ceeds 1 egg/g soil in chickpea fields and 2.1 eggs/g soil in ciation with extensive root necrosis, suggest that they afe lentil fields (Greco et al., 1988). H. ciceriwas found in dif- highly pathogenic to this food legume in Turkey. Di Viro ferent areas of Turkey (Fig. 3). It was most frequent in et al. (1992) demonstrated that up to 50% of chickpea south-east, but was present also in the Anatolian Plateau yield can be lost in fields infested with P. thomei in Syria. (Gudul and Kaiseri) and the Mediterranean coast (Izrnir). However, the extent of damage caused by root-lesion H. ciceri is common in the provinces of Aleppo and Idleb nematodes at farm level is less than that caused by cyst in northern Syria (Greco et al., 1992). Despite extensive and root-knot nematodes. Nevertheless,root-Iesion nema- cultivation of chickpea and lentil, bolli hosts of the nematodes afe widely distributed and, therefore, must be con- lode, in the provinces of Dara'a and Sweda in southern sidered of economic importance at the country level. The Syria, the cyst nematode was not found there. Most prob-

MEDITERRANEAN SEA

. Pratylenchusalleni . p Itylenchus penetrans [] Il brachyurus . Il thornei O Il mediterraneus t. Il lese

Fig. 2 - Distribution Pratylencbus species found in roots of chickpea, lenti! and vetch crops in Turkey

249 MEDITERRANEAN SEA

À Pratylenchoides alkani . Zygotylenchus \Quevarai o Il erzurumensis A Heterodera ciceri . Il leiocauda D Meloidogyne artiellia

Fig. 3 - Distribution of some plant parasitic nematodes in roots of chickpea, lentil and vetch crops in Turkey.

ably the desert area between the cities of Damascus and North Africa (Di Vita et al., 1994) where, H. ciceri has not Nabak has acted as a barrier against the spread of this been found. nematode. H. cicerl has not been reported on chickpea, in More surveys need to be undertaken to better under- countries bordering Syria and Turkey. Several Cicer spp., stand the impact of these nematodes on chickpea and len- considered to bave originated in Syria and Turkey, afe til crops in Turkey. Other investigations afe also necessary good hosts far H. cicerl (Di Viro et al., 1988). Ali this to obtain greater insight into the effect of nematodes on would suggest that H. cicerl originated in the area of pulse production in Turkey and to develop an effective northem Syria and Turkey. However, the damage caused management system far controlling those species of eco- by this nernatode in chickpea and lentil appears more se- nomic importance. vere in Syria than Turkey. Most probably, the two-year crop rotation in Syria as compared with three years in Tur- Acknowledgement:We thank Mr. F. Catalana far tech- key, increases the severity of the nematode infestation in nical assistanceand Mr. V. Radicci far preparing the fig- the former country (Saxena et al., 1992). ures. Meloidogyne artiellia is very darnaging to chickpea in northem Syria and occurs in several other countries in the Mediterranean basin (Sikora and Greco, 1990). Surprising- Uterature cited ly, it was detected in only one root sample of chickpea at COOLENW. A., 1979. Methods far the extraction of Meloidogyne Usak, despite the fact that in Turkey chickpea is grown in spp. and other nematodes from roots and soil, pp. 317-329. rotation with cereals, which afe good hosts far the nema- In: Root-Knot Nematodes (Meloidogyne Species) Systematics, rode. Biology and Control. (Eds. Lamberti F. and Taylor C.E.). Aca- demic Press, London. Heterodera cicerl, P. thornei and P. mediterraneus afe DI Vrro M. and GRECON., 1986. The pea cyst nernatode, pp. 321- widely distributed in both Syria and Turkey. The two Prat- 332. In: Cyst Nematodes. (Eds. Lamberti F. and Taylor C.E.). ylenchus species and P. penetrans were also common in Plenum Press, London.

- 250- DI VITa M. and GRECON., 1988. The reiationship between initiai GRECON., DI VITa M.; SAXENAM. C. and REDDYM. V., 1988. Effect popuiation densities of Meloidogyne artiellta and yieid of win- of Heterodera ciceri on yield of chickpea and lentil and devel- ter and spring chickpea. Nematol. medit., 16: 163-166. opment of this netnatode on chickpea in Syria. Nematologica, DI VITa M., GRECON., HAuLA H. M., MABSOUTEL., LABDI M., BENI- 34: 98-114. WAL S. P. S., SAXENAM. C., SINGHK. B. and SoLH M. B., 1994. HANDOOZ. A. and GOLDENM. A., 1989. A key and diagnostic com- Nematodes of winter season iegumes in north Africa. Nema- pendium to the species of the genus Pratylencbus Filipjev, tal. medit., 22: 3-10. 1936 (lesion nematodes). J. Nematol., 21: 202-218. DI VITa M., GRECON. and SAXENAM. C., 1992. Pathogenicity of SAXENAM. C., GRECON. and DI VITa M., 1992. Contrai of Heterode- Pratylencbus tbomei on chickpea in Syria. Nematol. medit., ra ciceriby crop rotation. Nematol. medit., 20; 75-78. 2Q 71-73. SElNHORSTJ. W., 1959. A rapid method far the transfer of nema- DI VITa M., GRECON., SINGH K. B. and SAXENAM. C., 1988. Re- todes from fJXative to anhydrous glycerin. Nematologica: 4: sponse of chickpea germpiasm iines to Heterodera ciceri. 67-69. Nematol. medit., 16: 17-18. SHERS. A., 1970. Revision of the genus Pratylencboides Winslow, GRECON., 1985. Nematodes of faba beans, chickpeas, and ientils 1958 (Netnatoda: Tylenchoidea). Froc. belmintb. Soc. Wasb., in the Mediterranean region and their contrai, pp. 179-187. In: 37: 154-166. Proc. Inter. Worksbop oJ Faba beans, Kabuli Cbickpeas, and SIKORAR. A. and GRECON., 1990. Nematode parasites of food Lentils in tbe 1980s. (Eds. Saxena M. C. and Varma S.). ICAR- legumes, pp. 181-235. In: PlanI Parasitic Nematodes in DA, Aleppo (Syria), 16-20 May 1983. Subtropical and Tropical Agriculture (Eds. Luc M., Siko- GRECON. and DI VITa M., 1988. The importance of piant parasitic ra R. A. and Bridge J.). CAB International, Wallingford, nematodes in food iegume production in the Mediterranean region, pp. 28-45. In: Proc. oJ Worksbop on: Nematodes Para- U.K. sitic to Cereals and Legumes in Temperate Semi-arid Regions. VOVLASN., GRECON. and DI VITa M., 1985. Heterodera ciceri sp.n. (Nematoda: Heteroderidae) on Cicer arietinum L. from north- Lamaca (Cyprus), 1-5 March 1987. GRECON., DI VITa M., REDDYM. V. and SAXENAM. C., 1984. A pre- ern Syria. Nematol. medit., 13: 239-252. iiminary survey of piant parasitic nematodes of ieguminous YOUNGT. W., 1954. An incubation method far collecting migratory crops in Syria. Nematol. medit., 12: 87-93. endoparasitic nematodes. Pl. Dis. Reptr., 38: 794-795. GRECON., DI VITa M. and SAXENAM. C., 1992. Piant parasitic nem- YUKSELA. S., 1977. Pratylencboides alkani sp.n. and P. erzuru- atodes of cDOi season food iegumes in Syria. Nematol. medit., mensis sp.n. (Nematoda: Tylenchoidea) from soil in Turkey. 2Q 37-46. Pmc Helminth ."oc wa.çh. 44: 18~-188.

Accepted for publication on 31 August 199'

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