RESEARCH/INVESTIGACIÓN DESCRIPTION OF SOME XIPHINEMA SPECIES POPULATIONS (NEMATODA) FROM ARGENTINA E. J. Chaves1* and E. A. Mondino2 NEMA-AGRiS, Laboratorio de análisis de nematodos en suelo y plantas, 1900 La Plata, Argentina; 2Laboratório de Biologia do Solo, Depto. de Solos, Universidade Federal Rural do Rio de Janeiro, BR-465, km 7 Seropédica, 23890000 RJ-Brasil. *Corresponding author:
[email protected] 1
ABSTRACT Chaves, E. J., and E. A. Mondino. 2013. Description of some Xiphinema species populations (nematoda) from Argentina. Nematropica 43:68-77. Observations are reported on the morphology and morphometrics of Argentinian populations of Xiphinema krugi, Xiphinema rivesi, Xiphinema vulgare and Xiphinema surinamense found in cultivated and uncultivated soils from the Buenos Aires, Santa Fe, Tucumán and Misiones Provinces. Key words: Xiphinema, morphology, morphometrics, cultivated.
RESUMEN Chaves, E. J. and E. A. Mondino. 2013. Descripción de algunas poblaciones de especies de Xiphinema (nematoda) de Argentina. Nematropica 43:68-77. En el presente trabajo son reportadas observaciones morfométricas y morfológicas de poblaciones Argentinas de Xiphinema krugi, X. rivesi, X. vulgare and X. surinamense encontradas en suelos cultivados y no cultivados de las provincias de Buenos Aires, Santa fe, Tucumán y Misiones. Palabras clave: Xiphinema, morfométricas, morfológicas, cultivado.
INTRODUCTION
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Xiphinema, “the dagger nematode”, is one of the principal genera of plant parasitic nematodes, which is found widely throughout most of the world and is found on all of the continents, except Antarctica. The economic importance of the genus Xiphinema is related to the virus vector ability and consequent phytosanitary risk of some species, nevertheless, the knowledge on this group of nematodes in Argentina is scarce. Information on distribution of these nematodes in Argentina was studied by Luc and Doucet (1990) and Doucet et al. (1998), and description of some populations of X. krugi and X. surinamense from Córdoba and Entre Ríos provinces was provided by Decraemer et al. (1998). The objective of this study was to report our observations on the morphology and morphometrics of Argentinian populations of Xiphinema krugi, X. rivesi, X. vulgare and X. surinamense found in cultivated and uncultivated soils from the Buenos Aires, Santa Fe, Tucumán and Misiones provinces. Additional
information on the occurrence of Xiphinema species in Argentina is provided in this article. MATERIALS AND METHODS Soil samples were collected by the first author in cultivated and uncultivated soils during a survey of plant-parasitic nematodes in several regions of Argentina between 1978-1980 (Chaves, 1984) and in 1996. Nematodes were extracted with centrifugationflotation technique, fixed in hot 4% formaldehyde and mounted in pure dehydrated glycerine (de Grisse, 1969). The specimens were extracted, fixed, measured and drawn between 1981-1982 and in 1996. Descriptions Xiphinema krugi Lordello, 1955 (Table 1-2; Fig. 1, A-H, Fig. 3, B, E); Female (n = 13) Body ventrally arcuate, more or less C-shaped.
Description of Xiphinema species from Argentina: Chaves and Mondino Cuticule smooth; internally with transverse striae 0.6 µm. Lateral cord occupying 17% of body width. Lateral pores usually distinct throughout the body. Dorsal and ventral body pores distinct in the anterior body region. Head rounded, 6 µm high, 14 µm wide, offset by slight constriction. Amphid aperture occupying ½ of head width. Guiding sheath of spear 4-18 µm long, its posterior margin 102 µm (94-110) from the anterior end. Odontophore flanges well developed, 10 µm wide. Nerve ring 10-12 µm wide at 209 µm (202-218) from the anterior end. Total esophageal length 403 µm (370437), the basal bulb of esophagus measuring 94 µm (85-104) long and 22 µm (20-27) wide. Cardia 10-14 µm long. Hemizonid 6-7 µm wide at 186 µm (173-199) from the anterior end. Vulva transverse slit, at 736 µm (640-822) from anterior end. Two genital branches, the anterior one reduced 92 µm (74-106) long, consisting of a uterus with distinct large lumen and short pouch-like oviduct; between the uterus and oviduct a constriction is found formed by a weakly developed sphincter. The posterior genital branch is normally developed 299 µm (202-534) long, consisting of ovary, oviduct, sphincter and uterus with a wider portion. No spermatozoa, no Z organ. In one female an egg 173 µm long, 43 µm wide was present near the vagina. Vagina 44-52 % of body width. Tail conoid with ventral peg of variable length. Two pairs of caudal pores. Cuticle on tail with minute oblique lines. A tail blind terminal canal is present in all specimens. Rectum 37 µm (34-41) long. Male Not found. Juveniles Resemble females. The elongate tail in the first two stages become more conoid and subdigitate in J4 (Fig. 1, D-G); Table1 Remarks All the populations of X. krugi here reported are morphometrically similar to the original description (Lordello, 1955) and to the populations described by Cohn and Sher (1972), Williams and Luc (1977), Luc and Hunt (1978), Loof and Sharma (1979), Heyns (1977), Ferraz (1980), Ebsary et al. (1984), Oliveira et al., 2006, and Argentinean populations reported by Decraemer et al. (1998), and present a tail shape as shown in figure 1 H. The tail shape of X. krugi varies from one with a fairly long peg to one without peg (Coomans et al., 2001). The tail is subconoid in original description; regularly ogival with a very slight bulge at its extremity to conoid rounded with distinct ventral peg (Luc and Hunt, 1978); longer with a bluntly knobbed tail terminus and shorter tail with rounded terminus in Arkansas and Hawaii populations, respectively (Robbins and Ye, 2010).
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Luc and Hunt (1978) redefined X. krugi and observed a great variation in several biometrical characters. Analysing measurements of the tail and of the anterior genital branch, they suggested the occurrence of groups of different geographical origin. Oliveira et al. (2006) demonstrated the possibility that X. krugi is a species complex comprised of four distinct genotypes and/or cryptic species. Morphometrical data of populations described here most agrees with PX11 and PX26 Brazil populations (RFLP profile B). Habitat and localities Soil around potato plants in Concepción, Tucumán Province; garlic in Médanos and corn in Saladillo, Buenos Aires Province; strawberry in Coronda, Santa Fe Province, collected by E. Chaves 1978-1980. Eggplant in Helvecia, Santa Fe Province collected by C. Medera 1979. Table 2 Xiphinema rivesi Dalmasso, 1969. (Table 3, Fig. 2 A, B, I, Fig. 4); Female (n = 21) Body ventrally arcuate, closed or open C posture, tapering toward the extremities. Cuticle smooth, with 0.6 µm wide transverse striae internally. Lateral cord occupying 24-27% of body width. Lateral pores obscure; dorsal and ventral body pores not seen. Head rounded, almost continuous with the rest of the body, although a slight depression can be noticed. Head 10 µm wide. Amphid aperture occupying one half of head width. Guiding sheat of spear 7.5 µm (6-10) long, posterior margin located at 74 µm (71-79) from anterior part of body. Stylet flanges well developed 7 µm (6.58) wide. Nerve ring 8-10 µm wide at 167 µm (153173) from anterior end. Total oesophageal length 338 µm (314-368); basal bulb 74 µm (70-80) long, 16 µm (14-19) wide. Cardia 6-7 µm long. Intestine obscured by lipid granules. Hemizonid 5 µm wide at 141 µm ( 139-144) from anterior part. Vulva transverse slit, at 985 µm (892-1125) from anterior part. Two genital branches, the anterior sligthly shorter or equal to the posterior, measuring 157 µm (122-182) and 174 µm (145-213), respectively. Uterus small, oviduct simple, ovaries reflexed. Sphincter not discernible. Vagina 23-32% of body width. No Z-organ or spermatozoa. Bacteria present in the ovaries of the all specimens. Tail conoid with two pairs of caudal pores. Cuticle on the tail with very faint radial striae. An obscure tail blind canal is present. Prerectum not discernible. Rectum 18 µm (16-20) long. Male Not found. Juveniles Resembles adults in general shape.
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NEMATROPICA Vol. 43, No. 1, 2013 Remarks The X. rivesi populations from Argentina show some differences with respect to the original description (Dalmasso, 1969). In fact, the odontostyle, the odontophore and the tail are slightly shorter and the anterior genital branch is larger than the posterior one in the original description; conversely they are similar to the USA populations described by Lamberti and Zacheo (1979) and Wotjowicz et al. (1982), and the Canada populations described by Ebsary et al., (1984). X. rivesi seems to be the most widely distributed member of X. americanum group in Argentina, it has a wide host range and is one of the five species possessing only three juvenile stages (Robbins et al., 1996). It was synonymized with X. americanum by Stegarescu (1980), but Wojtowicz et al. (1982) consider X. rivesi as a valid species and add that the head of X. americanum is slightly offset, its stylet is shorter and its tail is of a different shape, being more pointed. Later, Georgi (1988) assumed that the ratio between the length and diameter of the hyaline tail tip was useful in distinguishing X. rivesi from X. americanum and Alkemade and Loof (1990) stated that the tail shape terminus and the anal body diameter are the only valuable characters to differentiate these two species. Habitat and locality Found in soil around garlic in Los Talas, Berisso, and in alfalfa field in Don Atilio farm, Tandil, Buenos Aires province, E. Chaves, 1980 and 1996 respectively. Table 3 Xiphinema vulgare Tarjan, 1964. (Table 4, Fig. 1, I-L, Fig. 3, A, D); Female Body arcuate only in the posterior part. Cuticle smooth; with fine transverse striae internally. Head rounded, separated from body by an incisure. Guiding sheath of the odontostyle 14 µm long, its posterior part at 101 µm from the anterior end. Odontophore flanges well developed, 7µm wide. Total esophageal length 372 µm; the basal bulb of esophagus measuring 14 x 91 µm. Cardia not seen. Esophago-intestinal junction not discernible. The anterior part of the intestine forms an evagination on one side of the esophageal bulb. Nerve ring 7µm wide located 122 µm from anterior extremity. Vulva transverse slit 1220 µm from anterior extreme. Two genital branches well developed, the anterior measuring 290 µm long, the posterior one 227 µm long. Uterus with three swollen chambers, two proximal and one distal, near the oviduct junction. A sphincter marks the separation from the oviduct. In the anterior branch the pars dilatata oviductus is only sligthly swollen, it is more developed in the posterior branch. No Z-organ or spermatozoa observed. Tail uniformly conoid, not clearly digitate, with rounded
terminus. Three pairs of caudal pores. Cuticule on the tail with minute oblique lines. Tail blind terminal canal present. Prerectum 502 µm long. Rectum 29 µm long. Male Not found. Juveniles Morphologically similar to the adult, except for the tail length wich is longer in J2 and J3. Remarks Only a female and two juveniles were found. The female has similar measurements to both X. vulgare and X. setariae Luc, 1958, but differ however from the type of X. vulgare in having shorter odontophore and odontostyle, longer tail length and higher c´ ratio. The tail length and c’ value most resemble X. setariae, but the remaining tail ratios given by Tarjan (1964) are similar to X. vulgare, and the hyaline part of the extremity of the tail also agrees with X. vulgare. Luc and Dalmasso (1975) stated that the hyaline tail is the most reliable character to separate X. vulgare from X. setariae, but such a concept was later rejected by Loof and Luc (1990). The status of X. vulgare and X. setariae is still controversial. Williams and Luc (1977), Loof and Sharma (1979), Brown et al. (1981) and Lamberti et al. (1995) support the validity of two species, but Cohn and Sher (1972), Loof and Luc (1990), Heyns and Coomans (1991), and Luc and Baujard (1996) consider X. vulgare a junior synonym of X. setariae. Nevertheless, the tail shape and length and c’ value of female, and tail shape of juveniles from Argentina resemble more X. parasetariae Luc, 1958 than the ones of the X. vulgare/X. setariae complex as the original descriptions given by Luc (1958) and descriptions of X. vulgare given by Brown et al. (1981), and X. parasetariae given by Heyns et al. (1994), and Sharma and Siddiqi (1990). According to Lamberti et al., (2001), because the synonymy of X. vulgare with X. setariae has been proposed by various authors and rejected by others, “to discuss the criteria used by the authors to arrive at their divergent conclusions is probably unproductive”. Habitat and locality Found in brackish soil in the Misiones Province (locality unknown), collected by J. Rodriguez 1979. Xiphinema surinamense Loof and Maas, 1972 (Table 5, Fig. 2. C-H, J, Fig. 3, C, F); Female (n = 2) Body ventrally arcuate after fixation, predominantly in the posterior part. Cuticule smooth, with fine transverse striae internally. Lateral cord occupying 16 % of body width. Lateral pores distinct throughout
Description of Xiphinema species from Argentina: Chaves and Mondino the body. Dorsal pores distinct in the anterior body region; the ventral ones distinct throughout the body. Head rounded almost continuous with the rest of the body with a slight depression. Amphidial aperture one-half of corresponding head width. Guiding sheath of odontostyle 11-14 µm long; its posterior margin 100-109 µm from anterior extreme. Odontophore flanges well developed 10 µm wide. Total esophageal length 404-407 µm; esophageal bulb 23-24 µm wide, 95-97µm long; cardia 9 µm long. Nerve ring 12 µm wide located 138-149 µm from the anterior extreme. Hemizonid 6 µm wide at 230-318 µm from anterior extreme. Vulva transverse slit, 829-970 µm from anterior extreme. Two genital branches: anterior branch reduced, without ovary, 275-300 µm long; the posterior one is normally developed 430-450 µm long, with reflexed ovary. In both branches the uterus is wide with the proximal parts well muscularized; the distal parts have a vesicular wall. A sphincter is present between uterus and oviduct. In the anterior branch the oviduct is reduced to a swollen sac. No Z-organ or sperm visible. One oval egg 54 x 27 µm was present in the uterus of one specimen. Vagina occupying 1/3 of body width. Tail hemielliptical with two or three pairs of caudal pores. Cuticle on tail with minute oblique lines. One specimen with tail blind terminal canal. Prerectum 225-300 µm long. Rectum 36-42 µm long. Male Not found. Juveniles Resembles adult in general shape. The tail elongate in the two first stages becomes more rounded in J3. A blind tail terminal canal is clearly visible in J3 and less visible in J2. The measurements are similar to those given by Loof and Sharma (1979), except for J3 tail length, that is longer (39 µm vs 30-32 µm). Remarks The biometrics of the two females from Misiones agree with the original description except for the shorter stylet and it is more similar to the Brazilian population described by Loof and Sharma (1979). There was an egg but sperm were not observed. There are two caudal pores in the original description, and two or three in Misiones specimens. The lateral pores, inconspicuous in the original description, are clearly visible on the Argentinean specimens. The structure of anterior genital branch of Misiones population differs from the others Argentinean populations described by Decraemer et al. (1998) in having a well demarcated ovejector from the glandular part of the uterus and in lacking cristalloid structures. However the anterior uterus of the Misiones population close resembles the paratype illustrated by Decraemer et al. (1998).
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Habitat and locality Found in brackish soil associated with X. vulgare in the Misiones Province (locality unknown) collected by J. Rodriguez 1979. LITERATURE CITED Alkemade, J. R. M., and P. A. A. Loof. 1990. The genus Xiphinema Cobb, 1913 (Nematoda: Longidoridae) in Perú. Revue Nématologie, 13:339-348. Brown, D. J. , M. Luc, and Purbadi. 1981. A description of some juveniles stages of Xiphinema vulgare (Nematoda:Dorylaimoidea). Nematologia Mediterranea, 9:205-210. Chaves, E. 1984. Observations on plant parasitic nematodes from Argentina. PhD. thesis, University of Ghent, Belgium, 106 pp. Cohn, E., and S. A. Sher. 1972. A contribution to the taxonomy of the genus Xiphinema Cobb, 1913. Journal of Nematology, 4:36-65. Coomans, A., R. Huys, J. Heyns and M. Luc. 2001. Character analysis, phylogeny and biogeography of the genus Xiphinema Cobb, 1913 (Nematoda: Longidoridae). Annales du Musée Royal de l’Afrique Centrale (Zoologie), Tervuren, Belgique, 287:1-239. Dalmasso A., 1969. Etude anatomique et taxonomique des genres Xiphinema, Longidorus et Paralongidorus (Nematoda:Dorylaimidae). Memoires du Museum National d´Histoire Naturelle, Ser. A. Zoologie, 61:33-82. Decraemer, W., M. E. Doucet, and A. Coomans. 1998. Longidoridae from Argentina with description of Paraxiphidorus brevistylus sp.n. (Nematoda: Longidoridae). Fundamental and Applied Nematology, 21:371-388. De Grisse, A. 1969. Redescription ou modifications de quelques techniques utilisées dans l’étude des nématodes phytoparasitaires. Mededelingen Rijksfakulteit Landbouwwetenschappen Gent, 34:351-369. Doucet, M. E., L. C. C. B. Ferraz, J. C. Magunacelaya, and D. J. F. Brown. 1998. The occurrence and distribution of longidorid nematodes in Latin America. Russian Journal of Nematology, 6:111128. Ebsary, J. W. Potter, and W. R. Allen. 1984. Redescription and distribution of Xiphinema rivesi Dalmasso, 1969 and Xiphinema americanum Cobb, 1913 in Canada with a description of Xiphinema occiduum n. sp. (Nematoda: Longidoridae). Canadian Journal of Zoology, 62:1696-1702. Ferraz, L. C. B., 1980. Observations on some Xiphinema species found in Brazil (Nematoda: Dorylaimoidea). Nematologia Mediterranea, 8:141151.
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Fig. 1. Xiphinema krugi: A, female anterior region; B, amphid shape; C, female anterior genital branch; D-H, tail of J1, J2, J3, J4 and female respectively. X. vulgare: I-K, tail of J2 , J3 and female respectively; L, female anterior region.
Description of Xiphinema species from Argentina: Chaves and Mondino
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Fig. 2. Xiphinema rivesi: A, female anterior region; B, female tail. X. surinamense: C, female anterior genital branch; D-F, tail of J1, J2 and J3 respectively; G, female anterior region; H, female tail; I-J, amphid shape of X. rivesi and X. surinamense, respectively.
Fig. 3. Photomicrographs of anterior and posterior regions of X. vulgare (A, D), X. surinamense (C, F) and Xiphinema krugi (B, E). Scale bars: A, B, C, F, E = 20µm, D = 50 µm.
Fig. 4. Photomicrographs of Xiphinema rivesi A, C, female anterior and posterior region of garlic population, B, D female anterior and posterior region of lucerne population. Scale bars = 20 µm.
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Description of Xiphinema species from Argentina: Chaves and Mondino
Table 1. Morphometrics of females of Xiphinema krugi from different populations in Argentina Concepción Helvecia Coronda Saladillo Médanos n 3 4 1 4 1 L (mm) 2.20 2.20 2.37 2.14 2.23 (2.10-2.23) (2.00-2.34) (2.00-2.225) a 48 47 49 50.7 48 (46.7-49.6) (42.5-50) (50-51) b 5.5 5.1 6.3 5.4 5.6 (5.2-6.0) (4.9-5.4) (5.2-5.7) c 61 55 55 58 54 (57-67) (52-60) (55-62) c´ 1.0 1.3 1.5 1.2 1.3 (1.0-1.1) (1.1-1.4) (1.2-1.3) V 34.6 33.7 34 32 33 (34-35) (33-35) (31-33) Odontostyle (µm) 112 108 110 105 103 (111-113) (106-111) (103-108) Odontophore (µm) 70 71.7 64 68.5 68 (71.73) (67-70) Stylet (µm) 182 180 174 174 171 (181-183) (178-182) (173-178) Tail length 35 39.5 43 37 41 (33-37) (39-41) (36-38) Anterior genital branch/vulval diameter 1.6 2.3 2.0 2.0 2.0 (1.8-2.4) n = number of specimens; L = body length; a = body length/body width; b = body length/distance from anterior end to end of pharynx; c = body length/tail length; c’ = tail length/ body width at anus or cloaca; V = distance from anterior end to vulva x 100/ body length.
Table 2. Morphometrics of juveniles of Xiphinema krugi J1 n 2 L (mm) 0.69-0.77
J2 J3 J4 8 16 9 1.05 1.31 1.75 (0.93-1.12) (1.19-1.48) (1.56-1.91) a 34.5-37.5 37 41.7 45.4 (34-40) (37-47) (43-49) b 3.2-3.4 3.8 4 4.7 (3.2-4.2) (3.5-4.8) (4-5.5) c 18-19 23.6 29 41 (23-25) (25-34) (39-45) c´ 2.5-3.0 2.1 1.8 1.4 (1.9-2.5) (1.6-2.4) (1.3-1.6) Odontostyle 46 58 76 92 (57-59) (71-80) (89-96) Odontophore 33-35 45 51 61 (43-46) (47-54) (58-64) Stylet 79-81 103 127 153 (100-105) (120-132) (151-156) Replacement ondontostyle 57 77 91 107 (74-79) (87-96) (99-116) Tail 39-42 44 44 43 (39-47) (41-50) (36-48) n = number of specimens; L = body length; a = body length/body width; b = body length/distance from anterior end to end of pharynx; c = body length/tail length; c’ = tail length/body width at anus or cloaca; V = distance from anterior end to vulva x 100/body length.
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Table 3. Measurements of Xiphinema rivesi from Argentina Population Los Talas Female J2 n 10 2 L (mm) 1.85 1.46-1.56 (1.68-2.10) a 42 43-44 (38-48) b 5.4 4.75-5.0 (5-6) c 59 43-47 (53-66) c´ 1.3 1.5-1.6 (1.2-1.5) V 53 (51-54) Odontostyle (µm) 91 68-75 (86-97) Odontophore (µm) 47 40-41 (44-51) Stylet (µm) 138 108-116 (132-148) Replacement - odontostylet (µm) 86-89
Population Tandil Female J2 J3 11 1 5 1.93 1.10 1.43 (1.71-2.04) (1.38-1.47) 51 46 45-54z (45-54) 6.2 3.8 4.8 (5.7) (4.7-5.0) 60 33 42.5 (54-66) (39-46) 1.5 2.3 1.9 (1.4-1.8) (1.8-2.1) 53.4 (52-56) 92 55 71 (87-97) (69-73) 48 37 42y (45-51) (39-45) 141 92 112y (135-148) (110-117) 71 90 (86-95) Tail length (µm) 31 33-34 32 33 33.5 (30-34) (31.36) (30-35) n = number of specimens; L = body length; a = body length/body width; b = body length/distance from anterior end to end of pharynx; c = body length/tail length; c’ = tail length/body width at anus or cloaca; V = distance from anterior end to vulva x 100/body length. z n = 2, yn = 3
Table 4. Measurements of Xiphinema vulgare from Argentina Female J2 J3 n 1 2 1 L 2.98 1.12-1.20 1.60 a 65 46-47 59 b 8 4.3-4.6 5 c 46 16-16.5 20.6 c´ 2.5 4.2-4.3 4.3 V 41 Odontostyle 105 61 74 Odontophore 60 38-41 49 Stylet 165 99-102 123 Replacement odontostyle 74-76 91 Tail 65 70-73 79 LNT 18 8-9 16 Tail/LNT 3.6 7.7-9 4.8 n = number of specimens; L = body length; a = body length/body width; b = body length/distance from anterior end to end of pharynx; c = body length/tail length; c’ = tail length/body width at anus or cloaca; V = distance from anterior end to vulva x 100/body length; LNT length of the hyaline part of tail.
Table 5. Measurements of Xiphinema surinamense from Argentina Female J1 J2 J3 n 2 1 1 1 L 2.22-2.46 0.73 0.89 1.16 a 43-48 41 37 39 b 5.4-6 3 3.6 3.7 c 72 17.5 25 29.5 c´ 0.8-0.9 3.2 1.9 1.7 V 37-39 Odontostyle 103-108 46 51 70 Odontophore 72-76 37 42 54 Stylet 175-184 83 93 124 Replacement odontostyle 57 67 86 Tail 32-34 42 36 39 n = number of specimens; L = body length; a = body length/ body width; b = body length/distance from anterior end to end of pharynx; c = body length/tail length; c’ = tail length/ body width at anus or cloaca; V = distance from anterior end to vulva x 100/body length.
Description of Xiphinema species from Argentina: Chaves and Mondino Georgi, L. 1988. Morphological variation in Xiphinema spp. from New York Orchards. Journal of Nematology, 20:47-57. Heyns, J. 1977. The genus Xiphinema in South Africa. IV. X. krugi Lordello 1955, X. mediterraneum Martelli & Lamberti, 1967, and a new specie of the X. hallei group (Nematoda:Dorylaimida). Phytophylactica 9:109-114. Heyns, J., and A. Coomans. 1991. Longidoridae from Botswana. Phytophylactica 23:29-36. Heyns, J., A. Coomans, and M. Luc. 1994. Morphometrics of juvenile stages of some Xiphinema species (Nematoda: Longidoridae). Nematologica, 40:25-31. Lamberti, F., and T. Bleve-Zacheo. 1979. Studies on Xiphinema americanum sensu lato with descriptions of fifteen new species (Nematoda, Longidoridae). Nematologia Mediterranea, 7:51-106. Lamberti, F., T. D´Addabbo, M. Arias, A. Agostinelli, and M. A. Bravo. 1995. On the synonymy of Xiphinema vulgare Trajan, 1964 with X. setarie Luc, 1958 (Nematoda, Dorylamida). Nematología Mediterranea, 23:131-145. Lamberti, F., L. W. Duncan, F. De Luca, S. Molinari, A. Agostinelli, D. Dunn, M. I. Coiro, and V. Radicci. 2001. Biometric and molecular characterization and juvenile development stages of Xiphinema vulgare Tarjan, 1964 (Nematoda: Dorylaimdida). Nematologia Mediterranea, 29:137-144. Loof, P. A. A., and P. W. Th. Maas. 1972. The genus Xiphinema (Dorylaimida) in Surinam. Nematologica, 18:92-119. Loof, P. A. A., and R. D. Sharma. 1979. Plant parasitic nematodes from Bahia State, Brazil: the genus Xiphinema Cobb, 1913 (Dorylaimoidea). Nematologica, 25:111-127. Lordello, L. G. E. 1955. Xiphinema krugi n.sp. (Nematoda, Dorylaimidae) from Bazil with a key to the species of Xiphinema. Procceedings Helminthological Society Washington. 22:16-21. Luc, M. 1958. Xiphinema de l´Ouest Africain:description de cinq nouvelles espéces (Nematoda: Dorylaimidae). Nematologica 3:57-72. Luc, M., and P. Baujard. 1996. Xiphinema vulgare Tarjan, 1964 and X. insulanum Lamberti et al., 1995, two junior synonyms of X. setarie Luc, 1958 (Nematoda:Longidoridae). Nematologica 42:579582.
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Received: Accepted for publication: 25/X/2012 Recibido: Aceptado para publicación:
4/III/2013
