František Moravec 1 *, Maryam Khosheghbal 2 and Jamileh Pazooki 2

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1 DOI: /s W. Stefański Institute of Parasitology, PAS Acta Parasitologica, 2014, 59(2), ; ISSN Dichelyne (Dichelyne) spinigerus sp. nov. (Nematoda: Cucullanidae) from the marine fish Otolithes ruber (Sciaenidae) off Iran and first description of the male of Philometra otolithi Moravec et Manoharan, 2013 (Nematoda: Philometridae) František Moravec 1 *, Maryam Khosheghbal 2 and Jamileh Pazooki 2 1 Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, České Budějovice, Czech Republic; 2 Department of Marine Biology, Faculty of Biological Sciences, Shahid Beheshti University, Tehran, Iran Abstract Recent parasitological examinations of the marine perciform fish (tigerteeth croaker) Otolithes ruber (Bloch et Schneider) (Sciaenidae) from off Iran yielded one new and one previously known nematode species: Dichelyne (Dichelyne) spinigerus sp. nov. (Cucullanidae) from the host s intestine in the Persian Gulf and Philometra otolithi Moravec et Manoharan, 2013 (Philometridae) from the ovary in the Persian Gulf and the Sea of Oman. The new species D. spinigerus is mainly characterized by the tail tip of both sexes terminating in two shaply pointed spikes (one dorsal and one ventral) and bearing a pair of minute lateral cuticular spines at its base, situation of both deirids and the excretory pore well posterior to the level of the posterior end of oesophagus, absence of a precloacal sucker and the presence of one or two intestinal caeca. The male and small mature females of the gonad-infecting species P. otolithi are described for the first time, based on light and scanning electron microscopical studies. The male of P. otolithi is most similar to that of P. johnii Moravec et Ali, 2013, but differs from it by the structure of the cephalic end and the number of caudal papillae; both species also differ from each other by the presence of transverse lamellae in the buccal cavity of gravid and subgravid females of P. otolithi, which are missing in those of P. johnii. Keywords Parasitic nematode, Dichelyne, Philometra, marine fish, Otolithes, Iran Introduction The fauna of nematodes parasitizing marine fishes in waters of southern Iran remains little known. Despite several studies on nematode parasites in brackish and fresh waters, there are only a few reports on nematodes parasitizing marine fishes off the southern Iranian coast (Peyghan et al. 2004, 2006; Razi Jalali et al. 2008; Bagherpour et al. 2011; Eslami et al. 2011). Recently, Moravec et al. (2013) recorded two species of tissue-dwelling nematodes, Clavinemoides annulatus Moravec, Khosheghbal et Pazooki, 2013 and Philometra otolithi Moravec et Manoharan, 2013 (both Philometridae), from the tigertooth croaker Otolithes ruber (Bloch et Schneider) (Sciaenidae) in the Persian Gulf and the Sea of Oman. Subsequent parasitological examinations of O. ruber from the same region, carried out in 2013, revealed the presence of a new intestinal nematode species of Dichelyne (Dichelyne) Jägerskiöld, 1902 (Cucullanidae) and made it possible to discover the hitherto unknown male of the gonad-infecting philometrid P. otolithi. Detailed descriptions of these nematodes based on light and scanning electron microscopical (SEM) studies are presented below. Materials and Methods Fish were collected by bottom trawl to the northwest of Qeshm Island (26º42 26º44 N, 55º30 55º25 E) and off *Corresponding author: moravec@paru.cas.cz

2 230 František Moravec et al. Kolahi (27º01 N, 56º41 E) in the Persian Gulf and off Bandare-Jask (25º32 N, 58º26 E) in the Sea of Oman. The nematodes obtained were washed in physiological saline and were then fixed and preserved in 4% formalin. Philometrid males were dissected out from formalin-fixed fish ovaries. For light microscopy examination, the nematodes were cleared with glycerine. Drawings were made with the aid of a Zeiss drawing attachment. Specimens used for SEM were postfixed in 1% osmium tetroxide (in phosphate buffer), dehydrated through a graded acetone series, critical-point-dried and sputter-coated with gold; they were examined using a JEOL JSM- 7401F scanning electron microscope at an accelerating voltage of 4 kv (GB low mode). All measurements are in micrometres unless otherwise indicated. The fish nomenclature adopted follows FishBase (Froese and Pauly 2013). Results Family Cucullanidae Cobbold, 1864 Dichelyne (Dichelyne) spinigerus sp. nov. Description: Body small, cuticle markedly thick, especially at cephalic region. Lateral alae absent. Oral opening dorsoventrally elongate, surrounded by narrow membranous ala (colarette) and numerous minute teeth. Four submedian cephalic papillae and pair of smaller lateral amphids present (Figs 1A C, 2A C). Oesophagus relatively short, expanded at anterior end to form large pseudobuccal capsule (oesophastome) distinctly broader than posterior part of oesophagus; latter somewhat expanded (Fig. 1A, B). Oesophastome with distinct inner hole at base of its dorsal wall in lateral view (Fig. 1A C). Nerve ring encircling oesophagus somewhat anterior to middle of oesophagus, at 26 47% of its length. Oesophagus opening into intestine through small valve. Intestine forming usually one, dorsal, anterior caecum extending anteriorly below level of nerve ring; rarely two caeca or single dorsal caecum bent posteriorly present (Fig. 1A, B). Deirids small, situated near end of oesophagus, usually short distance posterior to end of oesophagus (Figs 1A, B; 2E), less often at its level or slightly anterior to it. Excretory pore far below level of end of oesophagus (Fig. 1A, B). Male (7 specimens; measurements of holotype in parentheses). Length of body (3.06) mm, maximum width (245). Maximum width of cuticle at oesophageal region (30). Length of entire oesophagus (476); oesophastome (136) long, (109) wide; maximum width of posterior part of oesophagus (82). Distance of nerve ring from anterior extremity (204), representing (43)% of oesophageal length. Deirids and excretory pore (582) and (775), respectively, from anterior end of body. Only one, dorsal, caecum present, (144) long; caecum of one specimen bent posteriorly. Precloacal sucker absent. Preanal papillae: 5 pairs of large subventral papillae present, last two pairs being close together, and 1 pair of large lateral papillae at level of posteriormost subventrals present; postanal papillae: 2 pairs of subventral and 2 pairs of lateral papillae present (Figs 1F, I, J; 2D, G). Anterior cloacal lip with conspicuous median cuticular elevation 9 15 (9) high (Figs 1I; 2D, G). Spicules narrow, slightly subequal, left and right spicule 721 1,020 and 884 1,142 (952 and 979), respectively, long, with nearly pointed distal ends (Fig. 1F, G); length ratio of spicules 1: (1:1.03); larger spicule represents (32)% of body length. Gubernaculum well sclerotized, (75) long (Fig. 1F, H). Tail conical, (120) long, forming narrow elongation (15) long; latter terminating in two (one dorsal and one ventral) sharply pointed spikes and bearing pair of minute lateral cuticular spines at its base (Figs 1I K; 2F). Female (7 specimens, eggs present only in allotype; measurements of allotype in parentheses). Length of body (3.31) mm, maximum width (394). Maximum width of cuticle at oesophageal region (48). Length of entire oesophagus (544); oesophastome (177) long, (136) wide; maximum width of posterior part of oesophagus (109). Distance of nerve ring from anterior extremity (245), representing (45)% of oesophageal length. Deirids and excretory pore (624) and (775), respectively, from anterior end of body. Only one, dorsal, caecum (109) long present in five specimens; two other specimens with two caeca 136/ 122 and 216/120 long. Vulva postequatorial, (1.77) mm from anterior extremity, at (53)% of body length (Fig. 1E). Uterus opposed. Mature eggs oval, thin-walled, with uncleaved content (Fig. 1L); size of eggs (n = 5) ( ). Tail conical, (126) long, forming narrow elongation (15) long; latter terminating in two (one dorsal and one ventral) sharply pointed spikes and bearing pair of minute lateral cuticular spines at its base (Fig. 1D, M); pair of distinct lateral phasmids present at mid-length of tail (Fig. 1M). Type host: Tigertooth croaker, Otolithes ruber (Sciaenidae, Perciformes). Site of infection: Intestine. Type locality: Northwest of Qeshm Island (26º42 26º44 N, 55º30 55º25 E), Persian Gulf, off Iran (collected in April 2013). Other locality: Off Kolahi (27º01 N, 56º41 E), Persian Gulf, off Iran (collected in February 2013). Total prevalence and mean intensity: 62% (8 fish infected/13 fish examined); 8 nematodes per fish. Deposition of types: Holotype, allotype and paratypes in the Helminthological Collection of the Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, České Budějovice (Cat. No. N 1039). Etymology: The Latin specific name of this nematode relates to its characteristic feature, i.e., the presence of cuticular spines on the tail tip (spinigerus = bearing spines).

3 Two nematodes from Otolithes ruber off Iran 231 Fig. 1. Dichelyne (D.) spinigerus sp. nov.: A anterior end of female (specimen with two caeca), lateral view. B anterior end of male (specimen with one caecum), lateral view. C cephalic end of male, lateral view. D tail tip of female, lateral view. E vulva, lateral view. F posterior end of male, lateral view. G distal tip of spicule, lateral view. H gubernaculum, lateral view. I and J posterior end of male, lateral and ventral views. K posterior end of male tail, ventral view. L egg. M tail of female, lateral view

4 232 František Moravec et al. Fig. 2. Dichelyne (D.) spinigerus sp. nov., scanning electron micrographs: A cephalic end, apical view. B and C circumoral denticles of male and female, respectively. D posterior end of male, sublateral view. E deirid. F tail tip of male, lateroventral view. G region of cloacal opening, lateroventral view. Abbreviations: a amphid; b cephalic papilla; c circumoral ala; d preanal papilla; e median precloacal cuticular elevation; f papilla of first postanal pair; s spicule Comments: In accordance with the classification of cucullanids given by Petter (1974), the available specimens belong to the genus Dichelyne Jägerskiöld, 1902; the absence of the ventral sucker and the number of preanal papil- lae show their belonging to the nominotypical subgenus Dichelyne. At present, the subgenus Dichelyne (Dichelyne) includes 18 species parasitic in freshwater, brackish-water and marine

5 Two nematodes from Otolithes ruber off Iran 233 fishes (see Moravec et al. 1999, 2001). Among these, minute cuticular spines on the male tail tip are present only in D. alatae De et Maity, 1995, D. hatwichi Moravec, Wolter et Körting, 1999, D. japonicus Moravec, Nagasawa et Ogawa, 2001, D. longispiculatus Wang et Lin, 1975, D. mexicanus Caspeta-Mandujano, Moravec et Salgado-Maldonado, 1999, D. rasheedae Petter, 1974 and D. spinicaudatus Petter, However, the character of these spines is different in different species. The tail tip of D. alatae, D. mexicanus and D. rasheedae is nondivided, all covered by very numerous minute spines, whereas that of D. hartwichi is nondivided, bearing a ring of few spines at its base (De and Maity 1995; Gibbons and Saayman 1996; Caspeta-Mandujano et al. 1999; Moravec et al. 1999, 2011); a similar ring of spines at base of the tail tip is also present in D. spinicaudatus, but the tail tip terminates in four spikes (Timi et al. 1997); the tail tip of D. longispiculatus terminates in a tricuspidated process (Wang and Lin 1975). The only species resembling D. spinigerus sp. nov. by the structure of the tail tip is D. japonicus, a species decribed from a single male collected in the marine sciaenid fish Argyrosomus argentatus (Houttuyni) off Japan (Moravec et al. 2001). However, both species differ distinctly by the location of deirids and the excretory pore; whereas deirids are situated short distance posterior to the level of nerve ring and the excretory pore at mid-way between the nerve ring and the end of oesophagus in D. japonicus, both the excretory pore and deirids are well posterior to the end of oesophagus in the new species; moreover, D. spinigerus has a somewhat different arrangement of postanal papillae and the males of this new species are considerably larger than the male of D. japonicus (body length vs 1.79 mm). The presence of a distinct inner dorsal hole at the base of oesophastome, which is a characteristic feature of D. spinigerus, has not been described for any other Dichelyne species. Petter and Sey (1997) reported another species, Dichelyne (D.) exiguus (Yamaguti, 1954) from O. ruber (reported as O. argenteus) off Kuwait, mentioning that the same species was previously recorded by Rasheed (1968) from a sciaenid fish Pseudosciaena (?) sp. off the Karachi coast, Pakistan. According to both Rasheed (1968) and Petter and Sey (1997), their nematode specimens had the same structure of the tail tip as that in D. spinigerus, but the deirids were located between the middle and posterior end of oesophagus. However, because the original description of this species given by Yamaguti (1954) distinctly differs from that later provided by Rasheed (1968) and both these forms also differ in the family of fish hosts (Latidae vs Sciaenidae) and the geografical distribution (Sulawesi, Indonesia vs Pakistan), Moravec et al. (1999) proposed to retain this species in Cucullanus Müller, 1777, where it was originally placed. Apparently, the nematodes reported by Rasheed (1968) and Petter and Sey (1997) were other cucullanid species, representatives of Dichelyne. Probably at least the nematodes reported by Petter and Sey (1997) from O. ruber belonged in fact to the presently described D. spinigerus. The description provided by them is inadequte, based only on light microscopy; they illustrated the excretory pore at some distance posterior to the end of oesophagus (similar to that in D. spinigerus) and deirids were not illustrated at all. Family Philometridae Baylis et Daubney, 1926 Philometra otolithi Moravec et Manoharan, 2013 Description: Male (1 specimen). Body filiform, whitish, 2.65 mm long, maximum width at middle 60, somewhat tapering to both ends; no constriction posterior to cephalic end. Maximum width/body length 1:44; width of cephalic end 18, that of posterior end 30. Cuticle smooth. Cephalic end rounded. Oral aperture small, transversely oval, surrounded by 14 small cephalic papillae arranged in two circles: external circle formed by four submedian pairs of papillae; internal circle by four submedian and two lateral papillae. Small lateral amphids just posterior to lateral papillae of internal circle situated on semicircular elevations (Figs 3B; 4A). Oesophagus 378 long, maximum width 21, comprising 14% of body length, slightly inflated at anterior end; posterior part of muscular oesophagus overlapped by well developed oesophageal gland with large cell nucleus in middle (Fig. 3A). Oesophageal nucleus 201 from anterior extremity. Excretory pore hardly visible, situated short distance posterior to level of nerve ring. Testis reaching anteriorly nearly to nerve ring (Fig. 3A). Posterior end of body blunt, with broad, two-lobed, reniform lateral mounds; dorsal ends of these mounds well separated from each other (Figs 3I; 4B D). Four pairs of very flat, hardly visible caudal papillae close to each other situated on sides of cloacal aperture on mounds (Figs 3I; 4D). Pair of small phasmids present near middle of mounds (Figs 3I; 4D). Spicules slender, needle-like, equal, with somewhat expanded proximal and sharply pointed distal tips (Figs 3F; 4B); length of spicules 147, comprising 5.5% of body length. Gubernaculum narrow, 72 long, with anterior portion somewhat dorsally bent; length of anterior bent part 36, representing 50% of entire gubernaculum length; posterior end of gubernaculum with dorsal protuberance and numerous transverse lamella-like structures; dorsal protuberance on gubernaculum appears as single in lateral view but, in fact, it consists of two dorsolateral parts separated from each other by narrow, smooth longitudinal field when observed dorsally (Figs 3C, D, H, F; 4B, C, E, F). Length ratio of gubernaculum and spicules 1:2.04. Spicules and gubernaculum well sclerotized; spicules and gubernaculum yellowish, anterior part of gubernaculum colourless. Length of tail 3. Nongravid female (2 mature specimens). Body length mm, maximum width 45 54; maximum width/ length ratio 1: Width of cephalic end 30 33, of posterior end Entire oesophagus long, 30 wide, representing 12 15% of body length. Anterior oesophageal bulb 36

6 234 František Moravec et al. Fig. 3. Philometra otolithi Moravec et Manoharan, 2013: A anterior end of male, lateral view. B cephalic end of male, apical view. C and D distal end of gubernaculum, lateral and dorsal views. E anterior end of mature female, lateral view. F posterior end of male, lateral view. G posterior end of mature female, lateral view. H gubernaculum, lateral view. I caudal end of male, apical view. J vulva region of mature female, lateral view long, wide. Nerve ring, excretory pore and oesophageal nucleus , and , respectively, from anterior extremity (Fig. 3E). Intestinal ligament long. Vulva and incompletely developed vagina present, former situated from anterior extremity (at 66 69% of body length) (Fig. 3J). Uterus empty. Caudal end rounded (Fig. 3G). Subgravid female. Only body fragments of several subgravid specimens were collected. Their morphology and body size were comparable to those of P. otolithi subgravid specimens previously reported by Moravec et al. (2013). Host: Tigertooth croaker, Otolithes ruber (Sciaenidae, Perciformes). Site of infection: Ovary. Localities: Northwest of Qeshm Island (26º42 26º44 N, 55º30 55º25 E) and off Kolahi (27º01 N, 56º41 E), Persian Gulf and off Bandar-e-Jask (25º32 N, 58º26 E), Sea of Oman, off Iran (collected in February and April 2013). Total prevalence and mean intensity: 26% (6 fish infected/23 fish examined); 4 nematodes per fish. Deposition of voucher specimens: Helminthological Collection of the Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, České Budějovice (Cat. No. N 1002). Comments: This species was described from a single gravid female found in the ovary of O. ruber in the Bay of Bengal, off India (Moravec and Manoharan 2013) and subsequently

7 235 Two nematodes from Otolithes ruber off Iran subgravid and larger nongravid females of this gonad-infecting species of Philometra were recorded from the same host species in the Persian Gulf and the Sea of Oman off Iran (Moravec et al. 2013). The conspecific male and very small mature females of this parasite are described in the present paper for the first time. Fig. 4. Philometra otolithi Moravec et Manoharan, 2013, scanning electron micrographs of male: A cephalic end, apical view. B caudal end, subapical view. C caudal end, dorsal view. D caudal end (another specimen), apical view (arrows indicate phasmids). E region of cloacal opening, sublateral view. F distal tip of gubernaculum, dorsal view. Abbreviations: a amphid; b submedian pair of cephalic papillae of external circle; c submedian cephalic papilla of internal circle; d lateral cephalic papilla of internal circle; e cloacal aperture; f caudal mound; g distal tip of gubernaculum; h group of four flat caudal papillae; o oral aperture; s spicule

8 236 František Moravec et al. The examination of fixed ovaries of six specimens of O. ruber of the present material yielded one complete Philometra otolithi male and a posterior body fragment of another male with missing distal parts of spicules and gubernaculum, in addition to a few conspecific female specimens (mostly fragmented). By the shape and structure of the distal tip of the gubernaculum, i.e., the gubernaculum tip forming a dorsal lamellated protuberance in lateral view, but, in fact, consisting of two dorsolateral parts separated from each other by a narrow, smooth longitudinal field when observe dorsally, P. otolithi is similar only to P. johnii Moravec et Ali, 2013 and P. lopholatili Moravec et Bakenhaster, 2013, both gonad-infecting nematodes of perciform fishes. The former species (P. johnii) was described from Johnius dussumieri (Cuvier) (Sciaenidae) in the Persian Gulf off Iraq (Moravec and Ali 2013) and subsequently it has been reported from Johnius sp. off the northern coast of Australia (Moravec and Diggles 2014), whereas the latter species (P. lopholatili) is a parasite of Lopholatilus chamaeleonticeps Goode et Bean (Malacanthidae) in the Gulf of Mexico (Moravec and Bakenhaster 2013). However, P. lopholatili male distinctly differs from that of P. otolithi in having the caudal mound V-shaped, uninterrupted dorsally (vs caudal mound dorsally interrupted), longer spicules ( vs 147 µm), gubernaculum ( vs 72 µm) and body ( vs 2.65 mm), a different shape of the anterior end of body (with a constriction just posterior to the cephalic end vs without such a constriction), in the host fish family (Malacanthidae vs Sciaenidae) and the geographical distribution (Atlantic region vs Indo-Pacific region). On the other hand, the general morphology and measurements of P. otolithi male are very similar to those of the male of P. johnii and, moreover, both these species are parasitic in hosts belonging to the same fish family (Sciaenidae) and occur in the same region (Persian Gulf). Some differences are only found in the shape of the cephalic aperture (triangular vs transversely oval), structure of the cephalic end (absence vs presence of semicircular elevations near amphids) and the presence (vs absence) of a pair of large caudal papillae in the postcloacal region between lateral caudal mounds. Although the body lengths of gravid females of both these species are practically the same ( and 134 mm), these nematodes distinctly differ from each other by the presence of many conspicuous transverse lamellae in the buccal cavity of P. otolithi, which are absent in P. johnii (see Moravec and Ali 2013; Moravec and Manoharan 2013; Moravec et al. 2013). Acknowledgements. We thank Mr. Mohsen Safaei, Mr. Mohammad Momeni and Mr. Ali Salarpouri for providing sampling facilities. The authors thanks are also due to the staff of the Laboratory of Electron Microscopy, Institute of Parasitology, Biology Centre of the AS CR, České Budějovice for their technical assistance, and to Blanka Škoríková of the same Institute for help with illustrations. This study was partly supported by the Czech Science Foundation (grant No. P505/12/G112) and the Institute of Parasitology, BC AS CR (institutional support RVO: ). REFERENCES Bagherpour A., Afsharnasab M., Mobedi I., Jalali B., Mesbah M Prevalence and intensity of internal parasitic helminthes infecting black sole fish Brachirus orientalis (Bloch and Schneider, 1801) in the Persian Gulf. Iranian Journal of Fisheries Sciences, 10, Caspeta-Mandujano J.M., Moravec F., Salgado-Maldonado G Observations on cucullanid nematodes from freshwater fishes in Mexico, including Dichelyne mexicanus sp. n. 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