Two species of parasitic copepods (Caligidae) new to Japan

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Systematic Parasitology 57: 19–34, 2004. © 2004 Kluwer Academic Publishers. Printed in the Netherlands.

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Two species of parasitic copepods (Caligidae) new to Japan Ju-shey Ho1 , Samuel G´omez2 , Kazuo Ogawa3 & Masato Aritaki4 1 Department of

Biological Sciences, California State University, Long Beach, CA 90840-3702, USA de Ciencias del Mar y Limnolog´ıa, Unidad Acad´emica Mazatl´an, CP 82040, Ap. Postal 811, Mazatl´an, Sinaloa, Mexico 3 Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi, Bunkyo, Tokyo, 113-8657, Japan 4 Miyako Station of Japan Sea-Farming Association, Miyako, Iwate, 027-0097, Japan 2 Instituto

Accepted for publication 11th June, 2003

Abstract Two species of parasitic copepods (Siphonostomatoida: Caligidae), Caligus sclerotinosus Roubal, Armitage & Rohde, 1983, parasitic on red seabream Pagrus major (Temminck & Schlegel), and Lepeophtheirus longiventralis Yü & Wu, 1932, parasitic on spotted halibut Verasper variegatus (Temminck & Schlegel), are redescribed based on material found on their respective hosts cultured in Japan. Both species are new to Japan. Preliminary observation on the occurrence of L. longiventralis indicates that the larval development takes place on the body surface of the host and only the post-mated female migrates into the host’s gill-cavities. Whilst the occurrence of L. longiventralis in Japan can be considered as due to natural causes, the occurrence of C. sclerotinosus is likely due to anthropogenic activities. Introduction

Materials and methods

The Caligidae Burmeister, 1835 (Siphonostomatoida) is the largest family of parasitic Copepoda comprising more than 450 species. Of the 28 recognised genera of the Caligidae, Caligus Müller, 1785 and Lepeophtheirus Nordmann, 1832 are the two largest ones with more than 250 species in the former (Ho et al., 2000) and 107 species in the latter (Ho & Lin, 2001). According to Ho’s (2000) report on the sea-lice of Asia, 28 species of Caligus and 17 species of Lepeophtheirus are known from the fishes of Japan. In this paper we shall add one species each to these two genera, C. sclerotinosus Roubal, Armitage & Rohde, 1983 and L. longiventralis Yü & Wu, 1932. Since both species are reported here for the first time outside of their type-locality and, since some structural details were not mentioned in their original descriptions, a full redescription of each species is given based on this new material from Japan. Inasmuch as both species of sea-lice were found on the cultured fish in Japan, a discussion on their possible origin is also presented.

The parasitic copepods were obtained from the Miyako Station of the Japan Sea-Farming Association (JSFA) located at Miyako, Iwate, and the Oita Institute of Marine and Fisheries Science located at Kamiura, Oita, and preserved in 70% alcohol. They were dissected in a drop of glycerine under a dissecting microscope. The body parts and appendages were mounted on slides, using glycerine as the mountant, and examined under a compound microscope. All drawings were made with the aid of a camera lucida at a magnification up to ×1,000.

Caligus sclerotinosus Roubal, Armitage & Rohde, 1983 Material examined Nine ♀♀ collected on 18 August, 1999 from the body surface of a red seabream Pagrus major (Temminck & Schlegel) cultured at Kamae, Oita Prefecture. Four ♀♀ have been deposited in the National Science Museum

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Figure 1. Caligus sclerotinosus Roubal, Armitage & Rohde, 1983, female. A. habitus, dorsal; B. caudal ramus (3 terminal setae broken), dorsal; C. Genital complex and abdomen, ventral; D. leg 5, ventral. Scale-bars: A, 1 cm; B,D, 100 µm; C, 507 µm.

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Figure 2. Caligus sclerotinosus Roubal, Armitage & Rohde, female. A. antennule, ventral; B. antenna (B1), postantennal process (B2) and maxillule (B3), ventral; C. mandible, lateral; D. maxilla, ventral; E. maxilliped, ventral; F. sternal furca, ventral. Scale-bars: A,B,D,E 204 µm; C, 100 µm; F, 112 µm.

in Tokyo, Japan, with the catalogue number of NSMTCr 15142. Description Female (Figures 1–4) Body (Figure 1A) 2.98 (2.82-3.12) mm long, excluding setae on caudal rami. Cephalothoracic shield sub-

orbicular, slightly wider than long; with truncate central posterior margin. Fourth pediger 3.61 times wider than long. Genital complex (Figure 1C) trapezoidal, distinctly wider than long, with broadly protruded posterolateral corners carrying setae-bearing process (Figure 1D). Abdomen small, wider than long (Figure 1C). Caudal ramus (Figure 1B) nearly as long

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Figure 3. Caligus sclerotinosus Roubal, Armitage & Rohde, 1983, female. A. leg 1, ventral; B. tip of leg 1 exopod, ventral; C. leg 2, ventral. Scale-bars: A, 324 µm; B, 80 µm; C, 500 µm.

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Figure 4. Caligus sclerotinosus Roubal, Armitage & Rohde, female. A. leg 3, dorsal; B. leg 4, ventral. Scale-bars: A, 300 µm; B, 213 µm.

24 as wide, attaching obliquely to abdomen and with longer outer margin, ornamented with 1 setule-bearing papilla on dorsal surface and row of long setules subterminally on inner margin, and armed with 3 short and 3 long terminal setae. Egg-sacs short, containing at most 8 eggs. Antennule (Figure 2A) short, 2-segmented; proximal segment with usual 25 plumose and 2 simple setae on anterodistal surface; distal segment armed with 1 subterminal seta on posterior margin and 11 setae plus 2 aesthetascs (with blunt tip in Figure 2A) on distal margin. Antenna (B1 in Figure 2B) 3-segmented; proximal segment small, with large, spatula-like posteromedial protrusion; middle segment largest but unarmed; distal segment a curved, blunt claw with robust seta in basal region and another slender seta in middle region close to outer edge. Postantennary process (B2 in Figure 2B) large and bluntly pointed; 2 setule-bearing papillae in proximal region; another similar papilla on sternum near by. Mandible (Figure 2C) 4-sectioned, with 12 teeth on medial margin of distal blade. Maxillule (B3 in Figure 2B) comprising papilla bearing 3 unequal setae and robust, bluntly pointed dentiform process with small, basal tooth; triangular plate anterior to base of dentiform process bearing process opposite to basal tooth of maxillule. Postmaxillary area with long, prominent sclerite. Maxilla (Figure 2D) 2-segmented; proximal segment (lacertus) large but unarmed; slender distal segment (brachium) carrying large subterminal, striated membrane on outer edge and 2 unequal elements (short canna and long calamus) terminally. Corpus of maxilliped (Figure 2E) large but unarmed; subchela sharply pointed, with long shaft and short claw; setiform barbell present at base of claw. Sternal furca (Figure 2F) with triangular box and short, broad, diverging tines. Armature of rami of legs 1–4 (Figures 3A,B, 4A,B) as follows (Roman numerals indicating spines and Arabic numerals setae): Exopod Endopod Leg 1 1-0; III,1,3 (vestigial) Leg 2 I-1; I-1; II,I,5 0-1; 0-2; 6 Leg 3 I-0; I-1; III,4 0-1; 6 Leg 4 I-0; III (absent) Coxa of leg 1 (Figure 3A) small and indistinctly separated from basis, with long ventral setule close to outer margin; blunt, tooth-like process at both ends of intercoxal bar (plate) adjacent to inner end of coxa;

basis with long outer and short inner plumose seta; vestigial endopod unarmed and bluntly pointed; first segment of exopod large, with row of long setules on posterior edge and small, spiniform, subterminal seta on anterior margin; element 1 of 4 terminal elements on last segment of exopod small and located subterminally; elements 2 and 3 with accessory process (Figure 3B). Coxa of leg 2 (Figure 3C) small, with spinule-bearing papilla on ventral surface and large, plumose inner seta on posterior edge; basis with small, naked outer seta in addition to a posterior, marginal setule on ventral surface and long narrow membrane on posterior margin; outer edges of both basis and first exopodal segment fringed with large marginal membrane; outer margins of proximal and middle endopod segments fringed with setules; distal segment with patch of spinules on ventral surface close to outer margin. Leg 3 (Figure 4A) protopod (apron) with small outer and large inner plumose setae in addition to corrugated patch and elevated ridge (with serrated edge) near outer margin anterior to lateral, hyaline membrane; posterior margin of basis fringed with hyaline membrane and setule-bearing papilla on ventral surface adjacent to outer and inner ends of this membrane; posterior margin of velum (plate between bases of exopod and endopod) also fringed with hyaline membrane; outerdistal corner of first segment of endopod with spiniform outgrowth. Leg 4 (Figure 4B) protopod with small, plumose, outer seta; pectens on exopod segments at insertion of each of 4 spines. Leg 5 (Figure 1D) represented by 3 small, plumose setae in posterolateral area of genital complex, with 2 located subterminally on process and 1 on papilla at base of process. Male Not collected. Remarks This species was first described by Roubal (1981) based on a single specimen found on the body surface of a surf bream Acanthopagrus australis (Günther) collected from an unspecified local in northern New South Wales, Australia. Due to having ‘only one specimen, of which the furca is damaged and the caudal rami lack setation’, Roubal (1981, p. 33) refrained from assigning it a specific name and documented it as ‘Caligus sp.’. But two years later, with the finding of more specimens from ‘Chrysophrys auratus’ [= Pagurus auratus (Forster), according to Froese & Pauly (2002)] taken off the Coffs Harbour Region of

25 New South Wales, Roubal et al. (1983) supplemented the missing parts and appendages and named the parasite ‘Caligus sclerotinosus, sp. nov’. The parasite has not been sighted since then. The most outstanding characteristic of the present species is the structure of its leg 5. This appendage in Caligus spp. is generally so reduced that it is only represented by a tiny lobe tipped with two small plumose setae adjacent to a seta-bearing knob; but, in C. sclerotinosus, it appears as a prominent ventral process arising from the posterolateral region of the genital complex and armed subterminally with two plumose setae (see Figure 1D). So far as we are aware, only four of more than 250 species of Caligus exhibit a leg 5 as in the present species; these are: C. cordiventris Shiino, 1952; C. parvilatus Kim, 1998; C. reniformis Prabha & Pillai, 1983; and C. tylosuri (Rangnekar, 1956). However, with the possession of a 2-segmented exopod on leg 4 carrying an armature of I-0; III, C. sclerotinosus is easily distinguished from C. parvilatus, where the armature formula is I-0; II, and from C. reniformis, where it is 3-segmented and carrying five spines in total on the exopod. It is distinguishable from C. cordiventris in the structure of the tines on the sternal furka, terminal elements on the exopod of leg 1 and outer spines on the exopod of leg 2. Caligus tylosuri Rangnekar, 1956 was first described by Rangnekar (1956) based on the specimens recovered from the hound needlefish Tylosurus crocodilus crocodilus (Peron & Lesueur) taken off Bombay, India. It was then called ‘Tuxophorus tylosuri n. sp.’ Five years later, the parasite was found again by Pillai (1961) on the same host caught at Vizhingom, India, and he took the opportunity to transfer the species to Caligus, because the parasite lacks a pair of dorsal plates on the fourth pediger and the sternal furca has simple (not bifid) tines. It has the same structure of exopod on leg 4 as C. sclerotinosus. Nevertheless, according to Pillai’s (1961, 1985) redescription of C. tylosuri, it can be easily separated from the present species in having (1) a sternal furca with widely divergent tines, (2) a leg 5 tipped with a plumose seta and a blunt spiniform process, and (3) an elaborately constructed leg 6 comprising a process tipped with three plumose setae and three bluntly pointed projections.

Lepeophtheirus longiventralis Yü & Wu, 1932 Material examined All collected in 1999 from spotted halibut Verasper variegatus (Temminck & Schlegel) cultured at the Miyako Station of the Japan Sea-Farming Association located in Iwate Prefecture: 11 ♀♀ (6 ovigerous, 4 non-ovigerous, 1 pre-adult) on inner side of operculum, collected on 18 March; 45 ♀♀ (41 ovigerous, 4 non-ovigerous) on inner side of operculum, collected on 28 March; 11 chalimus larvae on body surface, collected on 28 March; 12 ♀♀ (1 ovigerous, 11 preadult), 46 ♂♂, and 24 mating pairs on body surface, collected on 5 April; 265 ♀♀ (161 ovigerous, 4 preadult), 1 ♂, and 6 mating pairs obtained on 9 April from freshwater washing of 2 halibut; 631 ovigerous ♀♀ and 5 ♂♂ obtained on 7 June from freshwater washing of 20 halibut. One-hundred and twenty ♀♀ and 2 ♂♂ from the last collection were deposited in the National Science Museum in Tokyo, Japan and received a catalogue number of NSMT-Cr 15141. Description Female (Figures 5–8) Body (Figure 5A) 5.96 (5.54-7.68) mm long, excluding setae on caudal rami. Cephalothoracic shield suborbicular, nearly as long as wide, with anterolateral margin folded as to resemble notch. Fourth pediger 1.71 times wider than long, partly covered by cephalothoracic shield. Genital complex (Figure 5B) distinctly longer than wide, with tapered anterior portion and greatly protruded posterolateral corners. Abdomen large and 1-segmented, distinctly longer (1.65 times) than cephalothoracic shield. Caudal ramus (Figure 5C) 1.41 times longer than wide, ornamented with row of setules on distal part of medial margin and armed with usual 3 short and 3 long setae. Complete egg-sacs c. 3/4 length of body, containing 53 eggs. Anntennule (Figure 6A) short, 2-segmented; proximal segment with 27 plumose setae on anterodistal surface; distal segment armed with subterminal seta on posterior margin and 11 setae plus 2 aesthetascs on distal margin. Antenna (B1 in Figure 6B) 3segmented; proximal segment smallest, armed with large, bluntly pointed posteromedial process; middle segment subrectangular and ornamented with patch of setules near outer border; distal segment with sharply pointed, uncinate claw, carrying 1 seta in proximal region and another seta in middle region. Postantennal

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Figure 5. Lepeophtheirus longiventralis Yü & Wu, 1932, female. A. habitus, dorsal; B. genital complex and abdomen, ventral; C. caudal ramus, ventral; D. leg 5, ventral. Scale-bars: A,B 2 mm; C, 226 µm; D, 500 µm.

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Figure 6. Lepeophtheirus longiventralis Yü & Wu, 1932, female. A. antennule, ventral; B. antenna (B1), postantenna process (B2) and maxillule (B3), ventral; C. mandible, lateral; D. maxilla, ventral; E. maxilliped, ventral; F. sternal furca, ventral. Scale-bars: A, 131 µm; B, 261 µm; C, 100 µm; D,E, 227 µm; F, 142 µm.

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Figure 7. Lepeophtheirus longiventralis Yü & Wu, 1932, female. A. leg 1, ventral; B. tip of leg 1 exopod, ventral; C. leg 2, ventral. Scale-bars: A, 225 µm; B, 100 µm; C, 450 µm.

process (B2 in Figure 6B) small, with 2 setule-bearing papillae in basal region and another similar papilla on adjacent sternum. Rounded protrusion on sternum between bases of antenna and postantennal process. Mandible (Figure 6C) with 12 teeth on medial margin of terminal blade and small notch opposite dentiferous margin. Maxillule (B3 in Figure 6B) comprising papilla bearing 3 unequal setae and bifurcate dentiform process with subspherical knob on base. Maxilla

(Figure 6D) 2-segmented; proximal segment (lacertus) large but unarmed; distal segment (brachium) carrying subterminal, striated membrane on outer edge and 2 unequal elements (short canna and long calamus) terminally. Corpus of maxilliped (Figure 6E) robust but unarmed; subchela sharply pointed, with long claw indistinguishably fused to short shaft; setiform barbell present at base of claw. Sternal furca (Figure 6F) with long box and bluntly pointed, nearly parallel tines.

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Figure 8. Lepeophtheirus longiventralis Yü & Wu, 1932, female. A. leg 3, dorsal; B. exopod of leg 3, dorsal; C. leg 4, ventral. Scale-bars: A, 436 µm; B, 305 µm; C, 450 µm.

30 Armature of rami of legs 1–4 (Figues 7A, C, 8A, C) as follows (Roman numerals indicating spines and Arabic numerals setae): Exopod Endopod Leg 1 1-0; III,1,3 (vestigial) Leg 2 I-1; I-1; II,I,5 0-1; 0-2; 6 Leg 3 I-1; I-1; III,4 0-1; 6 Leg 4 I-0; III (absent) Coxa of leg 1 (Figure 7A) small and indistinctly separated from basis, with tiny setule-bearing papilla on outer edge; basis with outer and inner plumose seta; vestigial endopod a process with broad base; first segment of exopod large, with row of long setules on posterior edge and small spine in anterodistal corner; middle 2 of 4 terminal elements on last segment of exopod finely serrated and with accessory process, element 1 (outermost), also finely serrated and longer than plumose element 4 (innermost); pectens on this segment at base of each of 3 outer terminal elements (Figure 7B). Coxa of leg 2 (Figure 7C) small, with tiny spinule-bearing papilla on ventral surface and large, plumose inner seta on posterior edge; basis with small, naked outer seta in addition to posterior, marginal setule (indicated with arrow in Figure 7C) on ventral surface and large hyaline membrane on posterior margin; outer edges of both basis and first exopodal segment fringed with large marginal membrane; outer margins of endopodal segments fringed with short spinules (see insertion in Figure 7C). Leg 3 (Figure 8A) protopod (apron) with small outer and large inner plumose setae in addition to scalloped area anterior to lateral hyaline membrane; velum and posterior margin of basis fringed with hyaline membrane; segmentation on exopod incomplete (Figure 8B); 2 setule-bearing papillae on protopod adjacent to velum (indicated with arrows in Figure 8A, B). Leg 4 (Figure 8C) protopod large, with plumose seta in outerdistal corner; exopod 2-segmented and much smaller than protopod; proximal segment with setule-bearing papilla on outer margin and pecten at base of outerdistal spine; distal segment with pecten at base of 2 inner spines. Leg 5 (Figure 5D) represented by 3 small, plumose setae on tiny ramus located in vicinity of egg-sac attachment area of genital complex (see Figure 5B). Male (Figures 9–10) Body (Figure 9A) 2.35 (2.28-2.40) mm long, excluding setae on caudal rami. Cephalothoracic shield

slightly (1.07 times) longer than wide (excluding hyaline lateral membranes). Fourth pediger 2.67 times wider than long. Genital complex (1.43 times) wider than long, with postero-ventral ridge tipped with leg 6 (Figure 9B). Abdomen small, 1-segmented and nearly as long as wide. Caudal ramus (Figure 9B) 1.33 times longer than wide. Frontal plate large (Figure 9A), with setule on anterior margin. Antenna (A1 in Figure 10A) 3segmented; proximal segment small, with large corrugated area in medial portion; middle segment large and subglobular, with 2 corrugated pads on ventral surface and 3 corrugated pads on dorsal surface (Figure 10B); distal segment a large, sharp claw with accessory tine and slender seta in middle region and spiniform seta in basal region. Postantennary process (Figure 10A) larger than in female. Dentiform process of maxillule (A2 in Figure 10A) different from that of female in bearing spiniform seta at base of outer tine. Postmaxillary sclerite with corrugated surface (A3 in Figure 10A). Sternal furca (Figure 10C) with small box and large tines. Leg 5 (Figure 9B) represented by 2 closely arranged, seta-bearing papillae on posterolateral margin of genital complex, with anterior papilla bearing 1 seta and posterior papilla 3 setae. Leg 6 (Figure 9B) represented by 3 plumose setae at tip of large lobe on posteroventral surface of genital complex. Remarks The original description of the present species was made by Yü & Wu (1932) based on observation of two female specimens found on the gills of a spotted halibut Verasper variegates (Temminck & Schlegel) collected in the Yellow Sea at Chefoo (now known as Yen-Dai) located in Shandong Province, China. Although details of the appendages were not found in the original description, there is no doubt that the numerous specimens obtained from the same host fish cultured in Japan are identifiable with the species dealt with by Yü & Wu (1932). The most distinctive features of the present species is the possession of a genital complex with its posterolateral corners produced into a large and long process and the presence of a long abdomen which is longer than the cephalothoracic shield. A search into the documented species of Lepeophtheirus revealed that there are only two species with an abdomen like the present species, i.e. longer than the cephalothoracic shield. They are L. elongatus Heegaard, 1962 and L. marcepes Wilson, 1944. However, L. elongatus dif-

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Figure 9. Lepeophtheirus longiventralis Yü & Wu, 1932, male. A. habitus, dorsal; B. genital complex and abdomen, ventral. Scale-bars: A, 1.2 mm; B, 500 µm.

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Figure 10. Lepeophtheirus longiventralis Yü & Wu, 1932, male. A. antenna (A1), postantennary proces (A2), maxillule and postmaxillary pad (A3), ventral; B. middle and terminal segments of antenna, dorsal; C. sternal furca, ventral. Scale-bars: A,B, 100 µm; C, 111 µm.

fers from the present species in having a 3-segmented abdomen and 3-segmented exopod on leg 4. Furthermore, according to Heegaard (1962), L. elongatus is a parasite of elasmobranchs, attaching to ‘the palate and tongue of a Whaler Shark (Galeolamna greyi Owen)’ caught at Rossiter Bay off Western Australia. L. marcepes was recovered from ‘the gills and under

surface of a lemon sole Pleuronectes quadrituberculatus caught in Alitak Bay, Kodiak Island, Alaska’ (Wilson, 1944). Although a detailed description of this species is lacking, from what was presented by Wilson (1944) in the original description, it can be distinguished from L. longiventralis in having (i) a 2-segmented abdomen; (ii) only slightly protruded

33 posterolateral corners of the genital complex; and (iii) a greatly shrivelled exopod of leg 4 with the formula of I-0; II. No comparison of the male is possible between these two species, because the male of L. marcepes is unknown.

Discussion The occurrence of Lepeophtheirus longiventralis on the spotted halibut Verasper varigatus in culture at Miyako Station was so extensive in the spring of 1999 that it provided us with an unexpected opportunity to make observations on the development and distribution of this parasites on its host. The chalimus stages, which appeared in late March, were found only on the body surface of the spotted halibut, and, as in the development of other caligids (Johnson & Albright, 1991; Lin et al., 1996), the male developed faster than the female. Soon after reaching its adult stage, the male started to engage in amplexus with a female while she was still at the chalimus stage of her development. This performance of ‘mate guarding’ was observed in large numbers during the first week of April. By the second week of April, almost no parasites were found on the host’s body surface, but a large number of females carrying egg-sacs were detected in the branchial cavities of the host, with the great majority of them attaching to the inner side of the operculum. Therefore, the female L. longiventralis must have made a post-mating migration from the body surface to the branchial cavities of the host. Inasmuch as both C. sclerotinosus and L. longiventralis were found, respectively, only on cultured red seabream and spotted halibut in Japan, one cannot but suspect that the occurrence of these parasites is due to the importation of live fish for culture in Japan. So far as we are aware, C. sclerotinosus appears to be host-specific to seabreams (Sparidae) and it has never been reported from anywhere other than off the coast of northern New South Wales, Australia (Roubal, 1981; Roubal et al., 1983). From the fact that one of us (JSH) has been conducting examinations of food fishes caught and landed at various fishing ports in Taiwan since 1997 and C. sclerotinosus is yet to be found there, it is almost safe to state that the sparids of Taiwan do not harbour C. sclerotinosus. On the other hand, it is a well-known fact among the fish culturists in Japan that juvenile red seabream have been introduced from Hong Kong for culture in Japan since 1981, this peaked in the period of 1986 to 1988 and

waned about 1992. Although there is no record of the importation of live red seabream from Australia and no C. sclerotinosus has been reported from southern China, it is difficult to believe that the occurrence of C. sclerotinosus on the cultured red seabream in Oita, Japan, is due to the natural process of animal dispersal, when the same species of parasite is not known to occur in the sparids of Taiwan. In other words, an anthropogenic cause cannot be ruled out in the case of the occurrence of C. sclerotinosus on the red seabream cultured in Japan. The spotted halibut V. variegatus is a species of flatfish native to the northwest Pacific, ranging from central Honshu, Japan, to Korea and the East China Sea (Froese & Pauly, 2002). So far as we are aware, the occurrence of L. longiventralis on the wild-caught specimens of halibut has been reported only once in China (Yü & Wu, 1932). At that time, only two ovigerous females were found. Thus, not having been recorded for the last 70 years in China, Korea or Japan, L. longiventralis can be considered a rare natural parasite of spotted halibut. This assumption finds support from the fact that the host fish from the Seto Inland Sea of Japan was examined by Yamaguti (1939) for the copepod parasites, but only ‘Anchistrotos pleuronichthydis’ [= Taeniastrotos pleuronichthydis (Yamaguti)], a gill parasite, was found. Since this is a larger parasite occurring in the same general site on the host, if L. longiventralis there was present on that host, it would not have been overlooked by Yamaguti. The source of the spotted halibut for culture at Miyako, Iwate, was allegedly from the catches in a set net installed in Oh-Funato Bay off Iwate. Although L. longiventralis rarely occurs on wild fish, repeated stocking of the host fish for culture increases the chance of introducing the parasite into the culture system. Just one ovigerous L. longiventralis hidden in the branchial cavity of a stocked halibut is enough to result in a heavy infection. As mentioned above, as many as 53 eggs were found in one egg-string of the ovigerous female; thus, introducing an ovigerous L. longiventralis into the culture system by accident is equivalent to starting a disease problem with at least 106 parasite eggs. A quarantine period for wild fish before stocking for culture should be considered as a way of avoiding this potential problem.

34 Acknowledgements We would like to thank Mr Kengo Ohta of the Miyako Station of the Japan Sea-Farming Association (JSFA) at Miyako, Iwate, and Dr Yutaka Fukuda of the Oita Institute of Marine and Fisheries Science at Kamiura, Oita, for providing us with the specimens dealt with in this report and for general information about fish culture in Japan. The completion of this study was supported by a grant from the Paramitas Foundation to one of us (JSH).

References Froese, R. & Pauly, D. (2002) Fish Base. World Wide Web electronic Publication, www.fishbase.org. Heegaard, P. (1962) Parasitic Copepoda from Australian waters. Records of the Australian Museum, 25, 149–234. Ho, J.-S. (2000) Sea lice (Copepoda, Caligidae): the potential pests to cage aquaculture in Asia. Aquabiology, 130, 442–447. (In Japanese). Ho, J.-S. & Lin, C.-L. (2001) Anuretes grandis sp. n., a caligid copepod (Siphonostomatoida) parasitic on Diagramma pictum (Pisces) in Taiwan, with discussion of Anuretes Heller, 1865. Folia Parasitologia, 47, 227–234. Ho, J.-S., Lin, C.-L. & Chen, S.-N. (2000) Species of Caligus Müller, 1785 (Copepoda: Caligidae) parasitic on marine fishes of Taiwan. Systematic Parasitology, 46, 159–179.

Johnson, S.C. & Albright, L.J. (1991) The developmental stages of Lepeophtheirus salmonis (Krøyer, 1837) (Copepoda: Caligidae). Canadian Journal of Zoology, 69, 929–950. Lin, C.-L., Ho, J.-S. & Chen, S.N. (1996) Developmental stages of Caligus epidemicus Hesitt, a copepod parasite of tilapia cultured in brackish water. Journal of Natural History, 30, 661–684. Pillai, N.K. (1961) Copepods parasitic on South Indian fishes. Pt. 1. Caligidae. Bulletin of the Central for Research Institute, University of Kerala, Trivandrum, 8, 87–130. Pillai, N.K. (1985) The fauna of India. Copepod parasites of marine fishes. Calcutta: Zoological Survey of India, 900 pp. Rangnekar, M.P. (1956) Parasitic copepods from the marine fishes of Bombay. Journal of the University of Bombay (New Series), 24(B), 42–65. Roubal, F.R. (1981) The taxonomy and site specificity of the metazoan ectoparasites on the black bream, Acanthopagrus australis (Günther), in northern New South Wales. Australian Journal of Zoology, Supplementary Series 84, 1–100. Roubal, F.R., Armitage, J. & Rohde, K. (1983) Taxonomy of metazoan ectoparasites of snapper, Chrysophrys auratus (Family Sparidae), from southern Australia, eastern Australia and New Zealand. Australian Journal of Zoology, Supplementary Series 94, 1–68. Wilson, C.B. (1944) Parasitic copepods in the United States National Museum. Proceedings of the United States National Museum, 94, 20–34. Yamaguti, S. (1939) Parasitic copepods from fishes of Japan. Part 4, Cyclopoida, II. Volumen Jubilare Professor Sado Yoshida, 2, 391–415. Yü S.C. & Wu H.W. (1932) Parasitic copepods on the flat-fishes from China. Bulletin of the Fan Memorial Institute of Biology, 3, 55–75. (In chinese).

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