Crustacea: Copepoda: Siphonostomatoida) Parasitic on Sillago Sihama (Actinopterygii: Perciformes: Sillaginidae

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Experimental Parasitology 125 (2010) 55–62

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Experimental Parasitology

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Parabrachiella jarai sp. nov. (Crustacea: Copepoda: Siphonostomatoida) parasitic on Sillago sihama (Actinopterygii: Perciformes: Sillaginidae)

Wojciech Piasecki a,*, Magdalena Młynarczyk a, Craig J. Hayward b,c a Division of Fish Diseases, Faculty of Food Sciences and Fisheries, West Pomeranian University of Technology, ul. Kazimierza Królewicza 4, 71-550 Szczecin, Poland b South Australian Research and Development Institute-Aquatic Sciences and the Australian Seafood Cooperative Research Centre, Lincoln Marine Science Centre, Hindmarsh Street, Port Lincoln, SA 5606, Australia c National Centre for Marine Conservation and Resource Sustainability, University of Tasmania, Locked Bag 1-370, Launceston Tas 7250, Australia article info abstract

Article history: The presently reported study provides a detailed morphological description of the female and the male of Received 10 April 2009 a new species of the genus Parabrachiella—Parabrachiella jarai sp. nov. The parasites were sampled from Received in revised form 24 September 2009 marine ﬁsh, silver sillago, Sillago sihama (Perciformes: Sillaginidae), captured in Malaysia in 1994 and Accepted 14 October 2009 Hong Kong in 1995. The new species bears some resemblance to Parabrachiella lata (Song et Chen, Available online 20 October 2009 1976) but differs from it in details of second antenna, mandible, and maxilliped. The genus Parabrachiella currently covers 67 species including those recently transferred from Neobr- Keywords: achiella Kabata, 1979. An amended generic diagnosis is proposed for Parabrachiella and Thysanote. Some Parasite members of Parabrachiella are herewith transferred to Thysanote and some Thysanote are now placed in New species Copepoda Parabrachiella. Parabrachiella Ó 2009 Elsevier Inc. All rights reserved. Thysanote Fish Sillago sihama Sillaginidae

1. Introduction site species, which turned out to be a new species. One of the host fishes studied (Sillago sihama) hosted two species of the genus Lernaeopodid copepods (Copepoda: Lernaeopodidae) are para- Parabrachiella. One of them was P. sihama, while the other repre- sites of predominantly marine fishes, but they also infect freshwa- sented species hitherto unknown to science. The latter species is ter and brackish water species. They are one of the largest families described below as Parabrachiella jarai sp. nov. of parasitic copepods (some 250 valid species) and most exten- Another, closely related, genus is Thysanote Krøyer, 1863. Fe- sively adapted to parasitism (Kabata, 1986). Lernaeopodids are also males belonging to this genus have distinct fimbriate posterior- very host specific. and maxillary processes (Piasecki et al., 2008). The structure of Only recently the genus Parabrachiella regained its senior posi- the male body is the same as in the genus Parabrachiella. Surpris- tion. Twenty years ago Kabata (1979) established the genus Neobr- ingly, some species without maxillary processes traditionally be- achiella, to accommodate selected species of the genus Brachiella, longed to Thysanote and vice versa—species with maxillary as well as species previously assigned to other genera such as processes have been assigned to Neobrachiella. The need for pre- Parabrachiella, Probrachiella, Epibrachiella, Branchiellina, Lernaeo- paring a checklist for species of Parabrachiella prompted us to pro- poda, and Isobranchia. Boxshall and Halsey (2004) noticed that pose the species transfers, between two above-mentioned genera, the name Parabrachiella Wilson, 1915 should have priority over where necessary. the name Neobrachiella Kabata, 1979. Therefore all of the former Neobrachiella species require a transfer to Parabrachiella. 2. Materials and methods One of us (CJH) surveyed fish, in the frames of his PhD studies, and collected a number of parasite specimens, including crusta- The parasites were sampled from the operculum of a marine ceans. The presently reported study focuses on one of those para- fish, silver sillago, Sillago sihama (Forsskål) (Perciformes: Sillagini- dae), captured in Malaysia (40 fish) and Hong Kong (38 fish) in * Corresponding author. Fax: +48 91 449 6657. 1994 and 1995, respectively. Examination of specimens of related E-mail addresses: [email protected], [email protected] (W. Piasecki). sillaginids occurring in South-East Asia (Sillago parvisquamis,

S. soringa, S. aeolus, S. chondropus, and Sillaginopsis panijus) and Mandible (Fig. 8) typically siphonostome with 9 teeth. Dental Middle East (Sillago arabica, S. attenuata) did not reveal those cope- formula: P2, S1, P1, S1, B4. pods, and nor was the species present on S. sihama sampled from First maxilla (Fig. 9) biramous with small endopod and promi- any other localities in South-East Asia, Middle East, eastern Africa, nent tripartite exopod. Endopod composed of short digitiform pro- Australia, and islands in the western Pacific Ocean, or on any of a cess surmounted with two setae: small terminal and larger total of 25 other sillaginid species examined. The study material subterminal. Exopod tripartite with two big digitiform processes consisted of ovigerous- and non-ovigerous females and males at- and short third one. Processes ending with conical elongate setifer- tached to females. The material studied were 10 copepod females ous processes. and 3 males from Hong Kong and 1 female from Malaysia. The Second maxillae (Fig. 10) completely fused together and form- copepods were studied under a compound microscope using a ing ‘‘maxillary trunk”. In fixed specimens contracted and wrinkled. modified ‘‘wooden slide” method of Humes and Gooding (1964). Paired openings of maxillary glands visible at base, ventrally. Details of all appendages were illustrated and described. The types Small, mushroom-shaped bulla partly hidden inside terminal collar are deposited in the Museum für Naturkunde in Berlin, Germany. (Figs. 3, 4, and 10). Terminology of the body parts is consistent with that proposed Maxilliped (Figs. 11 and 12) subchelate with robust corpus and by Kabata (1979) (with some exceptions). Appendage abbrevia- long slender subchela. Corpus robust, covered by thick, wrinkled tions used throughout the text are as follows: first antenna = A1, cuticle. On its medial side single process with seta and denticulate, second antenna = A2, mandible = Mdb, first maxilla = Mx1, second semispherical pad. Subchela sub-cylindrical with single ventral maxilla = Mx2, maxilliped = Mxp. seta. Claw large (constituting almost 1/3 of subchela) with second- The siphonostomatoid mandibular dental formula (Siphonosto- ary tooth. Large auxiliary seta at base of claw, medially. matoida including Lernaeopodidae) used here was first introduced Thoracic appendages not observed. by Kurtz (1877). Kabata (1979) proposed its Anglicized version Caudal rami (Figs. 1–4) probably represented by ventral pair of which has been widely used ever since. The tip of mandible has a posterior processes. Genital process (Fig. 13) consisting of two con- row of denticles on one edge. The anterior section is occupied by ical parts partly fused together with attached spermatophores larger, primary teeth (P) with distinct interdenticular spaces. (Fig. 14) in some females examined. Sometimes those spaces feature much smaller, secondary (S) teeth. MALE (Figs. 3 and 15–22) distinctly smaller than female Posterior denticles are smaller, usually uniform in size and shape (Fig. 15); representing male structural type A (Kabata, 1979); con- (sometimes diminishing posteriorly) and they are called basal sisting of two major parts: cephalosome (0.57 mm long) and gen- teeth (B). The dental formula shows the sequence of those teeth ital trunk (0.65 mm long). Long axis of genital trunk inclined at starting from distalmost tooth (e.g., P2, S1, P1, S1, B4.). almost right angle to long axis of cephalosome. Appendages ar- Valid scientific names of host fishes were determined using ranged in undisturbed order: A1, A2, Mdb, Mx1, Mx2, Mxp. FishBase (Froese and Pauly, 2009). First antenna (Fig. 16) three-segmented. Basal segment longest with small seta (whip). Terminal segment with well developed armature consisting of 4 setae and 1 tubercle. 3. Results Second antenna (Fig. 17) biramous, elongate. Sympod cylindrical, unarmed. Bulbous, one-segmented, unarmed exopod dis- 3.1. Parabrachiella jarai sp. nov. (Figs. 1–22) tinctly shorter than endopod. Endopod two-segmented with basal segment with denticulate pad. Terminal segment with well FEMALE (Figs. 1–14). Body typically lernaeopodid (Figs. 1–4), developed lernaeopodid armature consisting of big, curved claw consisting of three distinct parts: cephalosome, genital trunk, and 1, big seta 2, tubercle 3 (at base of seta 2), denticulate pad 4, maxillary ‘‘trunk” (fused Mx2). Cephalosome elongate, 2.11 mm and big seta 5. long (1.96–2.25 mm), regularly cylindrical; on fixed specimens Mandible (Fig. 18) typical siphonostome with 9 teeth. Dental flexed dorsally. Genital trunk sub-spherical, or drop-shaped, formula: P2, S1, P1, S1, B5 (last basal tooth small). 2.25 mm long (1.88–2.39 mm), 1.5 mm wide (1.37–1.68 mm); its First maxilla (Fig. 19) similar as in female, although more slen- length slightly exceeding length of cephalosome. Posterior part der. Endopod terminating with 2 equal small setae. outfitted with two pairs of digitiform posterior processes, one of Second maxilla (Fig. 20) subchelate (made of strong thick cuti- which possibly representing caudal rami. Relative length of pro- cle) with robust pyriform corpus and strong subchela. Corpus un- cesses variable, approximating trunk width or even length armed. Subchela with well delimited, powerful claw, and slightly (Fig. 4). Small but distinct genital process present between poster- shorter cylindrical shaft. Subchela closing against large bulbous ior processes. Egg sacs multiseriate, twice as long as genital trunk. outgrowth of corpus. Maxillary ‘‘trunk” relatively short. Appendages (except Mx2) situ- Maxilliped (Fig. 21) subchelate, similar in structure to second ated at distal end of cephalosome. Anteriormost second antennae maxilla but stronger in appearance. Subchela very robust with followed by first antennae and mouth cone with inserted mandi- claw positioned at right angle to shaft. Closed subchela partly hid- bles and flanked by first maxillae. Second maxillae displaced ante- ing tip of claw behind medial outgrowth of corpus. riorly in front of maxillipeds and located closely behind mouth Thoracic appendages not observed. cone. Caudal rami (Fig. 22) partly hidden in depression of cuticle; First antenna (Fig. 5) sub-cylindrical; three-segmented. Basal consisting of paired conical outgrowths with obscure segmentation segment almost as long as two other segments combined, and and no additional setation. armed subterminally with single seta (whip). Terminal segment Type host: Sillago sihama (Forsskål). with well developed terminal armature, consisting of three long Site of infection: Inner surface of operculum. setae and three tubercles. Type locality: Sai Kung, Hong Kong. Second antenna (Figs. 6 and 7) biramous. Robust, cylindrical Prevalence and intensity: 40 host fish from Sai Kung, Hong Kong sympod unarmed. Bulbous, one-segmented, unarmed exopod dis- (December 1995) were infected by 10 females (and 3 males at- tinctly longer and thicker than endopod. Endopod two-segmented tached to them) from; 38 host fish from Cendering, Malaysia (April with small, almost straight claw 1, aligned with long axis of endo- 1994) yielded 1 parasite female. pod, small seta 2, seta 5 and prominent denticulate pad 4 (Figs. 6 Etymology: The specific name of the new species is intended to and 7). honour Professor Zbigniew J. Jara (1918–2008)—a renowned Polish W. Piasecki et al. / Experimental Parasitology 125 (2010) 55–62 57

Figs. 1–9. Parabrachiella jarai sp. nov. female. Fig. 1. Ovigerous specimen; whole. Fig. 2. Nonovigerous specimen; whole. Fig. 3. Ovigerous specimen (holotype); whole with male (allotype) attached. Fig. 4. Another non-ovigerous specimen; whole. Fig. 5. First antenna. Fig. 6. Second antenna; whole. Fig. 7. Second antenna; endopod. Fig. 8. Mandible. Fig. 9. First maxilla. Abbreviations: DP – dorsal papilla; M – male; 1, 2, 3, 4, 5 – armament of endopod of second antenna (according to Kabata, 1979). Scale bars in mm.

ﬁsh pathologist and parasitologist (Lonc, 2004; Olech and Piasecki, 4. Discussion 2009). Deposition of types: Holotype, allotype, and 5 paratypes have The morphology of the presently described new species bears been deposited in the Museum für Naturkunde in Berlin (ZMB the closest resemblance (in overall appearance) to P. lata (Song et 27689) (all type specimens under a single number). Chen, 1976). The differences, however, in the structure of append- 58 W. Piasecki et al. / Experimental Parasitology 125 (2010) 55–62

Figs. 10–14. Parabrachiella jarai sp. nov.; female; appendages. Fig. 10. Second maxilla. Fig. 11. Maxilliped. Fig. 12. Maxilliped (from another specimen). Fig. 13. Genital process. Fig. 14. Spermatophore. Abbreviations: B – bulla; MG – maxillary gland. Scale bars in mm. ages of both males and females are distinct and explicit (Song and would be impractical and premature. It should be emphasized that Chen, 1976; Roubal, 1981; Ho et al., 2007) and they cover: (1) many of the existing species have been inadequately described and shape of ‘‘torso” (base of Mx2) (plain in P. jarai female vs. distinct illustrated. Therefore those species have to be re-described before lateral lobes/inflations in P. lata; (2) unarmed A2 exopod in P. jarai any reliable key is proposed. Moreover, a number of specimens, female (vs. denticulate area in P. lata); (3) different dental formulas previously re-described under well established names represent of female Mdb (P2, S1, P1, S1, B4 in P. jarai (vs. P1, S1, P1, S1, P1, S1, probably new species and we are going to focus on them our future B5 in P. lata); (4) single denticulate pad on medial side of Mxp cor- studies. pus of female in P. jarai (vs. two denticulate pads in P. lata); (5) un- The presently described new species has been assigned to armed exopod of male A2 in P. jarai (vs. two spiniform setae and Group 2. This group is the largest, consisting of 35 members denticulate pad in P. lata. (6) different dental formulas of male (including the new species): P. albida, P. anisotremi, P. auriculata, Mdb (P2, S1, P1, S1, B5 in P. jarai vs. P4, S1, B5 in P. lata). Moreover, P. bera, P. brevicapita, P. chavesii, P. chevreuxii, P. dentici, P. dispar, P. lata was found on ‘‘Sparus latus”=Acanthopagrus latus (Houttuyn, P. elegans, P. fasciata, P. gracilis, P. gulosa, P. hoi, P. hostilis, P. indica, 1782) (family Sparidae), while P. jarai parasitized Sillago sihama P. insidiosa, P. jarai sp. nov., P. johnii, P. lata, P. lutiani, P. menticirrhi, (family Sillaginidae). P. merluccii, P. multifimbriata P. oralis, P. otolithi, P. paralichthyos, P. Parabrachiella jarai n. sp. is very host specific. Of 26 sillaginid regia, P. richiardii, P. rotunda, P. sciaenae, P. seriolae, P. sihama, P. species examined by one of the authors (CJH) throughout the trichiuri, and P. yongxingensis. Indo-West Pacific, ranging from East Africa to Australia, New Cale- The identity of a number of Parabrachiella species should be donia and Japan, it parasitized only one: Sillago sihama, and was reconsidered. Some specimens used for redescriptions, especially only found at two locations that this species was examined, both those found on different hosts should be re-examined. Among in South-East Asia. them are ‘‘Neobrachiella pillai Kabata et Tareen, 1987” (=Parabrachi- The number of species of the genus Parabrachiella considered ella lutiani (Tripathi, 1962)), the ‘‘short form” of ‘‘Neobrachiella valid by the present authors is 67 (Table 1). Castro Romero and rostrata” found by Rubec (1988) on Greenland halibut, Reinhardtius Baeza Kuroki (1987) provided a key to females of those species hippoglossoides, and the long-armed form of P. annulata (Mark- (at that time members of the genus Neobrachiella). They proposed ewitsch, 1940) sensu Ho (1975). a tentative division into three groups, based on the number of pos- P. chevreuxii (van Beneden, 1891), described from an uncon- terior processes (including caudal rami): GROUP I (2 pairs), GROUP firmed and unlikely host (‘‘Squalus sp.”) is certainly not a species II (1 pair), and GROUP III (more than 2 pairs). We concluded that described from sciaenid fishes by Brian (1906) and Kabata (1966, constructing an updated key for such high number of species 1979). It has differing structure and body proportions. The sciaenid W. Piasecki et al. / Experimental Parasitology 125 (2010) 55–62 59

Figs. 15–22. Parabrachiella jarai sp. nov.; male; whole; lateral. Fig. 15. Whole; lateral. Fig. 16. First antenna. Fig. 17. Second antenna; whole. Fig. 18. Mandible. Fig. 19. First maxilla. Fig. 20. Second maxilla. Fig. 21. Maxilliped. Fig. 22. Caudal rami. Abbreviations: 1, 2, 3, 4, 5 – armament of endopod of second antenna (according to Kabata, 1979). Scale bars in mm. parasite should be referred to as P. sciaenae (Brian, 1906) comb. probably represents an unknown species. New specimens are nov. needed, however, to describe missing details of its morphology. ‘‘Neobrachiella sp.”, described by Piasecki (1993) from a Califor- As mentioned earlier, some representatives of the genus Thysa- nia halibut, Paralichthys californicus, from southern California, note bear a close resemblance to those of the genus Parabrachiella. 60 W. Piasecki et al. / Experimental Parasitology 125 (2010) 55–62

Table 1 List of all valid species of Parabrachiella with their principal data (host data for original record only).

Valid name Original name Type host Host family Type locality 1 P. albida (Rangnekar, 1956) Charopinus ‘‘Pseudoscieana albida” = Daysciaena albida (Cuvier, Sciaenidae Indian Ocean, Bombay albidus 1830) 2 P. amphipacifica (Ho, 1982) Neobrachiella Psychrolutes phrictus Stein et Bond, 1978, P. sio Psychrolutidae Pacific N. amphipacifica Nelson, 1980 3 P. anisotremi (Castro Romero et Brachiella Anisotremus scapularis (Tschudi, 1846) Haemulidae Pacific S., Chile, Antofagasta Baeza Kuroki, 1989) anisotremi 4 P. annulata (Markewitsch, 1940) Brachiella Ereunias grallator Jordan et Snyder, 1901 Ereuniidae Pacific N., Japan, Misaki annulata 5 P. anserina (Wilson, 1908) Brachiella ‘‘Sebastodes glaucus”=Sebastes glaucus Hilgendorf, Sebastidae Pacific N., off Bering Island anserina 1880 6 P. auriculata (Castro Romero et Neobrachiella ‘‘Sciaena gilberti”=Cilus gilberti (Abbott, 1899) (and Sciaenidae Pacific S., Chile Baeza Kuroki, 1987) auriculata S. deliciosa) 7 P. bera (Yamaguti, 1939) Brachiella bera ‘‘Halichoeres poecilopterus”=Parajulis poecilepterus Labridae Pacific N., Japan Tarumi (Temminck et Schlegel, 1845) 8 P. bispinosa (von Nordmann, Brachiella ‘‘Gadus sp.” (misidentification possible) Trigla sp. Triglidae Atlantic N. ??? 1832) bispinosa (according to Kabata 1979) 9 P. brevibrachiata (Kabata, 1992) Neobrachiella ‘‘Trypterophycis intermedius”=Tripterophycis Moridae Pacific S., Australia, Port Kembla brevibrachiata gilchristi Boulenger, 1902 NSW 10 P. brevicapita (Ho et Do, 1984) Neobrachiella Nibea albiflora (Richardson, 1846) Sciaenidae Pacific N., Japan, Kojima Bay brevicapita 11 P. chavesii (van Beneden, 1891) Brachiella ‘‘Ceratopterus sp.” = Manta birostris (Walbaum, Elasmobranchii: Atlantic N., Azores chavesii 1792) (misidentification possible) Rajiformes: Myliobatidae 12 P. chevreuxii (van Beneden, 1891) Brachiella ‘‘Squalus sp.” (misidentification possible) Elasmobranchii: Atlantic N., Senegal chevreuxii Squaliformes: Squalidae 13 P. chlorophthalmi (Kabata, 1992) Neobrachiella ‘‘Chlorophthalmus nigripinnis”=Paraulopus Paraulopidae Pacific S., Australia New South chlorophthalmi nigripinnis (Günther, 1878) Wales 14 P. cirrocauda (Heegaard, 1962) Brachiella ‘‘Physiculus barbatus”=Pseudophycis barbata Moridae Pacific S., Australia, Victoria, cirrocauda Günther, 1863 Corner Inlet 15 P. dentici (Nunes Ruivo, 1962) Brachiella dentici ‘‘Dentex filosus”=Dentex gibbosus (Rafinesque, Sparidae Atlantic S., Angola 1810) 16 P. dispar (Castro Romero et Baeza Neobrachiella ‘‘Sciaena gilberti”=Cilus gilberti (Abbott, 1899) Sciaenidae Pacific S., Chile, Antofagasta Kuroki, 1987) dispar 17 P. elegans (Richiardi, 1880) Brachiella elegans Lichia amia, L. gauca, Seriola lalandi Carangidae Atlantic N. Mediterranean 18 P. exigua (Brian, 1906) Brachiella exigua Pagellus erythrinus (L.) Sparidae Atlantic N., Mediterranean Sea, off Napoli 19 P. exilis (Shiino, 1956) Epibrachilla exilis ‘‘Kyphosus lembus”=Kyphosus vaigiensis (Quoy et Kyphosidae Pacific N., Japan, Nagaturo Gaimard, 1825) 20 P. fasciata (Castro Romero et Neobrachiella Sciaena fasciata (Tschudi, 1846) Sciaenidae Pacific S., Chile, Antofagasta Baeza Kuroki, 1987) fasciata 21 P. genypteri (Capart, 1959) Brachiella Genypterus capensis (Smith, 1847) Ophidiidae Atlantic S., Namibia, Fort Rock genypteri Point 22 P. gracilis (Wilson, 1908) Brachiella gracilis ‘‘Cynoscion nobilis” Atractoscion nobilis (Ayres, 1860) Sciaenidae Pacific N., California S. 23 P. gulosa (Wilson, 1915) Brachiella gulosa Sciaenops ocellatus (Linnaeus, 1766) Sciaenidae Atlantic N., USA East coast 24 P. gymnobrachiata (Kabata, 1968) Thysanote Epinephelus merra Bloch, 1793 Serranidae Pacific S., Australia, Heron Island gymnobrachiata 25 P. hoi (Piasecki, 1993) Neobrachiella hoi Chilara taylori (Girard, 1858) Ophidiidae Pacific N., California S. 26 P. hoplognathi (Yamaguti, 1939) Epibrachiella ‘‘Hoplognathus sp.” = Oplegnathus sp. Oplegnathidae Pacific N., Japan, Suruga Bay hoplognathi 27 P. hostilis (Heller, 1868) Anchorella Umbrina cirrosa (L.) Sciaenidae Atlantic N., Mediterranean Sea hostilis 28 P. hugu (Yamaguti, 1939) Clavellopsis hugu ‘‘Spheroides rubripes”=Takifugu rubripes (Temminck Tetraodontidae Pacific N., Sea of Japan et Schlegel, 1850) 29 P. incurva Shiino, 1956 ‘‘Kyphosus lembus”=Kyphosus vaigiensis (Quoy et Kyphosidae Pacific N., Japan Seto Gaimard, 1825) 30 P. indica (Tripathi, 1962) Brachiella indica ‘‘Sciaena glauca”=Johnius glaucus (Day, 1876) Sciaenidae Indian Ocean, India, Puri 31 P. insidiosa (Heller, 1868) Brachiella ‘‘Gadus sp.” Gadidae Atlantic N., Mediterranean Sea, insidiosa Adriatic 32 P. intermedia (Bere, 1936) Brachiella Sciaenops ocellatus (Linnaeus, 1766) Sciaenidae Atlantic N., Gulf of Mexico intermedia 33 P. jarai sp. nov. Sillago sihama (Forsskål, 1775) Sillaginidae Pacific N., Hong Kong 34 P. johnii (Yamaguti, 1939) Clavellopsis johni ‘‘Johnius goma”=Protonibea diacanthus (Lacepède, Sciaenidae Pacific N., East China Sea 1802) 35 P. kabatai (Luque et Farfan, 1991) Neobrachiella Isacia conceptionis (Cuvier, 1830) Haemulidae Pacific S., Peru, Chorrillios kabatai 36 P. lata (Song et Chen, 1976) Brachiella lata ‘‘Sparus latus”=Acanthopagrus latus (Houttuyn, Sparidae Pacific N., China, Hainan Dao, 1782) Sanya 37 P. lutiani (Pillai, 1968) Brachiella indica ‘‘Lutianus sp.” = Lutjanus sp. Lutjanidae Indian Ocean, India Pillai, 1968 38 P. menticirrhi (Luque et Farfan, Neobrachiella Menticirrhus ophicephalus (Jenyns, 1840) Sciaenidae Pacific S., Peru, Chorrillios 1990) menticirrhi 39 P. merluccii (Bassett-Smith, 1896) Brachiella ‘‘Gadus merluccius”=Merluccius merluccius (L.) Merlucciidae Atlantic N., UK, Plymouth merluccii 40 P. microdigitata (Kabata, 1992) Neobrachiella ‘‘Helicolenus papillosus”=Scorpaena papillosa Scorpaenidae Pacific S., Australia, New South microdigitata (Schneider et Forster, 1801) Wales W. Piasecki et al. / Experimental Parasitology 125 (2010) 55–62 61

Table 1 (continued)

Valid name Original name Type host Host family Type locality 41 P. mirifica (Kabata, 1992) Neobrachiella ‘‘Hoplichtys haswelli”=Hoplichthys haswelli Hoplichthyidae Pacific S., Australia, New South mirifica McCulloch, 1907 Wales 42 P. mitrata (Wilson, 1915) Brachiella mitrata ‘‘Lopholatilus chameleonticeps” = Lopholatilus Malacanthidae Atlantic N., USA, Massachusetts chamaeleonticeps Goode et Bean, 1879 43 P. mugilis (Kabata, Raibaut et Ben Eubrachiella ‘‘Mugil auratus”=Liza aurata (Risso, 1810) Mugilidae Atlantic N., Mediterranean Sea, Hassine, 1971) mugilis Lake of Tunis (lagoon) 44 P. multifimbriata (Basset-Smith, Brachiella Serranus sp. Serranidae Indian Ocean, Oman, Muscat 1898) multifimbriata 45 P. nitida (Wilson, 1915) Brachiella nitida Albatrossia pectoralis (Gilbert, 1892) Macrouridae Pacific N. 46 P. oralis (Castro Romero et Baeza Neobrachiella Sciaena deliciosa (Tschudi, 1846) Sciaenidae Pacific S., Chile Kuroki, 1987) oralis 47 P. otolithi (Pillai, 1962) Brachiella otolithi ‘‘Otolithus argenteus”=Otolithes ruber (Bloch et Sciaenidae Indian Ocean, India, Kerala Schneider, 1801) 48 P. paralichthyos (Castro Romero et Neobrachiella Paralichthys adspersus (Steindachner, 1867) Paralichthyidae Pacific S., Chile Baeza Kuroki, 1986) paralichthyos 49 P. pinguis (Wilson, 1915) Brachiella pinguis ‘‘Antimora viola”=Antimora microlepis Bean, 1890 Moridae Atlantic N., Newfoundland S. 50 P. regia (Lewis, 1967) Brachiella regia ‘‘Lampris regius”=Lampris guttatus (Brünnich, 1788) Lampridae Pacific N., Hawaii 51 P. richiardi (Ben Hassine et Brachiella Umbrina cirrosa (L.) Sciaenidae Atlantic N., Mediterranean Sea, Raibaut, 1978) richiardi Tunis 52 P. robusta (Wilson, 1912) Clavella robusta ‘‘Sebastodes auriculatus”=Sebastes auriculatus Sebastidae Pacific N. Canada, Nanaimo BC Girard, 1854 53 P. rostrata (Krøyer, 1837) Brachiella Hippoglossus hippoglossus (L.) Pleuronectidae Atlantic N., Kattegat rostrata 54 P. rotunda (Pearse, 1952) Brachiella Prionotus tribulus crassiceps Ginsburg, 1950 Triglidae Atlantic N., Gulf of Mexico, Texas rotunda 55 P. sciaenae (Brian, 1906) Clavella sciaenae Sciaena antarctica??? (in 1923 – ‘‘Sciaena aquilla”) Sciaenidae Atlantic N. ??? 56 P. septicauda (Shiino, 1956) Epibrachiella Doederleinia berycoides (Hilgendorf, 1879) Acropomatidae Pacific N., Japan, Mie Pref. septicauda 57 P. seriolae (Yamaguti et Yamasu, Brachiella seriolae Seriola quinqueradiata Temminck et Schlegel, 1845 Carangidae Pacific N., Japan 1960) 58 P. sihama Song et Chen, 1976 Sillago sihama (Forsskål, 1775) Sillaginidae Pacific N., China, Hainan Dao, Sanya 59 P. spinicephala Ringuelet, 1945 ‘‘Pinguipes fasciatus”=Pinguipes brasilianus Cuvier, Pinguipedidae Atlantic S., Mar del Plata 1829 60 P. stellifera (Heegaard, 1962) Brachiella Sphaeroides sp. Tetraodontidae Indian Ocean, Western Australia stellifera 61 P. sublobulata (Barnard, 1955) Epibrachiella Congiopodus torvus (Gronow, 1772) Congiopodidae Atlantic S., Africa, S., Table Bay sublobulata 62 P. superba (Leigh-Sharpe, 1934) Brachiella Malacocephalus laevis (Lowe, 1843) Macrouridae Pacific S. (Indian Ocean); Flores superba Sea 63 P. supplicans (Barnard, 1955) Brachiella Genypterus capensis (Smith, 1847) Ophidiidae Atlantic S., South Africa, supplicans Table Bay 64 P. tetrici (Kabata, 1968) Brachiella tetrici ‘‘Pseudolabrus tetricus”=Notolabrus tetricus Labridae Indian Ocean, Australia, Port (Richardson, 1840) Willunga 65 P. trichiuri (Yamaguti, 1939) Clavellopsis Trichiurus japonicus L. Trichiuridae Pacific N., Japan Toyama Bay trichiuri 66 P. triglae (Claus, 1860) Brachiella triglae Trigla sp. Triglidae Atlantic N. ??? 67 P. yongxingensis (Song et Chen, Brachiella Lethrinus sp. Lethrinidae Pacific N., South China Sea 1976) yongxingensis Yongxing Dao, Xisha Quandao

The males in both genera look alike. We believe that the existing tioned species to the genus Thysanote as Thysanote papillosa (Pear- diagnosis of the genus Thysanote (cf. Kabata and Tareen, 1981)is se, 1952) comb. nov. Consequently, also Neobrachiella impudica impractical. According to those authors the principal reason for (von Nordmann, 1832) should become Thysanote impudica (von retaining Thysanote is the pattern of mandibular denticulation, Nordmann, 1832) comb. nov. allegedly more primitive in Thysanote (2–3 secondary teeth in Neo- Many researchers referring to the posterior processes of Parbr- brachiella versus 1–2 in Thysanote). The majority of nominal species achiella tend to treat one of the pairs as caudal rami (‘‘uropods”). assigned to Thysanote and Parabrachiella have been recorded only Such reasoning may not always be reliable. According to Ho et al. once or twice. Many descriptions contain inadequate (or non-reli- (2007), who first studied a complete life cycle of a Parabrachiella, able) data on the mandible. Consequently, if the mandibular crite- the posterior processes, not being caudal rami, are not present at rion is preserved, the status of many species will remain any of the chalimus stages and they are apparently formed after unresolved. We propose, herewith, to disregard the mandibular the last moult. criterion and to distinguish between the two genera based on the Copepods of the genus Parabrachiella seem to be highly host presence of posterior- and maxillary processes in Thysanote and specific, infecting single fish species (or only a few closely related only posterior processes in Parabrachiella. Consequently, P. multif- hosts). They have been recorded from various teleost fishes, repre- imbriata (Bassett-Smith, 1898) comb. nov. and P. gymnobrachiata senting an extensive set of the families. The most frequently in- (Kabata, 1968) comb. nov. are herewith transferred from Thysa- fected family is the Sciaenidae, hosting as many as 16 species, note. On the other hand, we noticed that ‘‘Branchiellina papillosa followed by Sparidae with 3 species. Three Parabrachiella species Pearse, 1952” is very similar to Thysanote chalermwati Piasecki, have been found in representatives of Moridae, Ophidiidae, and Ohtsuka et Yoshizaki, 2008 in the size, shape, and distribution of Triglidae. Two species have been recorded in Carangidae, Haemu- the processes. Therefore we propose to transfer the earlier men- lidae, Kyphosidae, Macrouridae, Labridae, Sebastidae, Serranidae, 62 W. Piasecki et al. / Experimental Parasitology 125 (2010) 55–62

Sillaginidae, Tetraodontidae, whereas a number of families (such as Castro Romero, R., Baeza Kuroki, H., 1987. Four new species of Neobrachiella Acropomatidae, Congiopodidae, Ereuniidae, Gadidae, Hoplichthyi- (Copepoda: Lernaeopodidae), parasitic on Sciaena genus (Teleostei: Sciaenidae) in the South Pacific. Estudios Oceanológicos 6, 1–24. dae, Lampridae, Lethrinidae, Lutjanidae, Malacanthidae, Merluccii- Froese, R., Pauly, D. (Eds.), 2009. FishBase. World Wide Web electronic publication. dae, Mugilidae, Oplegnathidae, Paralichthyidae, Paraulopidae, www.fishbase.org, version (03/2009). Pinguipedidae, Pleuronectidae, Psychrolutidae, Scorpaenidae, and Ho, J.-S., 1975. Copepod parasites of deep-sea fish off the Galápagos Islands. Parasitology 70, 359–375. Trichiuridae) have been associated with a single Parabrachiella spe- Ho, J.-S., Cheng, Y.R., Lin, C.L., 2007. The development of Parabrachiella lata (Song & cies. Parabrachiella seem to be parasites of exclusively teleost Chen, 1976), a lernaeopodid copepod parasitic on the black porgy, fishes, and the finding of ‘‘Brachiella chavesii”byvan Beneden Acanthopagrus schlegelii (Bleeker, 1854), of Taiwan. Crustaceana 80, 47–66. Humes, A.G., Gooding, R.U., 1964. A method for studying the external anatomy of (1891) on a ‘‘Ceratopterus sp.” = Manta birostris (Walbaum) copepods. Crustaceana 6, 238–240. (Elasmobranchii: Rajiformes: Myliobatidae) seems to be an error. Kabata, Z., 1966. Brachiella chevreuxii van Beneden, 1891 (Copepoda, Similarly, P. chevreuxii (van Beneden, 1891) was allegedly found Lernaeopodidae); a taxonomic problem. Crustaceana 10, 98–108. Kabata, Z., 1979. Parasitic Copepoda of British Fishes. Ray Society, London. on a ‘‘Squalus sp.”, which is also doubtful. Kabata, Z., 1986. Redescriptions of and comments on four little-known The narrow host specificity of Parabrachiella species seems to be Lernaeopodidae (Crustacea: Copepoda). Cananadian Journal of Zoology 64, their important characteristic feature. Therefore, cases of finding 1852–1859. (allegedly) the same species of copepod from fishes representing Kabata, Z., Gusev, A.V., 1966. Parasitic Copepoda of fishes from the collection of the Zoological Institute in Leningrad. Journal of the Linnean Society, Zoology 46, different families must be treated with caution (Kempter et al., 155–207. 2006). For example: Markewitsch (1940) described P. annulata Kabata, Z., Tareen, I.U., 1981. A new species of Thysanote Krøyer, 1863 (Copepoda, from the skin of a fish representing family Ereunidae, while Kabata Lernaeopodidae) from the Persian Gulf, with comments on the genus. Systematic Parasitology 3, 97–103. and Gusev (1966), Noble (1973), and Ho (1975) recorded it from Kempter, J., Piasecki, W., Wie˛ski, K., Krawczyk, B., 2006. Systematic position of fishes representing family Macrouridae. Also P. exilis (Shiino, copepods of the genus Achtheres (Crustacea: Copepoda: Siphonostomatoida) 1956) was originally described from Kyphosus vaigiensis (Kyphosi- parasitizing perch, Perca fluviatilis L., and zander, Sander lucioperca (L.). Journal of Fish Diseases 29, 103–113. dae) but Castro Romero and Baeza Kuroki (1986) re-described it Kurtz, W., 1877. Studien über die Familie der Lernaeopodiden. Zeitschrift für from Mugil cephalus (Mugilidae). wissenschaftliche Zoologie 29, 380–423. The majority of Parabrachiella species were found in the Pacific Lonc, E., 2004. Professor Zbigniew J. Jara—a renaissance man of the third millennium. Acta Ichthyologica et Piscatoria 34, 109–113. Ocean (37 species: 22 in North Pacific and 15 in South Pacific). Markewitsch, A.P., [Markevich or Markevicˇ] 1940. Novi vidi paraziticˇnih Copepoda. Some 23 species come from the Atlantic (18 form the North and Neue Arten parasitischer Copepoden. Dopovidi Akademii Nauk Ukrainskoj RSR, 5 from the South), while the Indian Ocean is the type locality for Kiev 11, 11–21. [In Ukrainian and German.]. Noble, E.R., 1973. Parasites and fishes in a deep-sea environment. Advances in only 7 species. Marine Biology 11, 121–195. Olech, W., Piasecki, W., 2009. In memory of Professor Zbigniew J. Jara (1918–2008). Acknowledgments Acta Ichthyologica et Piscatoria 39, 75–77. Piasecki, W., 1993. Description of Neobrachiella sp. (Copepoda, Siphonostomatoida, Lernaeopodidae) parasitic in the buccal cavity of California halibut (Paralichthys This material was collected as part of PhD studies by CJH. We californicus). Wiadomosći Parazytologiczne 39, 149–153. are grateful to Geoff Boxshall for providing some literature that Piasecki, W., Ohtsuka, S., Yoshizaki, R., 2008. A new species of Thysanote Krøyer, was difficult to access. 1863 (Copepoda: Siphonostomatoida: Lernaeopodidae), a fish parasite from Thailand. Acta Ichthyologica et Piscatoria 38, 29–35. Rubec, L.A., 1988. Neobrachiella rostrata (Copepoda, Lernaeopodidae) on the gills of References the Greenland halibut, Reinhardtius hippoglossoides from the Gulf of St. Lawrence. Canadian Journal of Zoology 66, 504–507. Boxshall, G.A., Halsey, S.H., 2004. An Introduction to Copepod Diversity. Ray Society, Roubal, F.R., 1981. The taxonomy and site specificity of the metazoan ectoparasites London. on the black bream, Acanthopagrus australis (Günther), in northern New South Brian, A., 1906. Copepodi parassiti dei Pesci d’Italia. Stab. Tipo-Litografico R. Istituto Wales. Australian Journal of Zoology Supplementary Series 84, 1–100. Sordomuti, Genova. Song, D.X., Chen, G.X., 1976. Some parasitic copepods from marine fishes of China. Castro Romero, R., Baeza Kuroki, H., 1986. Some species of Neobrachiella Kabata, Acta Zoologica Sinica 22, 406–424 [In Chinese with English Summary]. 1979 (Copepoda, Lernaeopodidae), parasitic on Chilean fishes, with description Van Beneden, P.J., 1891. Deux Lernaeopodiens nouveaux recueillis l’un aux Açores, of Neobrachiella paralichthyos sp. nov. from Paralichthys adspersus l’autre sur les côtes du Sénégal. Bulletin de l’Académie Royale de Belgique 22 (Steindachner). Crustaceana 51, 245–253. (3), 23–34. 本文献由“学霸图书馆-文献云下载”收集自网络，仅供学习交流使用。

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