J. Parasitol., 92(1), 2006, pp. 126–129 q American Society of Parasitologists 2006
AUSTRALICOLA PECTINATUS N. GEN. AND N. SP. (CESTODA: PSEUDOPHYLLIDEA) FROM THE DEEP-SEA FISH BERYX SPLENDENS FROM TASMANIA Roman Kuchta and Toma´sˇ Scholz* Faculty of Biological Sciences, University of South Bohemia and Institute of Parasitology, Academy of Sciences of the Czech Republic, ˇ eske´ Budeˇjovice, Czech Republic. e-mail:
[email protected] Branisˇovska´ 31, 370 05 C ABSTRACT: Australicola pectinatus n. gen., n. sp. (Pseudophyllidea: Triaenophoridae) is proposed to accommodate a new cestode from a deep-sea fish, the splendid alfonsino, Beryx splendens Lowe, 1834 (Beryciformes: Berycidae), from the Pacific coast of Tasmania. The new genus is placed in the Triaenophoridae, because it possesses a ventral uterine pore, marginal genital pore, and follicular vitellarium. Australicola is characterized by possessing a massive strobila with very short and wide, markedly craspedote proglottids; vitelline follicles forming a transverse equatorial band; a very deep and narrow genital atrium; a wide, convoluted vaginal canal; and unoperculate eggs. Australicola most closely resembles Eubothrium Nybelin, 1922 and Probothriocephalus Campbell, 1979 in having an unarmed scolex, an unarmed cirrus, the vagina anterior to the cirrus-sac, and cortical vitellaria. It differs from these 2 genera, in addition to the characteristics listed above, in possessing a dendritic rather than an entire ovary. Australicola pectinatus n. sp. is the third cestode described from B. splendens.
tylus Cuvier, 1829 found by L. W. Reimer in Mozambique (258239S, 358119E) in 1982 (deposited in L. W. Reimer’s collection).
Deep-sea fish have been reported as definitive hosts of endoparasitic helminths, including tapeworms (Cestoda), with about 90 cestode taxa described so far (Klimpel et al., 2001). Most of these parasites, however, have been described from fishes living in shallow coastal and shelf regions, whereas the fauna of bathypelagic fishes is very poorly known (Klimpel et al., 2001). Two pseudophyllidean cestodes, Tetrapapillocephalus magnus Protasova and Mordvinova, 1986 and Probothriocephalus berycis (Protasova and Parukhin, 1986) Bray, Jones & Andersen, 1994 (syn. Partitiotestis berycis Protasova and Parukhin, 1986), have been described from the splendid alfonsino, Beryx splendens Lowe, 1834 (Beryciformes: Berycidae). Parasitological examination of this fish from the Pacific coast of Tasmania revealed the presence of a previously undescribed pseudophyllidean cestode of the Triaenophoridae Lo¨nnberg, 1889. Because it cannot be assigned to any of the triaenophorid genera recognized as valid by Bray et al. (1994) and Kuchta and Scholz (2004), a new genus is proposed to accommodate this species, which is described in the present article.
DESCRIPTION Australicola n. gen. Diagnosis: Pseudophyllidea, Triaenophoridae. Strobila large, massive, consisting of very short and wide, markedly craspedote proglottids. Longitudinal musculature very well developed. Scolex unarmed, massive, tapered anteriorly, 4-sided in profile, with prominent bothrial edges. Apical disc small, but distinct; bothria very shallow, posteriorly sessile. Neck present, long. Single set of male and female reproductive organs per proglottid. Testes medullary; cirrus-sac elongate; cirrus unarmed. Genital atrium marginal, narrow and deep, irregularly alternating, pre-equatorial. Ovary dendritic, entirely in poral half of proglottid. Vaginal canal convoluted, anterior to cirrus-sac. Vitelline follicles largely cortical, with some follicles penetrating among bundles of muscle fibers of extensively developed longitudinal musculature; follicles forming transverse band along equatorial line, not confluent between proglottids. Uterine sac median, transversely oval, filling anteromedian 2 thirds of proglottids; uterine pore oval, thick-walled. Eggs unoperculate, unembryonated. Parasites of deep-sea teleosts. Taxonomic summary
MATERIALS AND METHODS Six cestodes were found in the intestine of 2 B. splendens, caught off the Pacific coast of Tasmania by Dr. Iva Dykova´ in November 2003. The cestodes were fixed with 4% formaldehyde solution, stained, and mounted in Canada balsam. Cross sections were prepared using standard procedures (staining with Heidenhain’s hematoxylin-eosin; thickness of sections, 12 mm). Illustrations were prepared using a drawing attachment of a Leitz Aristoplan microscope with Nomarski interference contrast. Measurements in the description are given in micrometers unless otherwise stated. For comparison, material of several triaenophorid genera from the helminthological collection of the Institute of Parasitology, Academy of ˇ eske´ Budeˇjovice (IPCAS), were studSciences of the Czech Republic, C ied, including the types of Probothriocephalus alaini Scholz and Bray, 2001 and Bathycestus brayi Kuchta and Scholz, 2004 (IPCAS C-303 and BMNH 1998.3.31.25, respectively). In addition, the type specimens of T. magnus and P. berycis from the helminthological collection of the Parasitological Institute, Russian Academy of Sciences, Moscow (GELAN 669 and 696, respectively) were studied as well as an incomplete specimen of an unidentified triaenophorid cestode from Beryx decadac-
Type and only species: Australicola pectinatus n. sp. Etymology: The generic name is composed from ‘‘Australi-’’, to refer to the continent where the tapeworms were found, i.e., Australia, and the Latin suffix ‘‘-cola’’, inhabitant. The gender of the genus is masculine. Remarks The new genus is placed in Triaenophoridae Lo¨nnberg, 1889 because it possesses a marginal genital pore, follicular vitellarium, and ventral uterine pore. This family currently includes 18 genera (Kuchta and Scholz, 2004). Australicola is characterized by possessing a massive strobila with very short and wide, markedly craspedote proglottids; vitelline follicles forming a transverse equatorial band; a very deep and narrow genital atrium; a wide, convoluted vaginal canal; and unoperculate eggs. Australicola most closely resembles Eubothrium Nybelin, 1922 and Probothriocephalus Campbell, 1979 in having an unarmed scolex, an unarmed cirrus, the vagina anterior to the cirrus-sac, and cortical vitellaria. It differs from these 2 genera, in addition to the characteristics listed above, in possessing a dendritic rather than an entire ovary (Kuchta and Scholz, 2004).
Australicola pectinatus n. gen. and n. sp. (Figs. 1–9)
Received 16 February 2005; revised 9 June 2005; accepted 9 June 2005. * Institute of Parasitology, Academy of Sciences of the Czech Republic, ˇ eske´ Budeˇjovice, Czech Republic. Branisˇovska´ 31, 370 05 C
(see photos at www.paru.cas.cz/structure/lpf/images/australicola/ pagep01.htm) Description (based on holotype—complete worm on 4 whole mounts, 126
KUCHTA AND SCHOLZ—AUSTRALICOLA PECTINATUS
127
FIGURES 1–9. Australicola pectinatus n. gen., n. sp. 1. Total view of the anterior part of the strobila (apical part of scolex missing). Paratype (AHC 28812-15). 2. Anterior part of the holotype (USNPC 96496). 3. Schematic drawing of the scolex shape from the apical view. 4. Scolex of the holotype; dorsoventral view. 5. Gravid proglottids, holotype. 6. Eggs. 7. Terminal genitalia, holotype; note the anterior position of the vagina. 8. Gravid proglottids, holotype. 9. Slightly oblique section showing the poral parts of 2 adjacent proglottids at the level of the ovary (anterior proglottid—on the right) and cirrus-sac (posterior, adjacent proglottid—on the left). Abbreviations: cs, cirrus-sac; ga, genital atrium; lm, longitudinal muscle bundles; oc, osmoregulatory canals; ov, ovary; t, testis; ut, uterus; va, vagina; vf, vitelline follicles.
128
THE JOURNAL OF PARASITOLOGY, VOL. 92, NO. 1, FEBRUARY 2006
1 paratype—incomplete worm [without terminal part of scolex] on 4 whole mounts, and 4 vouchers—incomplete worms on 11 whole mounts and 16 slides of cross sections of strobila): Strobila massive, up to 300 mm long and 9 mm wide, consisting of short and wide (length : width ratio 1:4–1:30), markedly craspedote proglottids. Internal segmentation distinct; pseudosegmentation absent. Longitudinal excretory canals numerous, connected by transverse anastomoses, difficult to observe (Fig. 7). Longitudinal musculature well developed, formed by numerous bundles of muscle fibers; circular muscle layer absent (Fig. 9). Scolex (1 complete, 3 incomplete) massive, lanceolate in dorsoventral view, 4-sided in apical (en face) view, with prominent lateral bothrial edges, unarmed (Figs. 1–4), 3,720 long by 1,240–1,360 wide. Two bothria very shallow, without free posterior margins (posteriorly sessile), 2,990–3,100 long by 956–1,360 wide. Apical disc small but distinct, 183 long by 453 wide. Neck present, finely wrinkled, 1,510–2,500 long by 927–1,570 (n 5 4); first proglottids starting after neck region with prominent proglottization (Figs. 1, 2). Immature proglottids 52–380 long by 1,070–5,240 wide (n 5 22) (Fig. 1). Mature proglottids, i.e., with spermatozoa in vas deferens, 271– 340 long by 5,370–5,480 wide (n 5 6), often arched (Fig. 1). Gravid proglottids, 335–1,057 long by 4,890–8,960 wide (n 5 15), arched, slightly deformed posteriorly by growing uterine sac (Figs. 5, 8). Testes medullary, round, 90–112 in number per proglottid (n 5 6), 58–97 in diameter (n 5 31), distributed in 1 wide band with fewer testes medially, confluent between proglottids, absent near lateral margins of proglottids (Figs. 5, 8). Cirrus-sac elongate, relatively short, representing 8–11% of width of mature proglottid (n 5 10) (Fig. 7), 312–451 long by 77–88 wide (n 5 10) (length : width ratio 3.7–5.4: 1), containing coiled, unarmed cirrus (Fig. 7). Vas deferens difficult to observe, forming numerous loops between cirrus-sac and ovary. Genital atrium long and narrow (Fig. 7), lateral, alternating irregularly (Fig. 1), pre-equatorial (at 34–44% of proglottid length). Ovary dendritic (Figs. 5, 8), also in cross section, in poral half of proglottid, near anterior margin of proglottid, 191–277 long by 656–879 wide (n 5 10). Vagina tubular, crossing ovary dorsally, then bent laterally, relatively wide (36–56 in diameter), forming tightly coiled loops in its distal (terminal) part, opening anterior to cirrus-sac into genital atrium, without vaginal sphincter (Figs. 7, 8). Vitelline follicles mostly cortical, with some follicles penetrating among bundles of extensively developed longitudinal muscle fibers; vitellarium forming transverse band of follicles along equatorial line of proglottid; follicles not confluent between proglottids (Figs. 5, 9). Uterine duct short, connecting ovary with uterine sac by short, straight canal in immature proglottids, J-shaped, filled with eggs in gravid proglottids (Figs. 5, 8). Uterine development of ptychobothriid type (Protasova, 1977). Uterine sac median, transversely oval, occupying anterior half of proglottid (Figs. 5, 8). Uterine pore ventromedian, thickwalled, near posterior margin of uterine sac. Eggs unoperculate, unembryonated, 77–86 long by 52–61 wide (x¯ 5 82 3 56) (n 5 14) (Fig. 6). Taxonomic summary Type host: Beryx splendens. Site of infection: Intestine. Type locality: Tasmania. Deposition of specimens: U.S. National Parasite Collection, Beltsville, Maryland—holotype (USNPC 96496) and vouchers (USNPC 96497); Australian Helminthological Collection, South Australian Museum, Adelaide, Australia—paratype (AHC 28812-15); The Natural History Museum, London, U.K.—vouchers (BMNH 2005.7.13.17-25); ˇ eske´ Budeˇjovice, Czech Republic— Institute of Parasitology, AS CR, C vouchers (IPCAS C-384). Etymology: The specific name pectinatus refers to the pectinate (i.e., comblike) appearance of the strobila of this species, caused by the markedly craspedote proglottids.
DISCUSSION Australicola pectinatus is another pseudophyllidean cestode described from a bathypelagic fish (Klimpel et al., 2001). It is placed in the Triaenophoridae because it possesses a marginal genital pore, follicular vitellaria, and a ventral uterine pore
(Bray et al., 1994). Australicola pectinatus is the third tapeworm reported from B. splendens; 2 other pseudophyllideans have been described from this fish from the Indian Ocean, namely, the triaenophorid P. berycis and bothriocephalid T. magnus. Both species are markedly different from A. pectinatus (see above). In their checklist, Klimpel et al. (2001) listed the finding of Heath (1989), who had reported an unidentified pseudophyllidean cestode from B. splendens from Australian waters. However, the present authors were unable to obtain specimens or any information about the morphology of this cestode, which may well be conspecific with A. pectinatus. In B. decadactylus from Mozambique, Dr. L. W. Reimer (unpubl. obs.) found triaenophorid cestodes that also may belong to Australicola. However, material kindly provided to the present authors by Dr. Reimer was not sufficient to confirm this preliminary identification. In the same fish species, B. decadactylus, another pseudophyllidean cestode, Bothriocephalus platycephalus Monticelli, 1889, was found, but Protasova (1977) considered this taxon to be a species inquirenda. The original description of B. platycephalus was not available to the present authors, but Ariola (1900) described this taxon based on Monticelli’s (1889) material and illustrated its scolex. Its shape and the presence of wide, shallow bothria indicate that B. platycephalus might be conspecific with A. pectinatus. This assumption also is supported by the large size of the strobila of B. platycephalus and the shape of its proglottids, as can be assessed from a very brief description of Ariola (1900). However, B. platycephalus was reported to have a median genital pore (‘‘Apparecchio riproductore con aperture genitali dorsoventrali’’—Ariola, 1900, p. 411), which is a typical characteristic of the Bothriocephalidae (triaenophorids always have a lateral genital pore [Bray et al., 1994]). Three species of Beryx are considered to be valid (Froese and Pauly, 2005). They have a cosmopolitan distribution and 2 of them, B. splendens and B. decadactylus, are of economic importance, being caught mainly in the Canary Islands, Hawaii, and Japan (Du¨rr and Gonza´lez, 2002). Beryx splendens is a bathypelagic fish occurring worldwide in tropical and temperate waters. It inhabits the outer continental shelf (depth of about 180 m) and the slope up to the depth of 1,300 m. Its food is composed mainly of small fish; crustaceans, including copepods; and cephalopods (Lehody et al., 1997; Du¨rr and Gonza´lez, 2002). The life cycle of A. pectinatus is unknown, like almost all other pseudophyllideans from marine teleosts (Protasova, 1977). Based on an analogy with species from freshwater fish (Williams and Jones, 1994; Marcogliese, 1995; Chervy, 2002), it can be speculated that planktonic crustaceans such as copepods may serve as intermediate hosts of A. pectinatus. These crustaceans form an important food item of juvenile alfonsino (Du¨rr and Gonza´lez, 2002). Larger fish that do not eat copepods might acquire infection by consuming small fish, such as myctophids, which may serve as paratenic or second intermediate hosts, but no data on the transmission patterns of A. pectinatus and other deep-sea fish pseudophyllideans are available. ACKNOWLEDGMENTS We are indebted to Iva Dykova´ for providing specimens of A. pectinatus collected in Tasmania and to Martina Borovkova´, both from the
KUCHTA AND SCHOLZ—AUSTRALICOLA PECTINATUS
Institute of Parasitology, Academy of Sciences of the Czech Republic, ˇ eske´ Budeˇjovice, for technical assistance and to Ekaterina N. ProtaC sova and Larisa V. Filimonova, Parasitological Institute, Russian Academy of Sciences, Moscow, for lending type specimens of T. magnus and P. berycis. We also thank L. W. Reimer for lending a cestode from B. decadactylus. The present study was supported by the Grant Agency of the Czech Republic (projects 524/04/0342 and 524/03/H133), the research project of the Institute of Parasitology, Academy of Sciences of the Czech Republic (Z60220518), Research Centre ‘‘Ichthyoparasitology’’ (LC 522), and the research project of the Faculty of Biological Sciences, University of South Bohemia (MSM 6007665801).
LITERATURE CITED ARIOLA, V. 1900. Revisione della famiglia Bothriocephalidae s. str. Archives de Parasitologie 3: 369–484. BRAY, R. A., A. JONES, AND K. I. ANDERSEN. 1994. Order Pseudophyllidea Carus, 1863. In Keys to the cestode parasites of vertebrates, L. F. Khalil, A. Jones, and R. A. Bray (eds.). CAB International, Wallingford, U.K., p. 205–247. CHERVY, L. 2002. The terminology of larval cestodes or metacestodes. Systematic Parasitology 52: 1–33. DU¨RR, J., AND J. A. GONZA´LEZ 2002. Feeding habits of Beryx splendens and Beryx decadactylus (Berycidae) off the Canary Islands. Fisheries Research 54: 363–374. FROESE, R., AND D. PAULY (EDS.). 2005. FishBase. World Wide Web electronic publication, accessed December 2005. http:// www.fishbase.org HEATH, B. M. 1989. A study of the endoparasitic helminths of deepsea fishes from southeastern Australia: Taxonomy, zoogeography
129
and host-patasite ecology. Ph.D. Dissertation. University of New England, Armidale, Australia, 360 p. KLIMPEL, S., A. SEEHAGEN, H.-W. PALM, AND H. ROSENTHAL. 2001. Deep-water metazoan fish parasites of the world. Logos Verlag, Berlin, Germany, 316 p. KUCHTA, R., AND T. SCHOLZ. 2004. Bathycestus brayi n. gen and n. sp. (Cestoda: Pseudophyllidea) from the deep-sea fish Notacanthus bonaparte in the Northeastern Atlantic. Journal of Parasitology 90: 316–321. LEHODEY, P., R. GRANDPERRIN, AND P. MARCHAL. 1997. Reproductive biology and ecology of a deep-demersal fish, alfonsino Beryx splendens, over the seamounts off New Caledonia. Marine Biology 128: 17–27. MARCOGLIESE, D. J. 1995. The role of zooplankton in the transmission of helminth parasites to fish. Reviews in Fish Biology and Fisheries 5: 336–371. MONTICELLI, F. S. 1889. Notes on some Entozoa in the collection of the British Museum. Proceedings of the Zoological Society of London, 321–325. PROTASOVA, E. N. 1977. Cestodes of fish—Bothriocephalata. In Principles of cestodology, K. M. Ryzhikov (ed.). Volume VIII. Nauka, Moscow, Russia, 298 p. [In Russian.] ———, AND T. N. MORDVINOVA. 1986. A ptychobothriid cestode, Tetrapapillocephalus magnus n. gen., n. sp. (Pseudophyllidea: Ptychobothriidae) from marine fish. Parazitologiya 20: 313–316. [In Russian.] ———, AND A. M. PARUKHIN 1986. New genera and species of cestodes (Pseudophyllidea: Amphicotylidae) from marine fishes. Parazitologiya 20: 278–287. [In Russian.] WILLIAMS, H., AND A. JONES. 1994. Parasitic worms of fish. Taylor & Francis, London, U.K., 593 p.
