A Checklist of the Protozoan and Metazoan Parasites Reported from the Atlantic Horse Mackerel, Trachurus Trachurus (L.)

Bull. Eur. Ass. Fish Pathol., 24(4) 2004, 180 A checklist of the protozoan and metazoan parasites reported from the Atlantic horse mackerel, Trachurus trachurus (L.)

K. MacKenzie1, N. Campbell1, S. Mattiucci2, P. Ramos3, A. Pereira3 and P. Abaunza4

1School of Biological Sciences (Zoology), University of Aberdeen, Aberdeen AB24 2TZ, Scotland; 2Institute of Parasitology, University of Rome “La Sapienza”, Pl. Aldo Moro 5, 00185 Rome, Italy; 3IPIMAR, Avenida Brasilia, 1400 Lisbon, Portugal; 4Instituto Español de Oceanografia, Centro Oceanografico de Santander, 39080 Santander, Spain.

Abstract The checklist was compiled from a literature search and from the results of the EC-funded HOMSIR project on stock structure of Trachurus trachurus. It consists of 68 different parasite taxa, 58 of which have been identified to species level, and includes 11 new host records and two possibly new species of myxosporean. The composition of the parasite fauna illustrates the im- portance of T. trachurus as an intermediate host for helminth parasites maturing in piscivorous fish and mammals.

Introduction structure analysis” (QLK5-Ct1999-01438), The Atlantic horse mackerel, Trachurus funded by the EU Commission within its 5th trachurus (L.), is a member of the family Framework Programme. An integral part of Carangidae, which includes many important this project is the use of parasites as biologi- commercial species worldwide. It is the most cal tags to help identify stocks of T. trachurus northerly representative of the genus in European waters. Trachurus and is distributed from West Africa/ Cape Verde Islands to the Norwegian Sea, Materials and Methods including Iceland, and throughout the Medi- In the HOMSIR project, a total of 1919 horse terranean and Black Seas (Smith-Vaniz, 1986). mackerel from 38 samples were examined for The diet of the Atlantic horse mackerel shows parasites. Most samples consisted of 50 fish, great diversity and is essentially composed with a range from 21 to 100. The fish ranged of plankton with crustaceans as the more char- in length from 11.3 to 43.1 cm and in age from acteristic prey organisms (Ben Salem, 1988). one to 29 years. The stations at which the fish The present checklist was compiled as part of were caught ranged from off the coast of the multidisciplinary international project Morocco to off southwest Norway, with three “HOMSIR: a multidisciplinary approach us- stations off the coast of Portugal, two off the ing genetic markers and biological tags in north coast of Spain, one in the North Sea, and horse mackerel (Trachurus trachurus) stock three to the west and southwest of the British Bull. Eur. Ass. Fish Pathol., 24(4) 2004, 181

Parasite Site of infection Apicomplexa Goussia cruciata (rThélohan, 1892) Live Myxosporea Alataspora serenum (rGaevskaya & Kovaleva, 1979) Gall bladde Alataspora solomoni (rYurakhno, 1988) Gall bladde Kudoa nova (Naidenova, 1975) Musculature Kudoa quadratum (Thélohan, 1895) Musculature *Kudoa sp. Gall bladder *Myxobolus srp. Live Monogenea Cemocotyle trachuri (sDillon & Hargis, 1965) Gill Gastrocotyle trachuri (svan Beneden & Hesse, 1863) Gill Heteraxinoides atlanticus (sGaevskaya & Kovaleva, 1979) Gill Pseudaxine trachuri (sParona & Perugia, 1889) Gill *Unidentified polyopisthocotylean monogenean Gills Paradiplectanotrema trachuri (sKovaleva, 1970) Stomach, oesophagu Digenea Lasiotocus typicum (eNicoll, 1912) Intestin Aphanurus stossichi (hMonticelli, 1891) Stomac *Bathycreadium elongatum (eMaillard, 1970) Intestin Lasiotocus tropicus (eManter, 1940) Intestin Derogenes varicus (hMüller, 1784) Stomac Ectenurus lepidus (hLooss, 1907) Stomac Ectenurus virgulus (hLooss, 1910) Stomac Helicometra pulchella (eRudolphi, 1819) Intestin Hemiurus communis (hOdhner, 1905) Stomac Hemiurus luehei (hOdhner, 1905) Stomac Lecithaster confusus (eOdhner, 1905) Intestin Lecithaster gibbosus (eRudolphi, 1802) Intestin Lecithocladium excisum (aRudolphi, 1819) Pyloric caec Monascus filiformis (Rudolphi, 1819) Pyloric caeca, intestine Opechona pyriforme (eLinton, 1900) Intestin Opechona bacillaris (eMolin, 1859) Intestin Pseudopecoeloides chloroscombri (eFischal & Thomas, 1970) Intestin Prodistomum polonii (eMolin, 1859) Intestin Prodistomum orientalis (eLayman, 1930) Intestin Pseudopecoeloides carangis (eYamaguti, 1938) Intestin Stephanostomum sep. (Gritli et al. ,1989) Intestin Lecithochirium musculus (hLooss, 1907) Stomac Tergestia laticollis (eRudolphi, 1819) Intestin Zoogonus rubellus (eOlsson, 1868) Intestin *Denotes new host records from the HOMSIR study. Table 1. Parasite species recorded from the Atlantic horse mackerel, Trachurus trachurus. Bull. Eur. Ass. Fish Pathol., 24(4) 2004, 182

Parasite Site of infection Cestoda (all postlarvae) Anthobothrium cornucopia (evan Beneden, 1850) Intestin Callitetrarhynchus gracilis (yRudolphi, 1819) Visceral cavit Christianella minuta (yvan Beneden, 1849) Visceral cavit Grillotia bothridiopunctata (yDollfus, 1969) Visceral cavit Grillotia erinaceus (van Beneden, 1858) Visceral cavity Lacistorhynchus tenuis (yvan Beneden, 1858) Visceral cavit Nybelinia sp. (Kovaleva (1970) Visceral cavity Nybelinia lingualis (Cyuvier, 1817) Visceral cavit Scolex pleuronectis (eMüller, 1788) Intestin *Pseudophyllidean plerocercoids Visceral cavity Acanthocephala *Corynosoma strumosum (yRudolphi, 1802) juveniles Visceral cavit *Corynosoma wegeneri (yHeinze, 1934) juveniles Visceral cavit Rhadinorhynchus cadenati (eGolvan & Houin, 1964) Intestin Nematoda Anisakis simplex (Rudolphi, 1809) larvae Visceral cavity Anisakis pegreffii (Campana-Rouget & Biocca, 1955) larvae Visceral cavity Anisakis physeteris (Baylis, 1923) larvae Visceral cavity Contracaecum sp. larvae (Rego (1987) Intestine, visceral cavity Cosmocephalus obvelatus (yCreplin, 1825) larvae Visceral cavit Hysterothylacium aduncum (eRudolphi, 1802) adults Stomach, intestin Hysterothylacium aduncum (yRudolphi, 1802) larvae Visceral cavit Paracuaria tridentata (yLinstow, 1877) larvae Visceral cavit *Pseudanisakis sp. larvae Visceral cavity *Pseudoterranova decipiens (eKrabbe, 1878) larvae Musculatur Raphidascaris sp. larvae (Rego (1987) Intestine, visceral cavity Crustacea Caligus diaphanus (nNordmann, 1832) Ski Caligus elongatus (nNordmann, 1832) Ski Caligus pelamydis (Khrøyer, 1863) Mout Peniculus fistula (sNordmann, 1832) Fin Lernanthropus trachuri (Bsrian, 1903) Gill Ceratothoa oestroides (hRisso, 1826) Mout *Praniza gnathiid isopod lnarva Ski * Argulus purpureus (Rnisso, 1826) Ski

Table 1. Continued. Bull. Eur. Ass. Fish Pathol., 24(4) 2004, 183

Isles. A further nine stations were distributed cations of Hysterothylacium aduncum and throughout the Mediterranean from inside the Anisakis sp. respectively. The Kudoa sp. and Straits of Gibraltar to the Aegean Sea. The Myxobolus sp. are possibly new species, as the parasites we recorded from our samples are spore forms and measurements are different listed in Table 1, together with earlier records from any of the published descriptions of from various literature sources, most notably members of these genera. a series of Russian papers by Kovaleva (1970) and Gaevskaya and Kovaleva (1979, 1980abc, Acknowledgments 1982 We are grateful to Drs D.I. Gibson, R.A. Bray and G.A. Boxshall of The Natural History Results Museum in London for providing relevant A total of 68 different parasite taxa have been excerpts from the museum’s host/parasite reported from T. trachurus, 58 of which have database, and for assistance with literature been identified to species level. In the and parasite taxonomy. We also thank all our HOMSIR project we recorded a total of 45 partners in the HOMSIR project for their help. taxa, 37 of which we identified to species level, and 11 of which appear to be new host records References for T. trachurus. These new host records are Ben Salem M (1988). Régime alimentaire de indicated in Table 1. Trachurus trachurus (Linnaeus, 1758) et de T. mediterraneus (Steindachner, 1868), (Poissons, Téléostéens, carangidae) de la province Discussion Atlantico-Mediterranéenne. Cybium 12: 247- Table 1 shows that T. trachurus has a wide and 253. varied parasite fauna, which includes an unu- Gaevskaya AV and Kovaleva AA (1979). sually large number of species that are spe- Monogeneans from the Atlantic horse mack- cific to the genus Trachurus. The Digenea is erels of the genus Trachurus. [In Russian]. Zool. the most abundant group in terms of num- Zh. 58: 1110-1116. bers of species, but we found that larval nema- Gaevskaya AV and Kovaleva AA (1980a). The todes were the most abundant metazoan para- reasons for the similarities and differences sites in terms of numbers of individuals. A between the parasite faunas of two subspe- cies of horse mackerel of the Atlantic Ocean notable feature is the large number of larval [In Russian]. Biol. Nauk. No. 6, Zoology: 52- and postlarval helminth species represented, 56. particularly cestodes and nematodes, under- Gaevskaya AV and Kovaleva AA (1980b). Eco- lining the importance of T. trachurus as an in- geographical characteristics of the parasite termediate and paratenic host for species fauna of Atlantic Ocean scad [In Russian]. In: maturing in piscivorous fish and mammals. Investigations on the Biological Resources of Based on our experience of the HOMSIR the Atlantic Ocean pp.18-24. Knizh, izd-vo, Kaliningrad. project, we suspect that the records of Contracaecum sp. and Raphidascaris sp. larvae by Rego (1987) were probably misidentifi- Bull. Eur. Ass. Fish Pathol., 24(4) 2004, 184

Gaevskaya AV and Kovaleva AV (1980c.) The Kovaleva AA (1970). Helminth fauna of mack- use of parasitological data in population stud- erel of the genus Trachurus (Carangidae, ies of Atlantic mackerel from the genus Perciformes) in the Atlantic basin. [In Rus- Trachurus. [Abstract in Russian]. In: IX Konf. sian]. Biol. Morya, Kiev, No. 20: 37-66. Ukrainskogo Parazitol. Obshch. Tezisy Dokladov. Chast’ 1. Kiev, Naukova Dumka: Rego AA (1987). Identificacao de helmintes de 132-133. peixes da costa continental portuguesa. Garcia de Orta. Serie de Zoologia, Lisboa 12: 113-116. Gaevskaya AV and Kovaleva AA (1982). The trematode fauna of Atlantic horse mackerels Smith-Vaniz WF (1986). The Carangidae. In of the genus Trachurus and its characteristics. “Fishes of the North-Eastern Atlantic and the Hydrobiol. J. 18: 50-55. Mediterranean, vol. II” (Whitehead, P.J.P., Bauchot, M. -L., Hureau, J.-C., Nielsen, J. and Gritli R, Zarrouk K and Kechrid F (1989). A Tortonese, E., Eds) pp.815-844. Unesco, Paris. propos d’une trematodose rare chez le poisson rouget. Maghreb Vet. 4: 18-21.