Skip to main content
SpringerLink
Log in

A revision of the Haploporinae Nicoll, 1914 (Digenea: Haploporidae) from mullets (Mugilidae): Haploporus Looss, 1902 and Lecithobotrys Looss, 1902

  • Published:
Systematic Parasitology Aims and scope Submit manuscript

Abstract

The status of the nominal species of Haploporus Looss, 1902 and Lecithobotrys Looss, 1902 is re-assessed by means of a comparative morphological study based on newly collected specimens from the western Mediterranean, the re-examination of museum material and a critical evaluation of published data. H. benedeni (Stossich, 1887) (type-species) is described and H. lateralis Looss, 1902 is considered to be its junior synonym. Additional data are given for H. pseudoindicus Rekharani & Madhavi, 1985, H. spinosus Machida, 1996 and H. magnisaccus Machida, 1996. Species parasitising Valamugil spp. from the Indo-West Pacific region, H. indicus Rekharani & Madhavi, 1985, H. spinosus, H. magnisaccus, H. mugilis Liu & Yang, 2002 and H. muscolosaccus Machida, 2003, are considered incertae sedis with respect to their generic affiliation. H. pacificus (Manter, 1963) (syn. Neohaploporus pacificus Manter, 1963), H. pseudoindicus and H. musculosaccus are designated as species inquirendae and H. lossii Al-Bassel, 1990 is considered to be a nomen nudum. Lecithobotrys putrescens Looss, 1902 is described based on newly collected material from Liza spp. Pseudolecithobotrys n. g. is erected to accommodate Lecithobotrys stomachicola Machida, 1996, as P. stomachicola (Machida, 1996) n. comb., from the North Pacific. L. aegyptiacus Hassan, El-Aziz, Khidr & Abu Samak, 1990 is considered to be a synonym of Saccocoelium tensum Looss, 1902, and L. brisbanensis (Martin, 1974) (syn. Paralecithobotrys brisbanensis Martin, 1974), L. vitellosus Sharma & Gupta, 1970 and L. suezcanali Nisreen Ezz El-Dien, Abdel-Rahman, El-Gawady, Imam & Fahmy, 1990 are regarded as species inquirendae. New generic diagnoses are presented for both Haploporus and Lecithobotrys.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figs. 1–2
Figs. 3–6
Figs. 7–9
Figs. 10–12
Figs. 13–14

Similar content being viewed by others

Notes

  1. A series of ultrastructure studies on a trematode identified as H. benedenii ex C. labrosus (see Sampour & Mas-Coma, 2004; Sampour, 2005, 2006) and H. lateralis ex L. aurata (see Sampour, 2008) lack locality data and supportive evidence for the identification of the parasites; these are therefore not included in the list of records.

References

  • Al-Bassel, D. A. H. M. (1990). Studies on the helminth parasites of some fishes from inland water in Egypt. PhD thesis, Cairo University, Cairo.

  • Al-Bassel, D. A. H. M. (2003). A general survey of the helminth parasites of fish from inland waters in the Fayoum Governorate, Egypt. Parasitology Research, 90, 135–139.

    Article  PubMed  Google Scholar 

  • Blasco-Costa, I., Montero, F. E., Balbuena, J. A., Raga, J. A., & Kostadinova, A. (2009a). A revision of the Haploporinae Nicoll, 1914 (Digenea: Haploporidae) from mullets (Mugilidae): Dicrogaster Looss, 1902 and Forticulcita Overstreet, 1982. Systematic Parasitology (in press).

  • Blasco-Costa, I., Montero, F. E., Gibson, D. I., Balbuena, J. A., & Kostadinova, A. (2009b). A revision of the Haploporinae Nicoll, 1914 (Digenea: Haploporidae) from mullets (Mugilidae): Two new haploporine genera and a key to the genera of the subfamily. Systematic Parasitology (in press).

  • Blasco-Costa, I., Montero, F. E., Gibson, D. I., Balbuena, J. A., Raga, J. A., & Kostadinova, A. (2009c). A revision of the Haploporinae Nicoll, 1914 (Digenea: Haploporidae) from mullets (Mugilidae): Saccocoelium Looss, 1902. Systematic Parasitology (in press).

  • Carvalho-Varela, M., Cunha-Ferreira, V., Cruze Silva, M. P., Monteiro, M. T., & Grazina-Freitas, M. S. (1981). Parasites and parasitosis in fish culture in Portugal. Journal of the World Mariculture Society, 12, 9–14.

    Google Scholar 

  • D’Amelio, S., Paggi, L., Berrilli, F., Di Cave, D. Orecchia, P., Gerasi, L., Markus, E. E., & Paperna, I. (1995). Divergence of the parasite communities of Liza ramada from coastal habitats of Israel and Italy. In R. W. Hoffmann (Ed.), Program and Abstracts of the Fourth International Symposium of Fish Parasitology, Munich, October 3–7, 1995, p. 58.

  • Dawes, B. (1947). The Trematoda of British fishes. London: Ray Society, 364 pp.

  • Di Cave, D., Kennedy, C. R., D’Amelio, S., Berrilli, F., & Orecchia, P. (1997). Struttura della comunità del metazoi parassiti di Liza ramada (Risso, 1826) nel lago di Burano. Biologia Marina Mediterranea, 4, 321–323.

    Google Scholar 

  • Dmitrieva, E. V., & Gaevskaya, A. V. (2001). Parasitological aspects of mugilids mariculture and of their introduction into the Sea of Azov and the Black Sea. Ekologiya Morya, Kiev, 55, 73–78 (In Russian).

    Google Scholar 

  • Domnich, I. F., & Sarabeev, V. L. (2000a). The trematodes of the Far-East-mullet-pelingas (Mugil soiuy) in the Azov Sea aquatories. Vestnik Zoologii, 34, 7–15 (In Russian).

    Google Scholar 

  • Domnich, I. F., & Sarabeev, V. L. (2000b). Contemporary fauna of fish parasites in the northern part of the Azov Sea. Visnik Zaporiz’kogo Derzhavnogo Universitetu, 1, 224–230 (In Ukrainian).

    Google Scholar 

  • Domnich, I. F., & Sarabeev, V. L. (2000c). Forming of the parasitic fauna of the pilengas in the Azov Sea. Acta Parasitologica, 45, 265–266.

    Google Scholar 

  • Dzikowski, R., Paperna, I., & Diamant, A. (2003). Use of fish parasite species richness indices in analyzing anthropogenically impacted coastal marine ecosystems. Helgoland Marine Research, 57, 220–227.

    Article  Google Scholar 

  • El-Shahawi, G. A. Z., & Al-Bassel, D. A. (1992). A general survey of the helminth parasites infecting the common fishes in some inland water in Egypt. Proceedings of the Zoological Society A.R. Egypt, 23, 227–241.

    Google Scholar 

  • Ergens, R. (1960). Helminth fauna of some fishes in Albania. Ceskoslovenská Parasitologie, 7, 49–90 (In Russian).

    Google Scholar 

  • Fares, A., & Maillard, C. (1974). Recherches sur quelques Haploporidae (Trematoda) parasites des Muges de Méditerranée Occidentale: systématique et cycles évolutifs. Zeitschrift für Parasitenkunde, 45, 11–43.

    Article  PubMed  CAS  Google Scholar 

  • Gibson, D. I., Bray, R. A., & Harris, E. A. (Compilers) (2005). Host-Parasite Database of the Natural History Museum, London. http://www.nhm.ac.uk/research-curation/projects/host-parasites/.

  • Hassan, S. H., Khidr, A. A., & Abu Samak, O. A. (1990). Four trematodes from marine fishes in Egypt. Journal of the Egyptian-German Society of Zoology, 2, 63–74.

    Google Scholar 

  • Liu, S.-f., Wang, Y.-h., Peng, W.-f., Yu, S.-z., & Yang, W.-c. (2004). Saccocoelium megasacculum n. sp., a new haploporid trematode from Liza carinatus in the Taiwan Strait. Journal of Parasitology, 90, 604–607.

    Article  PubMed  Google Scholar 

  • Liu, S.-f., & Yang, T.-b. (2002). Haploporus mugilis sp. n. (Digenea: Haploporidae) from Valamugil engeli (Pisces: Mugilidae) in the Taiwan Straits, China. Folia Parasitologia, 49, 93–95.

    Google Scholar 

  • Looss, D. A. (1902). Die Distomen-Unterfamilie der Haploporinae. Archives de Parasitologie, 6, 129–143.

    Google Scholar 

  • Lozano, C., Ubeda, J. M., De Rojas, M., Ariza, C., & Guevara, D. C. (2001). Estudio de digenidos de pèces marinos del sur de la Peninsula Iberica. Research and Reviews in Parasitology, 61, 103–116.

    Google Scholar 

  • Machida, M. (1996). Digenean trematodes from mullets in Japanese and adjacent waters. Japanese Journal of Parasitology, 45, 123–133.

    Google Scholar 

  • Machida, M. (2003). Additional two species of digenean trematodes from mullet of southern Japan. Bulletin of the National Science Museum, Tokyo, Ser. A, 29, 125–129.

    Google Scholar 

  • Madhavi, R. (2008). Family Monorchiidae. In R. A. Bray, D. I. Gibson, & A. Jones (Eds.), Keys to the Trematoda (Vol. 3, pp. 145–175). Wallingford: CAB International.

    Google Scholar 

  • Maltsev, V. N., & Zhdamirov, V. N. (2000). [Parasite infestation and ichthyopathological state of commercial fishes in Azov Sea.] In: Pontus Euxinus 2000. Young scientist’s conference, 16–18 May 2000, Sevastopol. Abstracts, pp. 41–42.

  • Manter, H. W. (1963). Studies on digenetic trematodes of fishes of Fiji, IV. Families Haploporidae, Angiodactilyidae, Monorchiidae, and Bucephalidae. Proceedings of the Helminthological Society of Washington, 30, 224–232.

  • Martin, W. E. (1973). Life history of Saccocoelioides pearsoni n. sp. and the description of Lecithobotrys sprenti n. sp. (Trematoda: Haploporidae). Transactions of the American Microscopical Society, 92, 80–95.

    Article  Google Scholar 

  • Martin, W. E. (1974). Paralecithobotrys brisbanensis sp. n. from Australian mullet (Trematoda: Haploporidae). Proceedings of the Helminthological Society of Washington, 41, 16–18.

  • Merella, P., & Garippa, G. (1998). Parasites of grey mullets from the Oristano lagoons (Sardinia). Parassitologia, 40(Supp. 1), 106.

    Google Scholar 

  • Merella, P., & Garippa, G. (2001). Metazoan parasites of grey mullets (Teleostei: Mugilidae) from the Mistras Lagoon (Sardinia, Western Mediterranean). Scientia Marina, 65, 201–206.

    Article  Google Scholar 

  • Nasir, P., & Gómez, Y. (1976). Carassotrema tilapiae n. sp. (Haploporidae Nicoll, 1914) from the freshwater fish, Tilapia mossambica (Peters), in Venezuela. Rivista di Parassitologia, 37, 207–228.

    Google Scholar 

  • Nicoll, W. (1914). Trematode parasites of fishes in the English Channel. Journal of the Marine Biological Association of the United Kingdom, 10, 466–505.

    Article  Google Scholar 

  • Nisreen Ezz El-Dien, M., Abdel-Rahman, M. S., El-Gawady, H. M. A., Imam, E. A. E., & Fahmy, M. M. (1990). Detection of two new trematode species from marine fishes in Egypt. Journal of the Egyptian Veterinary Medical Association, 50, 507–517.

    Google Scholar 

  • Nizova, G. A., Kovtun, I. F., & Syrovatka, N. I. (2001). [Peculiarities of the formation and epizootic importance of the parasite fauna of Soiuy mullet acclimated in the water bodies of the Azov basin.] Vosmoi S’ezd Gidrobiologicheskogo Obshchtestva, 2, 13–14 (In Russian).

  • Orecchia, P., & Paggi, L. (1978). Aspetti di sistematica e di ecologia degli elminti parassiti di pesci marini studiati presso l’Instituto di Parassitologia dell’Università di Roma. Parassitologia, 20, 73–89.

    PubMed  CAS  Google Scholar 

  • Orecchia, P., Paggi, L., & Radujković, B. M. (1988). Digeneans of fishes from the Adriatic Sea with a description of Lecithaster atherinae n. sp. from Atherina (Hepsetia) boyeri. Parassitologia, 30, 225–229.

    PubMed  CAS  Google Scholar 

  • Overstreet, R. M., & Curran, S. S. (2005). Family Haploporidae Nicoll, 1914. In A. Jones, R. A. Bray, & D. I. Gibson (Eds.), Keys to the Trematoda (Vol. 2, pp. 129–165). Wallingford: CAB International.

    Google Scholar 

  • Öztürk, M. O., & Aydogdu, A. (2003). Karacabey Bayramdere Dalyanı’ndaki kefal balıkları (Mugil cephalus L.)’nda belirlenen metazoon parazitler. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 50, 53–58 (In Turkish).

    Google Scholar 

  • Paggi, L., Orecchia, P., Cancrini, G., & Minervini, R. (1979). Aspetti morfologici ed ecologicidei parassiti di alcune specie ittiche di ambiente salmastro (Lago di Saubaudia – Prov. Latina – Italia). Atti della Società Italiana delle Scienze Veterinarie, 33, 272.

    Google Scholar 

  • Paggi, L., Orecchia, P., & Di Cave, D. (1988). Elmintofauna di specie ittiche eurialine di interesse commerciale del lago di Sabaudia (Latina-Italia). Parassitologia, 30(Suppl), 126–127.

    Google Scholar 

  • Palombi, A. (1931). Per una migliore conoscenza del Trematodi endoparassiti dei pesci del golfo di Napoli. I. Steringotrema divergens (Rud.) e Haploporus benedeni (Stoss.). Annuario del Museo Zoologico della R Università di Napoli N. S, 6, 1–15.

    Google Scholar 

  • Paperna, I. (1964). The metazoan parasite fauna of Israel inland water fishes. Bamidgeh. Bulletin of Fish Culture in Israel, 16, 3–66.

    Google Scholar 

  • Paperna, I., & Overstreet, R. M. (1981). Parasites and diseases of mullets (Mugilidae). In O. H. Oren (Ed.), Aquaculture of grey mullets (pp. 411–493). Cambridge: Cambridge University Press.

    Google Scholar 

  • Radujković, B. M., Orecchia, P., & Paggi, L. (1989). Parasites des poissons marins du Monténégro: Digenes. Acta Adriatica, 30, 137–187.

    Google Scholar 

  • Radujković, B. M., & Raibaut, A. (1989). Parasites des poissons marins du Monténégro: Liste des espèces de poissons avec leurs parasites. Acta Adriatica, 30, 307–319.

    Google Scholar 

  • Ragias, V., Athanassopoulou, F., & Sinis, A. (2005). Parasites of Mugilidae spp. reared under semi-intensive conditions in Greece. Bulletin of the European Association of Fish Pathologists, 25, 107–114.

    Google Scholar 

  • Ramadan, M. M., Saoud, M. F. A., Ashour, A. A., & Mansour, D. A. (1988). A review of the trematode genus Lecithobotrys (Haploporidae), with redescription of Lecithobotrys putrescens Looss, 1902 and Lecithobotrys helmymohamedi sp. n. from some Egyptian Lake Qarun fishes. Journal of the Egyptian Veterinary Medical Association, 48, 437–451.

    Google Scholar 

  • Rekharani, Z., & Madhavi, R. (1985). Digenetic trematodes from mullets of Visakhapatnam (India). Journal of Natural History, 19, 929–951.

    Article  Google Scholar 

  • Sampour, M. (2005). The ultrastructure of spermatogenesis of Haploporus benedenii (Haploporidae: Digenea). Bulletin of the European Association of Fish Pathologists, 25, 232–243.

    Google Scholar 

  • Sampour, M. (2006). The study of eggshell formation in Haploporus benedenii (Haploporidae: Digenea). Bulletin of the European Association of Fish Pathologists, 26, 217–221.

    Google Scholar 

  • Sampour, M. (2008). The study of vitelline gland of Haploporus lateralis (Digenea: Trematoda). Pakistan Journal of Biological Sciences, 11, 113–117.

    Article  PubMed  Google Scholar 

  • Sampour, M., & Mas-Coma, S. (2004). The ultrastructure of spermatogenesis of Haploporus benedenii (Haploporidae: Digenea). Multidisciplinarity for parasites, vectors and parasitic diseases. Proceedings of the IX European Multicolloquium of Parasitology, 2, 535–544.

  • Saoud, M. F. A., Ashour, A. A., Ramadan, M. M., & Lamloom, D. A. M. (1990). Helminth parasites of fishes from two inland lakes in Egypt. Japanese Journal of Parasitology, 39, 267–276.

    Google Scholar 

  • Sarabeev, V. (2000). [Seasonal dynamics of the parasitic infection of the pilengas in the northern part of the Azov Sea.] In: Materials of the international scientific conference of young scientists. Aquatic biological resources and ways of their rational use. Kiev, pp. 97–98 (In Russian).

  • Sarabeev, V. L., & Domnich, I. F. (2000). Age-related dynamics of parasitic infection of the pilengas (Mugil soiuy) in the Molochny Estuary of the Sea of Azov. Vestnik Zoologii, 14, 6–12 (In Russian).

    Google Scholar 

  • Sharma, P. N., & Gupta, A. N. (1970). Lecithobotrys vitellosus n. sp. (Haploporidae: Trematoda) from India. Rivista di Parassitologia, 31, 175–178.

    PubMed  CAS  Google Scholar 

  • Skrjabin, K. I. (1956). [Family Haploporidae Nicoll, 1914.] In K. I. Skrjabin (Ed.) [Trematodes of animals and man.] Osnovy Trematodologii, 12, 5–49 (In Russian).

  • Solonchenko, A. I., & Tkachuk, L. P. (1985). [Helminth infection of mullets from Azov-Black Sea basin.] Ekologiya Morya, Kiev, 20, 39–43 (In Russian).

    Google Scholar 

  • Stossich, M. (1887). Brani di elmintologia tergestina. Ser. 4. Bollletino della Società Adriatica di Scienzi Naturali in Trieste, 10, 90–96.

    Google Scholar 

  • van Beneden, P. J. (1870). Les poissons des côtes de Belgique, leurs parasites et leurs commensaux. Memoires de l’Académie des Sciences de Belgique, 38(4 mém.), 100 pp.

    Google Scholar 

  • Vlassenko, P. V. (1931). [On the parasitic worm fauna of fishes of the Black Sea.] Trudy Karadahs’koyi Biologichnoyi Stantsiyi imeni T.I. Vyazems’koho, 4, 88–136 (In Russian and German).

  • Wu, J.-y., Lu, J.-y., & Chen, Z.-s. (1999). Studies on the digenetic trematodes of shallow sea fishes from Guangdong Province, China. VI. Descriptions of two new species (Digenea). Acta Zootaxonomica Sinica, 24, 272–276 (In Chinese).

    Google Scholar 

  • Wu, J.-y., Lu, J.-y., & Zhu, T.-w. (1996). Studies on the digenetic trematodes of shallow sea fishes from Guangdong Province, China. IV. Descriptions of a new genus and a new species (Digenea, Monorchiidae). Acta Zootaxonomica Sinica, 21, 277–282 (In Chinese).

    Google Scholar 

  • Yamaguti, S. (1958). Systema helminthum. The digenetic trematodes of vertebrates (Vol. I). New York: Interscience, 1575 pp.

  • Yamaguti, S. (1971). Synopsis of the digenetic trematodes of vertebrates. Tokyo: Keigaku Publishing Co., Vol. I, 1074 pp; Vol. II, 349 pl.

  • Zabodash, V. M., & Semenenko, L. I. (1994). [Parasitic fauna of Mugil soiuy in water bodies of Ukraine.] Vestnik Zoologii, 2, 44–46 (In Russian).

Download references

Acknowledgements

We are grateful to Eileen Harris (Natural History Museum, London, UK) and Toshiaki Kuramochi (National Museum of Nature and Science, Tokyo, Japan) for the loan of specimens. This research was supported by an INTAS grant 03–51–5998; a FP6-MTKD grant (CT-2004-003175) to Juan Antonio Raga and Institute of Parasitology (Czech Academy of Sciences) grants (Z60220518 and LC522) to AK. IB-C benefitted from a doctoral fellowship from the Ministry of Science and Education of Spain (AP-2004-2999) and a visiting studentship to the Central Laboratory of General Ecology (Bulgarian Academy of Sciences).

Author information

Authors and Affiliations

  1. Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, P.O. Box 22 085, 46071, Valencia, Spain

    Isabel Blasco-Costa, Juan Antonio Balbuena & Juan Antonio Raga

  2. Department of Zoology, Natural History Museum, Cromwell Rd, London, SW7 5BD, UK

    David I. Gibson

  3. Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05, České Budějovice, Czech Republic

    Aneta Kostadinova

  4. Central Laboratory of General Ecology, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113, Sofia, Bulgaria

    Aneta Kostadinova

Authors
  1. Isabel Blasco-Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David I. Gibson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juan Antonio Balbuena
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juan Antonio Raga
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aneta Kostadinova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isabel Blasco-Costa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blasco-Costa, I., Gibson, D.I., Balbuena, J.A. et al. A revision of the Haploporinae Nicoll, 1914 (Digenea: Haploporidae) from mullets (Mugilidae): Haploporus Looss, 1902 and Lecithobotrys Looss, 1902. Syst Parasitol 73, 107–133 (2009). https://doi.org/10.1007/s11230-009-9175-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11230-009-9175-9

Keywords

Search

Navigation