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Description of a new species of rhinebothriidean tapeworm from the skate Dipturus batis in the Mediterranean Sea

Published online by Cambridge University Press:  17 August 2018

K. Benmeslem ,
H.S. Randhawa Open the ORCID record for H.S. Randhawa [Opens in a new window]  and
F. Tazerouti
K. Benmeslem
Affiliation:
Université des Sciences et de la Technologie Houari Boumediene, Faculté des Sciences Biologiques, Laboratoire de Biodiversité et Environnement: Interactions et Génomes, BP 32, El Alia Bab Ezzouar, Alger, Algeria
H.S. Randhawa*
Affiliation:
Directorate of Natural Resources, Fisheries Department, Falkland Islands Government, Bypass Road, Stanley, Falkland Islands, FIQQ 1ZZ; South Atlantic Environmental Research Institute, Stanley Cottage, Stanley, Falkland Islands, FIQQ 1ZZ; New Brunswick Museum, 277 Douglas Avenue, Saint John, New Brunswick, Canada, E2K 1E5
F. Tazerouti
Affiliation:
Université des Sciences et de la Technologie Houari Boumediene, Faculté des Sciences Biologiques, Laboratoire de Biodiversité et Environnement: Interactions et Génomes, BP 32, El Alia Bab Ezzouar, Alger, Algeria
*
Author for correspondence: H.S. Randhawa E-mail: [email protected]
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Abstract

Examination of rajid skates off the Algerian coast in the Mediterranean Sea revealed that three of the 33 Dipturus batis Linnaeus, 1758 examined harboured a new tapeworm species: Echeneibothrium algeriensis n. sp. This new species, collected from the anterior half of the spiral valves, is described on the basis of morphological data from light and scanning electron microscopy. The new species differs from previously described Echeneibothrium species by details of the scolex and loculi, total length, the length of the myzorhynchus, the number of proglottides, and the number of testes. Comparison of the diets of the ten skate species common in the Mediterranean basin indicates some varying degree of overlap, suggesting that host specificity in this host–parasite system is determined by other host and/or ecological variables such as adaptations of the parasites to their respective hosts, either on the morpho-anatomical level, in physiological characteristics of the parasite's habitat, in the trophic requirements for the successful transmission of the parasite, or in adaptations to the behavioural characteristics of the host. Furthermore, restricted overlap of E. algeriensis n. sp. with congeners in parasite assemblages of D. batis indicates some structuring according to attachment-site preferences. However, attachment-site preferences are not explained solely by morphological compatibility between bothridia and villi. This study reiterates the need to examine multiple factors synergistically in studies on host specificity of parasites, and the need to examine the parasite fauna of hosts across their entire geographical range in order to truly appreciate the biodiversity they harbour.

Keywords

Algerian coastbiodiversityCestodaDipturus batisEcheneibothrium algeriensis n. spEcheneibothriumMediterranean SeaRajiformesRhinebothriideatapeworms
Type
Research Paper
Information
Journal of Helminthology , Volume 93 , Issue 5 , September 2019 , pp. 589 - 600
Copyright
Copyright © Cambridge University Press 2018 

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References

Alexander, CG (1963) Tetraphyllidean and diphyllidean cestodes of New Zealand Selachians. Transactions of the Royal Society of New Zealand (Zoology) 3, 117–142.Google Scholar
Bianchi, CN and Morri, C (1994) Southern species in the Ligurian Sea (Northern Mediterranean): new records and a review. Bollettino dei Musei e degli Istituti Biologici dell'Università di Genova 58–59, 181–197.Google Scholar
Braccini, JM and Perez, JE (2005) Feeding habits of the sandskate Psammobatis extenta (Garman, 1913): sources of variation in dietary composition. Marine and Freshwater Research 56, 395–403.Google Scholar
Bradai, MN, Saidi, B and Enajjar, S (2012) Elasmobranchs of the Mediterranean and Black Sea: Status, Ecology and Biology. A Bibliographic Analysis. Studies and Reviews. General Fisheries Commission for the Mediterranean. No. 91. Rome: FAO, 108 pp.Google Scholar
Bueno, VM and Caira, JN (2017) Redescription and molecular assessment of relationships among three species of Echeneibothrium (Rhinebothriidea: Echeneibothriidae) parasitizing the yellownose skate, Dipturus chilensis, in Chile. Journal of Parasitology 103, 268–284.Google Scholar
Caira, JN and Healy, CJ (2004) Elasmobranchs as hosts of metazoan parasites. In Carrier, JC, Musick, JA and Heithaus, MR (eds), Biology of Sharks and their Relatives. Boca Raton, FL: CRC Press, pp. 523–551.Google Scholar
Caira, JN and Jensen, K (2014) A digest of tapeworms. Journal of Parasitology 100, 373–391.Google Scholar
Caira, JN and Jensen, K (eds) (2017) Planetary Biodiversity Inventory (2008–2017): Tapeworms from the Vertebrate Bowels of the Earth. Special Publication No. 25. Lawrence, KS: The University of Kansas Natural History Museum, 463 pp.Google Scholar
Caira, JN, Jensen, K and Healy, CJ (1999) On the phylogenetic relationships among tetraphyllidean, lecanicephalidean and diphyllidean tapeworm genera. Systematic Parasitology 42, 77–151.Google Scholar
Caira, JN et al. (2013) Phylogenetic analysis and reconfiguration of genera in the cestode order Diphyllidea. International Journal for Parasitology 43, 621–639.Google Scholar
Caira, JN et al. (2014) Orders out of chaos – molecular phylogenetics reveals the complexity of shark and stingray tapeworm relationships. International Journal of Parasitology 44, 55–73.Google Scholar
Caira, JN et al. (2017a) Three new genera of rhinebothriidean cestodes from stingrays in Southeast Asia. Folia Parasitologica 64, 008.Google Scholar
Caira, JN et al. (2017b) An overview of tapeworms from the vertebrate bowels of the Earth. In Caira, JN and Jensen, K (eds), Planetary Biodiversity Inventory (2008–2017): Tapeworms from the Vertebrate Bowels of the Earth. Special Publication No. 25. Lawrence, KS: The University of Kansas Natural History Museum, pp. 1–20.Google Scholar
Campbell, RA (1975) Two new species of Echeneibothrium (Cestoda: Tetraphyllidea) from skates in the Western Atlantic. Journal of Parasitology 61, 95–99.Google Scholar
Campbell, RA (1977) New tetraphyllidean and trypanorhynch cestodes from deep sea skates in the Western North Atlantic. Proceedings of the Helminthological Society of Washington 44, 191–197.Google Scholar
Carvajal, J and Dailey, MD (1975) Three new species of Echeneibothrium (Cestoda: Tetraphyllidea) from the skate, Raja chilensis Guichenot, 1848, with comments on mode of attachment and host specificity. Journal of Parasitology 61, 89–94.Google Scholar
Combes, C, Renaud, F and Le Brun, N (1991) Systématique et écologie: le point de vue d'un Parasitologiste. Biosystema 6, 55–68.Google Scholar
Cuoco, C, Mancusi, C and Serena, F (2005) Studio delle abitudini alimentari di Raja asterias Delaroche, 1809 (Chondrichthyes, Rajidae). Biologia Marina Mediterranea 12, 504–508.Google Scholar
Dulvy, NK and Reynolds, JD (2002) Predicting extinction vulnerability in skates. Conservation Biology 16, 440–450.Google Scholar
Dulvy, NK et al. (2006) Dipturus batis. The IUCN Red List of Threatened Species 2006: e.T39397A10198950, http://dx.doi.org/10.2305/IUCN.UK.2006.RLTS.T39397A10198950.enGoogle Scholar
Ebert, DA and Bizzarro, JJ (2007) Standardized diet compositions and trophic levels of skates (Chondrichthyes: Rajiformes: Rajoidei). Environmental Biology of Fishes 80, 221–237.Google Scholar
Euzet, L (1956) Une nouvelle espèce d’Echeneibothrium van Beneden, 1850. Bulletin de la Société Neuchâteloise des Sciences Naturelles 79, 39–41.Google Scholar
Euzet, L (1959) Recherches sur les cestodes Tétraphyllides de Sélaciens des côtes de France (Doctoral dissertation). Université de Montpellier, Montpellier, France.Google Scholar
Euzet, L (1994) Order Tetraphyllidea Carus, 1863. In Khalil, LF, Jones, A and Bray, RA (eds), Keys to the Cestode Parasites of Vertebrates. Cambridge: CAB International, pp. 149–194.Google Scholar
Euzet, L and Combes, C (1980) Les problèmes de l'espèce chez les animaux parasites. Mémoire de la Société Zoologique de France 40, 239–285.Google Scholar
FAO (Food and Agriculture Organization of the United Nations) (2009) Sharks and Rays of the Mediterranean and Black Sea. FAO Species Identification Cards. Rome: FAO, 113 pp.Google Scholar
Farias, I et al. (2006) Diet comparison of four ray species (Raja clavata, Raja brachyura, Raja montagui and Leucoraja naevus) caught along the Portuguese continental shelf. Aquatic Living Resources 19, 105–114.Google Scholar
Fatimetou, MK and Younes, S (2016) Diet of Raja asterias (Delaroche, 1809) caught along the Mediterranean part of the Moroccan coast (Northern Morocco). Journal of the Black Sea/Mediterranean Environment 22, 182–189.Google Scholar
Fischer, W, Bauchot, M-L and Schneider, M (1987) Fiches FAO d'identification des espèces pour les besoins de la pêche. (Révision 1). Méditerranée et Mer Noire. Zone de pêche 37, Volume 2. Vertébrés. Rome: FAO, pp. 761–1530.Google Scholar
Follesa, MC et al. (2012) Preliminary observations of the reproductive biology and diet for the Norwegian skate Dipturus nidarosiensis (Rajidae) from the Central Western Mediterranean Sea. Cybium 36, 473–477.Google Scholar
Griffiths, AM et al. (2010) Molecular markers reveal spatially segregated cryptic species in a critically endangered fish, the common skate (Dipturus batis). Proceedings of the Royal Society B 277, 1497–1503.Google Scholar
Hart, JF (1936) Cestoda from fishes of Puget Sound: III. Phyllobothrioidea. Transactions of the American Microscopical Society 55, 488–496.Google Scholar
Haseli, M et al. (2012) Two new species of Echinobothrium van Beneden, 1849 (Cestoda: Diphyllidea) from the Persian Gulf. Systematic Parasitology 82, 201–209.Google Scholar
Healy, CJ et al. (2009) Proposal for a new tapeworm order, Rhinebothriidea. International Journal for Parasitology 39, 497–511.Google Scholar
Hemida, F, Sergoua, W and Seridji, R (2007) Nouvelle liste commentée des raies du Bassin algérien. Rapport et Procès Verbaux des Réunions – Commission Internationale pour l'Exploration Scientifique de la Mer Méditerranée 38, 497.Google Scholar
Jensen, K (2005) Tapeworms of elasmobranchs (part I). A monograph on the Lecanicephalidea (Platyhelminthes, Cestoda). Bulletin of the University of Nebraska State Museum 18, 1–241.Google Scholar
Jereb, P et al. (eds) (2015) Cephalopod Biology and Fisheries in Europe: II. Species Accounts. ICES Cooperative Research Report 325. Copenhagen: International Council for the Exploration of the Sea, 360 pp.Google Scholar
Kadri, H et al. (2010) Régime alimentaire du pocheteau noir, Dipturus oxyrinchus, dans le Golfe de Gabes (Tunisie). Rapport et Procès Verbaux des Réunions – Commission Internationale pour l'Exploration Scientifique de la Mer Méditerranée 39, 551.Google Scholar
Keeling, CP and Burt, MDB (1996) Echeneibothrium canadensis n. sp. (Tetraphyllidea: Phyllobothriidae) in the spiral intestine of the thorny skate (Raja radiata) from the Canadian Atlantic Ocean. Canadian Journal of Zoology 74, 1590–1593.Google Scholar
Lucifora, LO et al. (2000) Feeding habits and prey selection by the skate Dipturus chilensis (Elasmobranchii: Rajidae) from the south-western Atlantic. Journal of the Marine Biological Association of the United Kingdom 80, 953–954.Google Scholar
Manger, BR (1972) Some cestode parasites of the elasmobranchs Raja batis and Squalus acanthias from Iceland. Bulletin of the British Museum of Natural History 24, 161–183.Google Scholar
Mulas, A et al. (2015) Diet and feeding behaviour of longnosed skate Dipturus oxyrinchus. Journal of Fish Biology 86, 121–138.Google Scholar
Poulin, R et al. (2016) Missing links: testing the completeness of host–parasite checklists. Parasitology 143, 114–122.Google Scholar
Randhawa, HS (2012) Numerical and functional responses of intestinal helminths in three rajid skates: evidence for competition between parasites? Parasitology 139, 1784–1793.Google Scholar
Randhawa, HS and Burt, MDB (2008) Determinants of host specificity and comments on attachment-site specificity of tetraphyllidean cestodes infecting rajid skates from the Northwest Atlantic. Journal of Parasitology 94, 436–461.Google Scholar
Randhawa, HS and Poulin, R (2010) Determinants of tapeworm species richness in elasmobranch fishes: untangling environmental and phylogenetic influences. Ecography 33, 866–877.Google Scholar
Randhawa, HS, Saunders, GW and Burt, MDB (2007) Establishment of the onset of host specificity in four phyllobothriid tapeworm species (Cestoda: Tetraphyllidea) using a molecular approach. Parasitology 134, 1291–1300.Google Scholar
Randhawa, HS et al. (2008) Redescription of Pseudanthobothrium hanseni Baer, 1956 and description of P. purtoni n. sp. (Cestoda: Tetraphyllidea) from different pairs of rajid skate hosts, with comments on the host specificity of the genus in the northwest Atlantic. Systematic Parasitology 70, 41–60.Google Scholar
Refés, W, Semahi, N and Boulahdid, M (2010) Diversité et biogéographie de l'ichtyofaune orientale de la côte algérienne. Journal des Sciences Halieutiques et Aquatiques 3, 54–66.Google Scholar
Riser, NW (1955) Studies on cestode parasites of sharks and skates. Journal of the Tennessee Academy of Sciences 30, 265–311.Google Scholar
Romanelli, M et al. (2007) Commercial catches, reproduction and feeding habits of Raja asterias (Chondrichthyes: Rajidae) in a coastal area of the Tyrrhenian Sea (Italy, northern Mediterranean). Acta Adriatica 48, 57–71.Google Scholar
Ruhnke, TR (2011) Tapeworms of elasmobranchs (part III). A monograph on the Phyllobothriidae (Platyhelminthes, Cestoda). Bulletin of the University of Nebraska State Museum 25, 1–208.Google Scholar
Ruhnke, TR, Caira, JN and Cox, A (2015) The cestode order Rhinebothriidea no longer family-less: a molecular phylogenetic investigation with erection of two new families and description of eight new species of Anthocephalum. Zootaxa 3904, 51–81.Google Scholar
Ruhnke, TR, Reyda, FB and Marques, FPL (2017) Rhinebothriidea. In Caira, JN and Jensen, K (eds), Planetary Biodiversity Inventory (2008–2017): Tapeworms from the Vertebrate Bowels of the Earth. Special Publication No. 25. Lawrence, KS: The University of Kansas Natural History Museum, pp. 327–348.Google Scholar
Šantic, M, Rada, B and Pallaoro, A (2013) Feeding habits of brown ray (Raja miraletus Linnaeus, 1758) from the eastern central Adriatic Sea. Marine Biology Research 9, 316–323.Google Scholar
Tazerouti, F, Euzet, L and Kechemir-Issad, N (2007) Redescription de trois espèces de Calyptrobothrium Monticelli, 1893 (Tetraphyllidea: Phyllobothriidae) parasites de Torpedo marmorata et T. nobiliana (Elasmobranchii: Torpedinidae). Remarques sue leur spécificité parasitaire et sur la position taxonomique des espèces auparavant attribuées à C. riggii Monticelli, 1893. Systematic Parasitology 67, 175–185.Google Scholar
Tazerouti, F, Kechemir-Issad, N and Euzet, L (2009) Acanthobothrium minus n. sp. (Tetraphyllidea: Onchobotriidae) parasite de Raja asterias (Elasmobranchii : Rajidae) en Méditerranée. Parasite 16, 203–207.Google Scholar
Tyler, GA (2006) Tapeworms of elasmobranchs (part II). A monograph on the Diphyllidea (Platyhelminthes, Cestoda). Bulletin of the University of Nebraska State Museum 20, 1–142.Google Scholar
Vannucci, S et al. (2006) Feeding ecology of rays in the southern Ligurian Sea. Biologia Marina Mediterranea 13, 296–297.Google Scholar
Vargas-Caro, C et al. (2015) A review of longnose skates Zearaja chilensis and Dipturus trachyderma (Rajiformes: Rajidae). Universitas Scientiarum 20, 321–359.Google Scholar
Waeschenbach, A et al. (2007) Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Molecular Phylogenetics and Evolution 45, 311–325.Google Scholar
Wheeler, A (1969) The Fishes of the British Isles and North-west Europe. London: Macmillan, 613 pp.Google Scholar
Williams, HH (1960) The intestine in members of the genus Raja and host-specificity in the Tetraphyllidea. Nature 188, 514–516.Google Scholar
Williams, HH (1966) The ecology, functional morphology and taxonomy of Echeneibothrium Beneden, 1849 (Cestoda: Tetraphyllidea), a revision of the genus and ocmments on Discobothrium Beneden, 1870, Pseudanthobothrium Baer, 1956, and Phormobothrium Alexander, 1963. Parasitology 56, 227–285.Google Scholar
Williams, HH (1968) The taxonomy, ecology and host-specificity of some Phyllobothriidae (Cestoda: Tetraphyllidea), a critical revision of Phyllobothrium Beneden, 1849 and comments on some allied genera. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 253, 231–307.Google Scholar
Williams, HH (1969) The genus Acanthobothrium Beneden 1849 (Cestoda: Tetraphyllidea). Nytt Magasin für Zoologi 17, 1–56.Google Scholar
Woodland, WNF (1927) A revised classification of tetraphyllidean Cestoda, with descriptions of some Phyllobothriidae from Plymouth. Proceedings of the Zoological Society of London 97, 519–548.Google Scholar
Yemisken, E et al. (2018) Feeding habits of three batoids in the Levantine Sea (north-eastern Mediterranean Sea) based on stomach content and isotopic data. Journal of the Marine Biological Association of the United Kingdom 98, 89–96.Google Scholar
Zschokke, F (1889) Recherches sur la structure anatomique et histologique des cestodes. Mémoirs de l'Institut National Genevois 17, 1–396.Google Scholar