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Parasitology Research

, Volume 114, Issue 10, pp 3721–3739 | Cite as

Macroparasites of allis shad (Alosa alosa) and twaite shad (Alosa fallax) of the Western Iberian Peninsula Rivers: ecological, phylogenetic and zoonotic insights

  • M. BaoEmail author
  • A. Roura
  • M. Mota
  • D.J. Nachón
  • C. Antunes
  • F. Cobo
  • K. MacKenzie
  • S. Pascual
Original Paper

Abstract

Samples of anadromous Alosa alosa (Clupeidae) (n = 163) and Alosa fallax (Clupeidae) (n = 223), caught in Western Iberian Peninsula Rivers from 2008 to 2013, were examined for buccal, branchial and internal macroparasites, which were identified using morphological and molecular methods. Alosa alosa were infected with Anisakis simplex s.s., Anisakis pegreffii, Hysterothylacium aduncum, Rhadinorhynchus pristis, Mazocraes alosae, Hemiurus appendiculatus, Ceratothoa italica and an unidentified ergasilid copepod. Ceratothoa italica represents a new host record for A. alosa. Alosa fallax were infected with A. simplex s.s., A. pegreffii, H. aduncum, H. appendiculatus, Clavellisa emarginata and an unidentified cymothoid isopod. This is the first report of C. italica, C. emarginata and M. alosae in the Iberian Peninsula. The phylogenetic positions of M. alosae, H. appendiculatus and C. emarginata were assessed using 18S and 28S ribosomal RNA (rRNA); our contributions provide a better understanding of the phylogenetic relationships within their groups. Qualitative and quantitative differences in the parasite faunas of these two shad species are consistent with different feeding strategies. The results provide information about host migration behaviour and transmission pathways through diet during the marine trophic phase of the shad’s life cycle and their roles as paratenic or final hosts and transporters of parasites between seawater and freshwater environments. The zoonotic parasites A. simplex s.s. and A. pegreffii pose a risk for consumers or riverine mammals (e.g. European otter). The use of parasites as biological tags for shad stocks in Western Iberian Rivers could be a useful approach in multidisciplinary studies concerning fish stock delimitation and characterization.

Keywords

Alosa spp Macroparasites Anisakis spp Phylogeny Freshwater Iberian Rivers 

Notes

Acknowledgments

The authors sincerely thank M.N. Cueto, J.M. Antonio and M.E. Garci of the ECOBIOMAR group at IIM-CSIC for molecular analysis, technical support and quality images of some parasites. M. Bao is supported by a PhD grant from the University of Aberdeen and also by financial support of the contract from the EU Project PARASITE (grant number 312068). A. Roura is supported by “Fundación Barrié de la Maza” postdoctoral fellowship and a Securing Food, Water and the Environment Research Focus Area grant (La Trobe University). This study was partially supported by a PhD grant from the Portuguese Foundation for Science and Technology (FCT) (SFRH/BD/44892/2008) and partially supported by the European Regional Development Fund (ERDF) through the COMPETE—Operational Competitiveness Programme and national funds through FCT—Foundation for Science and Technology, under the project “PEst-C/MAR/LA0015/2013. The authors thank the staff of the Station of Hydrobiology of the USC “Encoro do Con” due their participation in the surveys, with special mention to J. Sánchez for separating digenean fauna existing in the stomachs of A. fallax. This work has been partially supported by the project 10PXIB2111059PR of the Xunta de Galicia and the project MIGRANET of the Interreg IV B SUDOE (South-West Europe) Territorial Cooperation Programme (SOE2/P2/E288). D.J. Nachón is supported by a PhD grant from the Xunta de Galicia (PRE/2011/198).

Conflict of interests

The authors declare that they have no competing interests.

Authors’ contributions

MB and SP conceived and designed the study; MB, MM, DJN, CA and FC collected the data and collaborated in designing the study; MB performed the morphological identification studies; MB and AR performed the molecular genetic and phylogenetic studies; MB and KM performed the statistical analysis; MB, AR and KM analyzed the data and drafted the manuscript. All authors critically reviewed the manuscript and gave the final approval of the version to be published.

References

  1. Acolas ML, Bégout-Anras ML, Véron V, Jourdan H, Sabatié MR, Baglinière JL (2004) An assessment of upstream migration and reproductive behaviour of allis shad (Alosa alosa (L.)) using acoustic tracking. ICES J Mar Sci 61(8):1291–1304CrossRefGoogle Scholar
  2. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–722CrossRefGoogle Scholar
  3. Akmirza A (2013) Monogeneans of fish near Gökçeada, Turkey. Turk Zool Derg 37:441–448Google Scholar
  4. Aprahamian MW (1989) The diet of juvenile and adult twaite shad Alosa fallax fallax (Lacépède) from the rivers Severn and Wye (Britain). Hydrobiologia 179:173–182CrossRefGoogle Scholar
  5. Aprahamian MW, Baglinière JL, Sabatié MR, Alexandrino P, Aprahamian CD (2002) Synopsis of biological data on Alosa alosa and Alosa fallax spp. R&D Technical Report W1-014. Environment Agency R&D Dissemination Center, WRc, Frankland Road, Swindon, Wilts. SN5 8YF, pp. 314Google Scholar
  6. Arthur JR (1997) Recent advances in the use of parasites as biological tags for marine fish. In: Flegel TW, MacRae IH (eds) Diseases in Asian aquaculture III. Fish Health Section, Asian Fisheries Society, Manila, pp 141–154Google Scholar
  7. Assis CA, Almeida PR, Moreira F, Costa JL, Costa MJ (1992) Diet of twaite shad Alosa fallax (Lacépède) (Clupeidae) in the River Tagus Estuary, Portugal. J Fish Biol 41:1049–1050CrossRefGoogle Scholar
  8. Baglinière JL (2000) Le genre Alosa sp. In: Baglinière JL, Elie P (eds) Les aloses (Alosa alosa et Alosa fallax spp.). Écobiologie et variabilité des populations. CEMAGREF-INRA Editions, Paris, pp 3–30Google Scholar
  9. Baglinière JL, Sabatié MR, Rochard E, Alexandrino P, Aprahamian MW (2003) The Allis shad Alosa alosa: biology, ecology, range, and status of populations. Am Fish Soc Symp 35:85–102Google Scholar
  10. Bao M, Mota M, Nachón DJ, Antunes C, Cobo F, Garci ME, Pierce GJ, Pascual S (2015) Anisakis infection in allis shad, Alosa alosa (Linnaeus, 1758), and twaite shad, Alosa fallax (Lacépède, 1803) from Western Iberian Peninsula Rivers: zoonotic and ecological implications. Parasitol Res 114(6):2143–2154CrossRefPubMedGoogle Scholar
  11. Berland B (1989) Identification of larval nematodes from fish. In: Möller H (ed) Nematode problems in North Atlantic Fish. Workshop Report, Kiel, Germany, 3–4 April 1989. Int Counc Explor Sea CM/F:6, pp 16–22Google Scholar
  12. Bern Convention (1979) Convention on the Conservation of European Wildlife and Natural Habitats. Council of Europe: Bern, Switzerland. European Treaty Series number 104Google Scholar
  13. Bhat M, Cleland P (2010) Gastric anisakiasis. Clin Gastroenterol Hepatol 8(8):A20CrossRefPubMedGoogle Scholar
  14. Blair D, Bray RA, Barker SC (1998) Molecules and morphology in phylogenetic studies of the Hemiuroidea (Digenea: Trematoda: Platyhelminthes). Mol Phylogenet Evol 9(1):15–25CrossRefPubMedGoogle Scholar
  15. Boeger WA, Kritsky DC (1997) Coevolution of the Monogenoidea (Platyhelminthes) based on a revised hypothesis of parasite phylogeny. Int J Parasitol 27(12):1495–1511CrossRefPubMedGoogle Scholar
  16. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83(4):575–583CrossRefPubMedGoogle Scholar
  17. Bychowsky BE (1961) Monogenetic trematodes their systematics and phylogeny. English translation edited by Hargis WJ Jr. Washington: American Institute of Biological SciencesGoogle Scholar
  18. Cabral MJ, Almeida J, Almeida PR, Dellinger T, Ferrand de Almeida N, Oliveira ME, Palmeirim JM, Queiroz AL, Rogado L, Santos-Reis M (eds) (2006) Red book of the Portuguese vertebrates. 2nd ed. Instituto da Conservação da Natureza Assírio & Alvim LisboaGoogle Scholar
  19. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552CrossRefPubMedGoogle Scholar
  20. Catalano SR, Whittington ID, Donnellan SC, Gillanders BM (2014) Parasites as biological tags to assess host population structure: guidelines, recent genetic advances and comments on a holistic approach. Int J Parasitol Parasites Wildl 3:220–226CrossRefPubMedCentralPubMedGoogle Scholar
  21. Ceyhan T, Akyol O, Sever TM, Kara A (2012) Diet composition of adult twaite shad (Alosa fallax) in the Aegean Sea (Izmir Bay, Turkey). J Mar Biol Assoc UK 92(3):601–604CrossRefGoogle Scholar
  22. Cobo F, Nachón DJ, Vieira-Lanero R, Barca S, Sánchez-Hernández J, Rivas S, Couto MT, Gómez P, Silva S, Morquecho C, Lago L, Servia MJ (2010) Seguemento da poboación de saboga ou zamborca (Alosa fallax Lacépède, 1803) no río Ulla. Estación de Hidrobioloxía de “Encoro do Con”-Universidade de Santiago de Compostela. Xunta de GaliciaGoogle Scholar
  23. Costa MJ, Almeida PR, Domingos IM, Costa JL, Correia MJ, Chaves ML, Teixeira CM (2001) Present status of the main shads’ populations in Portugal. Bull Fr Peche Piscic 362(363):1109–1116CrossRefGoogle Scholar
  24. Cribb TH, Bray RA, Olson PD, Timothy D, Littlewood J (2003) Life cycle evolution in the Digenea: a new perspective from phylogeny. Adv Parasitol 54:197–254CrossRefPubMedGoogle Scholar
  25. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefPubMedGoogle Scholar
  26. Dawes B (1968) The trematoda. Cambridge University Press, LondonGoogle Scholar
  27. Dezfuli BS, Giari L, Simoni E, Menegatti R, Shinn AP, Manera M (2007) Gill histopathology of cultured European sea bass, Dicentrarchus labrax (L.), infected with Diplectanum aequans (Wagener 1857) Diesing 1958 (Diplectanidae: Monogenea). Parasitol Res 100:707–713CrossRefPubMedGoogle Scholar
  28. Doadrio I, Perea S, Garzón-Heydt P, González JL (2011) Ictiofauna continental española. Bases para su seguimiento. DG Medio Natural y Política Forestal. MARM, MadridGoogle Scholar
  29. Doherty D, O’Maoiléidigh N, McCarthy TK (2004) The biology, ecology and future conservation of twaite shad (Alosa fallax Lacépède), allis shad (Alosa alosa L.) and Killarney shad (Alosa fallax killarnensis Tate Regan) in Ireland. Biol Environ Proc R Ir Acad 104B:93–102CrossRefGoogle Scholar
  30. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  31. Gibson DI, Bray RA (1979) The Hemiuroidea: terminology, systematics and evolution. Bull Br Mus Nat Hist Zool 36:35–146Google Scholar
  32. Gibson DI, Bray RA (1986) The Hemiuridae (Digenea) of fishes from the north-east Atlantic. Bull Br Mus Nat Hist Zool 51:1–125Google Scholar
  33. Golvan YJ (1969) Systémaatique des acanthocéphales (Acanthocephala Rudolphi 1801). Première partie l’ordre des Palaecanthocephala Meyer 1931, première fascicule la super-famille des Echinorhynchoidea (Cobbold 1896) Golvan et Houin 1963. Mém Mus Natn Hist Nat 57:1–373Google Scholar
  34. Gregori M, Aznar FJ, Abollo E, Roura A, González AF, Pascual S (2012) Nyctiphanes couchii as intermediate host for the acanthocephalan Bolbosoma balaenae in temperate waters of the NE Atlantic. Dis Aquat Organ 99:37–47CrossRefPubMedGoogle Scholar
  35. Gregori M, Aznar FJ, Abollo E, Roura A, González AF, Pascual S (2013) Nyctiphanes couchii as intermediate host for Rhadinorhynchus sp. (Acanthocephala, Echinorhynchidae) from NW Iberian Peninsula waters. Dis Aquat Organ 105:9–20CrossRefPubMedGoogle Scholar
  36. Gregori M, Roura A, Abollo E, González AF, Pascual S (2015) Anisakis simplex complex (Nematoda: Anisakidae) in zooplankton communities from temperate NE Atlantic waters. J Nat Hist 49:755–773CrossRefGoogle Scholar
  37. Habitats Directive (1992) Council Directive 92/43/EEC on the Conservation of natural habitats and of wild fauna and flora. Off J L206:7–50Google Scholar
  38. Horton T (2000) Ceratothoa steindachneri (Isopoda: Cymothoidae) new to British waters with a key to north-east Atlantic and Mediterranean Ceratothoa. J Mar Biol Assoc UK 80(6):1041–1052CrossRefGoogle Scholar
  39. Huys R, Llewellyn-Hughes J, Olson PD, Nagasawa K (2006) Small subunit rDNA and Bayesian inference reveal Pectenophilus ornatus support assignment of Chondracanthidae and Xarifiidae to Lichomolgoidea (Cyclopoida). Biol J Linn Soc 87:403–425CrossRefGoogle Scholar
  40. Huys R, Llewellyn-Hughes J, Conroy-Dalton S, Olson PD, Spinks JN, Johnston DA (2007) Extraordinary host switching in siphonostomatoid copepods and the demise of the Monstrilloida: integrating molecular data, ontogeny and antennulary morphology. Mol Phylogenet Evol 43:368–378CrossRefPubMedGoogle Scholar
  41. Jolly MT, Aprahamian MW, Hawkins SJ, Henderson PA, Henderson PA, Hillman R, O’Maoiléidigh N, Maitland PS, Piper R, Genner MJ (2012) Population genetic structure of protected allis shad (Alosa alosa) and twaite shad (Alosa fallax). Mar Biol 159:675–687CrossRefGoogle Scholar
  42. Jovelin R, Justine JL (2001) Phylogenetic relationships within the polyopisthocotylean monogeneans (Platyhelminthes) inferred from partial 28S rDNA sequences. Int J Parasitol 31:393–401CrossRefPubMedGoogle Scholar
  43. Kabata Z (1979) Parasitic copepoda of British fishes. Ray Society, London, p 468Google Scholar
  44. Kabata Z (1992) Copepods parasitic on fishes: keys and notes for identification of the species. Synopses Br Fauna New Ser 47:1–264Google Scholar
  45. Kennedy CR (1981) The occurrence of Eubothrium fragile (Cestoda: Pseudophyllidae) in twaite shad, Alosa fallax (Lacépède) in the River Severn. J Fish Biol 19:171–177CrossRefGoogle Scholar
  46. Kleinertz S, Klimpel S, Palm HW (2012) Parasite communities and feeding ecology of the European sprat (Sprattus sprattus L.) over its range of distribution. Parasitol Res 110:1147–1157CrossRefPubMedGoogle Scholar
  47. Køie M (1990) On the morphology and life-history of Hemiurus luehei Odhner, 1905 (Digenea: Hemiuridae). J Helminthol 64:193–202CrossRefPubMedGoogle Scholar
  48. Køie M (1993) Aspects of the life cycle and morphology of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda, Ascaridoidea, Anisakidae). Can J Zool 71(7):1289–1296CrossRefGoogle Scholar
  49. Køie M (1995) The life-cycle and biology of Hemiurus communis Odhner, 1905 (Digenea, Hemiuridae). Parasite 2(2):195–202CrossRefGoogle Scholar
  50. Kuchta R, Hanzelová V, Shinn AP, Poddubnaya LG, Scholz T (2005) Redescription of Eubothrium fragile (Rudolphi, 1802) and E. rugosum (Batsch, 1786) (Cestoda: Pseudophyllidea), parasites of fish in the Holarctic region. Folia Parasitol 52:251–260CrossRefPubMedGoogle Scholar
  51. La Mesa G, Annunziatellis A, Jr E-F, Fortuna CM (2015) Modeling environmental, temporal and spatial effects on twaite shad (Alosa fallax) by-catches in the central Mediterranean Sea. Fish Oceanogr 24(2):107–117CrossRefGoogle Scholar
  52. Li M, Shi S-F, Brown CL, Yang T-B (2011) Phylogeographical pattern of Mazocraeoides gonialosae (Monogenea, Mazocraeidae) on the dotted gizzard shad, Konosirus punctatus, along the coast of China. Int J Parasitol 41(12):1263–1272CrossRefPubMedGoogle Scholar
  53. Lia RP, Zizzo N, Tinelli A, Lionetti A, Cantacessi C, Otranto D (2007) Mass mortality in wild greater amberjack (Seriola dumerili) infected by Zeuxapta seriolae (Monogenea: Heteraxinidae) in the Ionian Sea. Bull Eur Assoc Fish Pathol 27(3):108–111Google Scholar
  54. Littlewood DTJ, Rohde K, Clough KA (1999) The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biol J Linn Soc 66:75–114CrossRefGoogle Scholar
  55. MacKenzie K (1987) Parasites as indicators of host populations. Int J Parasitol 17(2):345–352CrossRefPubMedGoogle Scholar
  56. MacKenzie K, Hemmingsen W (2014) Parasites as biological tags in marine fisheries research: European Atlantic waters. Parasitology 142(01):54–67CrossRefPubMedGoogle Scholar
  57. Maitland PS, Lyle AA (2005) Ecology of Allis shad Alosa alosa and Twaite shad Alosa fallax in the Solway Firth, Scotland. Hydrobiologia 534:205–221CrossRefGoogle Scholar
  58. Mamaev YL (1982) Notes on the systematics of mazocraeid monogeneans with a redescription of some poorly studied taxa. Helminthologia 19:25–39Google Scholar
  59. Martin J, Rougemont Q, Drouineau H, Launey S, Jatteau P, Bareille G, Berail S, Pécheyran C, Feunteun E, Roques S, Clavé D, Nachón DJ, Antunes C, Mota M, Réveillac E, Daverat F (2015) Dispersal capacities of anadromous Allis shad population inferred from a coupled genetic and otolith approach. Can J Fish Aquat Sci. doi: 10.1139/cjfas-2014-0510 Google Scholar
  60. MIGRANET (2012) Observatorio de las Poblaciones de Peces Migradores en el Espacio SUDOE. Informe General del Estado de Conservación y Amenazas de las Especies de Peces Migradores: Ríos Ulla y Umia de Galicia (España); Río Nivelle de Aquitaine (Francia) y Tramo Internacional del Río Miño (Portugal-Norte)Google Scholar
  61. Mladineo I, Poljak V (2014) Ecology and genetic structure of zoonotic Anisakis spp. from Adriatic commercial fish species. Appl Environ Microbiol 80(4):1281–1290CrossRefPubMedCentralPubMedGoogle Scholar
  62. Mollaret I, Jamieson BGM, Justine JL (2000) Phylogeny of the Monopisthocotylea and Polyopisthocotylea (Platyhelminthes) inferred from 28S rDNA sequences. Int J Parasitol 30:171–185CrossRefPubMedGoogle Scholar
  63. Moravec F (2004) Metazoan parasites of salmonid fishes of Europe. Academia (Praha). pp 510Google Scholar
  64. Mota M, Antunes C (2011) First report on the status of Allis shad (Alosa alosa) in the Minho River (Northwestern Iberian Peninsula). J Appl Ichthyol 27(3):56–59CrossRefGoogle Scholar
  65. Mota M, Antunes C (2012) A preliminary characterization of the habitat use and feeding of Allis shad (Alosa alosa) juveniles in the Minho river tidal freshwater wetlands. Limnetica 31(1):165–172Google Scholar
  66. Mota M, Bio A, Bao M, Pascual S, Rochard E, Antunes C (2015) New insights into biology and ecology of the Minho River Allis shad Alosa alosa L.—contribution to the conservation of one of the last European shad populations. Rev Fish Biol Fish 25(2):395–412CrossRefGoogle Scholar
  67. Nachón DJ, Sánchez-Hernández J, Vieira-Lanero R, Cobo F (2013) Feeding of twaite shad, Alosa fallax (Lacépède, 1803), during the upstream spawning migration in the River Ulla (NW Spain). Mar Freshw Res 64:233–236CrossRefGoogle Scholar
  68. Nunn AD, Noble RAA, Harvey JP (2008) The diets and parasites of larval and 0+ juvenile twaite shad in the lower reaches and estuaries of rivers Wye, Usk, and Towy, UK. Hydrobiologia 614:209–218CrossRefGoogle Scholar
  69. Olson PD, Littlewood DTJ (2002) Phylogenetics of the Monogenea—evidence from a medley of molecules. Int J Parasitol 32:233–244CrossRefPubMedGoogle Scholar
  70. Olson PD, Tkach VV (2005) Advances and trends in the molecular systematics of the parasitic platyhelminthes. Adv Parasitol 60:165–243CrossRefPubMedGoogle Scholar
  71. Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33:733–755CrossRefPubMedGoogle Scholar
  72. OSPAR (2009) Background document for Allis shad Alosa alosa. Biodiversity series. Publication Number: 418/2009Google Scholar
  73. Özer A, Öztürk T, Kornyychuk Y (2013) First report of Mazocraes alosae (Herman, 1782), Pronoprymna ventricosa (Rudolphi, 1891) and Lecithaster confusus Odhner, 1905 in pontic shad Alosa immaculata Bennet, 1835 near Turkish coast of the Black Sea. Lucrări Ştiinţifice Ser Zootehnie 59:311–314Google Scholar
  74. Pankov P, Webster BL, Blasco-Costa I, Gibson DI, Littlewood DTJ, Balbuena JA, Kostadinova A (2006) Robinia aurata n.g., n. sp. (Digenea: Hemiuridae) from the mugilid Liza aurata with a molecular confirmation of its position within the Hemiuroidea. Parasitology 133(2):217–227CrossRefPubMedGoogle Scholar
  75. Pereira TG, Batista I, Bandarra NM, Ferreira J, Fradinho N, Afonso F (2013) Chemical composition and nutritional value of raw and fried allis shad (Alosa alosa). Int J Food Sci Technol 48:1303–1308CrossRefGoogle Scholar
  76. Rodrigues HO, Carvalho-Varela M, Rodrigues e Rigoletto SS (1972) Alguns trematódeos digenéticos de peixes do Oceano Atlântico–Costa Continental Portuguésa Costa Continental de Africa [Some digenic trematodes of fish from the Atlantic Ocean—the continental Portuguese coast and the continental African coast]. Atlas da Sociedade De Biologia do Rio De Janeiro 15:87–93Google Scholar
  77. Rokicki J, Rolbiecki L, Skóra A (2009) Helminth parasites of twaite shad, Alosa fallax (Actinopterygh: Clupeiformes: Clupeidae), from the Southern Baltic Sea. Acta Ichthyol Piscat 39(1):7–10CrossRefGoogle Scholar
  78. Rosen DE (1982) Teleostean interrelationships, morphological function and evolutionary inference. Am Zool 22:261–273Google Scholar
  79. Rougier T, Lambert P, Drouineau H, Girardin M, Castelnaud G, Carry L, Aprahamian M, Ribot E, Rochard R (2012) Collapse of Allis shad, Alosa alosa, in the Gironde system (southwest France): environmental change, fishing mortality, or Allee effect? ICES J Mar Sci 69(10):1802–1811CrossRefGoogle Scholar
  80. Roura A, Álvarez-Salgado XA, González AF, Gregori M, Rosón G, Guerra A (2013) Short-term meso-scale variability of mesozooplankton communities in a coastal upwelling system (NW Spain). Prog Oceanogr 109:18–32CrossRefGoogle Scholar
  81. Sabatié MR (1993) Recherches sur l’écologie et la biologie des aloses au Maroc (Alosa alosa Linné, 1758 et Alosa fallax Lacépède, 1803): exploitation et taxonomie des populations atlantiques, bioécologie des aloses de l’Ouest Sebou. Ph.D. thesis. University of Bretagne Occidentale, BrestGoogle Scholar
  82. Sala-Bozano M, Van-Oosterhout C, Mariani S (2012) Impact of a mouth parasite in a marine fish differs between geographical areas. Biol J Linn Soc 105:842–852CrossRefGoogle Scholar
  83. Shih HH, Jeng MS (2002) Hysterothylacium aduncum (Nematoda: Anisakidae) infecting a herbivorous fish, Siganus fluorescens, off the Taiwanese coast of the Northwest Pacific. Zool Stud 41(2):208–215Google Scholar
  84. Silva S, Servia MJ, Vieira-Lanero R, Cobo F (2013) Downstream migration and hematophagous feeding of newly metamorphosed sea lampreys (Petromyzon marinus Linnaeus, 1758). Hydrobiologia 700(1):277–286CrossRefGoogle Scholar
  85. Skóra ME, Sapota MR, Skóra KE, Pawelec A (2012) Diet of twaite shad Alosa fallax (Lacépède, 1803) (Clupeidae) in the Gulf of Gdansk, the Baltic Sea. Oceanol Hydrobiol Stud 41(3):24–32CrossRefGoogle Scholar
  86. Smith JW (1983) Larval Anisakis simplex (Rudolphi, 1809, det. Krabbe, 1878) and larval Hysterothylacium sp. (Nematoda: Ascaridoidea) in euphausiids (Crustacea: Malacostraca) in the North-East Atlantic and northern North Sea. J Helminthol 57:167–177CrossRefGoogle Scholar
  87. Solórzano M (2004) Peixes. In: Viéitez E, Rey JM (eds) A natureza ameazada. Consello da Cultura Galega. Sección de Patrimonio CulturalGoogle Scholar
  88. Suzuki N, Hoshino K, Murakami K, Takeyama H, Chow S (2008) Molecular diet analysis of Phyllosoma larvae of the Japanese spiny lobster Palinurus japonicus (Decapoda: Crustacea). Mar Biotechnol 10:49–55CrossRefPubMedGoogle Scholar
  89. Taverny C, Elie P (2001a) Répartition spatio-temporelle de la grande alose Alosa alosa (Linné, 1766) et de L’alose feinte Alosa fallax (Lacépède, 1803) dans le golfe de Gascogne. Bull Fr Peche Piscic 362(363):803–821CrossRefGoogle Scholar
  90. Taverny C, Elie P (2001b) Régime alimentaire de la grande alose Alosa alosa (Linné, 1766) et de L’alose feinte Alosa fallax (Lacépède, 1803) dans le golfe de Gascogne. Bull Fr Peche Piscic 362(363):837–852CrossRefGoogle Scholar
  91. Taverny C, Cassou-Leins JJ, Cassou-Leins F, Elie P (2000) De l’oeuf à l’adulte en mer. In: Baglinière JL, Elie P (eds) Les aloses (Alosa alosa et Alosa fallax spp.). Écobiologie et variabilité des populations. INRACEMAGREF, Paris, pp 93–124Google Scholar
  92. Trancart T, Rochette S, Acou A, Lasne E, Feunteun E (2014) Modeling marine shad distribution using data from French bycatch fishery surveys. Mar Ecol Prog Ser 511:181–192CrossRefGoogle Scholar
  93. Williams HH, MacKenzie K, McCarthy AM (1992) Parasites as biological indicators of the population biology, migrations, diet and phylogenetics of fish. Rev Fish Biol Fish 2:144–176CrossRefGoogle Scholar
  94. XUNTA (2008) Plan Galego de Ordenación dos recursos piscícolas e ecosistemas acuáticos continentais. Xunta de GaliciaGoogle Scholar
  95. Yamaguti S (1963) Systema helminthum, vol V, Acanthocephala. Wiley Interscience, New YorkGoogle Scholar
  96. Yamaguti S (1968) Systema helminthum, vol IV, Monogenea and Aspidogotylea. Wiley Interscience, New YorkGoogle Scholar
  97. Zhu X, Gasser RB, Jacobs DE, Hung GC, Chilton NB (2000) Relationship among some ascaridoid nematodes based on ribosomal DNA sequence data. Parasitol Res 86:738–744CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • M. Bao
    • 1
    • 2
    • 3
    Email author
  • A. Roura
    • 1
    • 4
  • M. Mota
    • 5
    • 6
    • 7
  • D.J. Nachón
    • 8
    • 9
  • C. Antunes
    • 6
    • 7
  • F. Cobo
    • 8
    • 9
  • K. MacKenzie
    • 10
  • S. Pascual
    • 1
  1. 1.ECOBIOMARInstituto de Investigaciones Marinas (CSIC)VigoSpain
  2. 2.OCEANLABUniversity of AberdeenNewburghUK
  3. 3.College of Physical Science, School of Natural and Computing SciencesUniversity of AberdeenAberdeenUK
  4. 4.Department of Ecology, Environment and EvolutionLa Trobe UniversityMelbourneAustralia
  5. 5.ICBAS–Institute of Biomedical Sciences Abel SalazarUniversity of PortoPortoPortugal
  6. 6.Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR)University of PortoPortoPortugal
  7. 7.Aquamuseum of Minho RiverVila Nova de CerveiraPortugal
  8. 8.Department of Zoology and Physical Anthropology, Faculty of BiologyUniversity of Santiago de CompostelaSantiago de CompostelaSpain
  9. 9.Station of Hydrobiology ‘Encoro do Con’Vilagarcía de ArousaSpain
  10. 10.School of Biological Sciences (Zoology)University of AberdeenAberdeenUK

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