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Metazoan parasite communities in Alosa alosa (Linnaeus, 1758) and Alosa fallax (Lacépède, 1803) (Clupeidae) from North-East Atlantic coastal waters and connected rivers

Abstract

Metazoan parasites were studied in 96 Alosa alosa and 78 Alosa fallax from North-East Atlantic coastal waters and connected rivers (among them three sympatric sites) in order to increase knowledge on these anadromous endangered fish and measure the parasitic impact on host condition. All shads were infected by one to six metazoan parasite taxa among the 12 identified in the whole sampling, with a mean abundance of parasites higher for A. alosa (167 ± 10) than for A. fallax (112 ± 11). Helminths, mostly trophically transmitted, were the best represented (eight taxa, prevalence up to 99%) in contrast with crustaceans and Petromyzontidae that rarely occurred (four taxa, prevalence <6%). Despite some quantitative differences, metazoan parasite communities of A. alosa and A. fallax remained stable in composition whatever the host developmental stage, sex, sample site, and salinity. Among the nine parasite taxa harbored by each Alosa species, six were shared with some differences in distribution patterns including in sympatric conditions, suggesting increasing dissimilarities between A. alosa and A. fallax with the age. Information on feeding ecology provided by trophically transmitted helminths confirmed euryphagous opportunistic diet of immatures and adults of both shad species, and assessed feeding of adults during spawning migrations. Our study also revealed the significant negative impact of Hemiurus appendiculatus on A. alosa and Pronoprymna ventricosa on A. fallax. Because helminth parasites are omnipresent in the shads and decrease their fitness, parasitological data must be included in further investigations and management programs on A. alosa and A. fallax.

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References

  1. Acou AE, Lasne E, Feunteun E (coord.) (2013) Programme de connaissance Natura2000 en mer : les habitats marins des espèces amphihalines. Evaluation de la cohérence du réseau Natura2000 en mer pour la grande alose (Alosa alosa), l’alose feinte (A. fallax sp.), la lamproie marine (Petromyzon marinus) et la lamproie fluviatile (Lampetra fluviatilis). Rapport préliminaire du Muséum National d’Histoire Naturelle, Station marine de Dinard

  2. Alexandrino P, Faria R, Linhares D, Castro F, Le Corre M, Sabatié R, Baglinière JL, Weiss S (2006) Interspecific differentiation and intraspecific substructure in two closely related clupeids with extensive hybridization, Alosa alosa and Alosa fallax. J Fish Biol 69:242–259

  3. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

  4. Anderson TK, Sukhdeo MVK (2010) Abiotic versus biotic hierarchies in the assembly of parasite populations. Parasitology 137:743–754

  5. Anderson RC, Chabaud AG, Willmott S (2009) Keys to the nematode parasites of vertebrates. CABI Head Office, UK

  6. Aprahamian MW (1985) The effect of the migration of Alosa fallax fallax (Lacépède) into fresh water, on branchial and gut parasites. J Fish Biol 27:521–532

  7. Aprahamian MW, Aprahamian CD, Baglinière JL, Sabatié R, Alexandrino P (2003a) Alosa alosa and Alosa fallax spp. Literature review and bibliography. RandD Technical Report W1 014/TR, Bristol, Environment Agency

  8. Aprahamian MW, Baglinière JL, Sabatié MR, Alexandrino P, Thiel R, Aprahamian CD (2003b) Biology, status, and conservation of the anadromous Atlantic twaite shad Alosa fallax fallax. Am Fish Soc Symp 35:103–124

  9. Assis CA, Almeida PR, Moreira F, Costa JL, Costa MJ (1992) Diet of the twaite shad Alosa fallax (Lacépède) (Clupeidae) in the River Tagus Estuary, Portugal. J Fish Biol 41:1049–1050

  10. Baglinière JL, Elie P (2000) Les aloses (Alosa alosa et Alosa fallax spp.): Ecobiologie et variabilité des populations. CEMAGREF-INRA, Paris

  11. Baglinière JL, Sabatié R, Rochard E, Alexandrino P, Aprahamian MW (2003) The allis shad Alosa alosa: biology, ecology, range, and status of populations. Am Fish Soc Symp 35:85–102

  12. Bao M, Mota M, Nachón DJ, Antunes C, Cobo F, Garci ME, Pierce GJ, Pascual S (2015a) 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 114:2143–2154

  13. Bao M, Roura A, Mota M, Nachón DJ, Antunes C, Cobo F, MacKenzie K, Pascual S (2015b) Macroparasites of allis shad (Alosa alosa) and twaite shad (Alosa fallax) of the Western Iberian Peninsula Rivers: ecological, phylogenetic and zoonotic insights. Parasitol Res 114:3721–3739

  14. Barnes C, Sweeting CJ, Jennings S, Barry JT, Polunin NVC (2007) Effect of temperature and ration size on carbon and nitrogen stable isotope trophic fractionation. Funct Ecol 21:356–362

  15. Bolger T, Connolly PL (1989) The selection of suitable indices for the measurement and analysis of food condition. J Fish Biol 34:171–198

  16. Bouchut A, Roger E, Gourbal B, Grunau C, Coustau C, Mitta G (2008) The compatibility polymorphism in invertebrate host/trematodes interactions: research of molecular determinants. Parasite 15:304–309

  17. Bray RA, Gibson DI (1980) The Fellodistomidae (Digenea) of fishes from the NE Atlantic. Bull Br Mus Nat Hist 37:199–293

  18. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

  19. Bychowsky BE (1957) Monogenetic Trematodes, their systematics and phylogeny. (Hargis Jr WJ Editor) Translated by Oustinoff PC, American Institute of Biological Sciences, Washington

  20. Campbell N, Cross MA, Chubb JC, Cunningham CO, Hatfield EMC, Mackenzie K (2007) Spatial and temporal variations in parasite prevalence and infracommunity structure in herring (Clupea harengus L.) caught to the west of the British Isles and in the North and Baltic Seas: implications for fisheries science. J Helminthol 81:137–146

  21. Carney JP, Dick TA (1999) Enteric helminthes of perch (Perca fluviatilis L.) and yellow perch (Perca flavescens Mitchill): stochastic or predictable assemblages? J Parasitol 85:785–795

  22. 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 Ass UK 92:601–604

  23. Chiriac E, Udrescu M (1973) Fauna Republicii Socialiste România. Plathelminthes. Volumul II Fascicula 4 Trematoda. Editura Academiei Republicii Socialiste România

  24. Combes C (1995) Interactions durables. Écologie et évolution du parasitisme. Masson, Paris

  25. Correia MJ, Costa JL, Teixeira C, Almeida PR, Domingos I, Costa MJ (2001) Feeding habits and condition of landlocked population of Allis shad (Alosa alosa) in Portugal. Bull Fr Pêche Piscic 362/362:823–835

  26. Dessier A, Dupuy C, Trancart T, Audras A, Bustamante P, Gérard C (2016) Low diversity of helminth parasites in Sardina pilchardus and Engraulis encrasicolus (Clupeidae) from the Bay of Biscay. Mar Freshw res 67:1583–1588

  27. Dogiel VA, Petrushevski GK, Polyanski YI (1958) Parasitology of fishes. Leningrad University Press, Leningrad. Translated from the Russian by Kabata Z, Oliver and Boyd Ltd, Edinburgh

  28. Doherty D, McCarthy TK (2002) Chapter 10: aspects of the ecology, parasites and future conservation of twaite shad, Alosa fallax, and allis shad, Alosa alosa, in south-eastern Ireland. In: Collares-Pereira MJ, Coelho MM, Cowx IG (eds) Conservation of freshwater fishes: options for the future. Fishing News Books, Blackwell Sci, Oxford

  29. Esch GW, Wetzel E, Zelmer DA, Schotthoeffer AM (1997) Long-term changes in parasite population and community structure: a case history. Am Midl Nat 137:369–387

  30. Fagerholm HP (1991) Systematic implications of male caudal morphology in ascaridoid nematode parasites. Syst Parasitol 19:215–228

  31. Faria R, Weiss S, Alexandrino P (2012) Comparative phylogeography and demographic history of European shads (Alosa alosa and A. fallax) inferred from mitochondrial DNA. BMC Evol Biol 12:194. doi:10.1186/1471-2148-12-194

  32. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks CA

  33. Freyhof J, Kottelat M (2008a) Alosa alosa. The IUCN Red List of Threatened Species 2008: e.T903A13091343

  34. Freyhof J, Kottelat M (2008b) Alosa fallax. The IUCN Red List of Threatened Species 2008: e.T904A13092303

  35. Gérard C, Amilhat E, Trancart T, Faliex E, Virag L, Feunteun E, Acou A (2013) Influence of introduced vs native parasites on the body condition of migrant silver eels. Parasite 20. doi:10.1051/parasite/2013040

  36. Gérard C, Verrez-Bagnis V, Jérôme M, Lasne E (2015) Petromyzon marinus (Petromyzontidae), an unusual host for helminth parasites in Western Europe. Dis Aquat org 113:263–267

  37. Gérard C, Hervé M, Réveillac E, Acou A (2016) Spatial distribution and impact of the gill-parasitic Mazocraes alosae (Herman, 1782) (Monogenea Polyopisthocotylea) on Alosa alosa (Linnaeus, 1758) and Alosa fallax (Lacépède, 1803) (Clupeidae). Hydrobiologia 763:371–379

  38. Gibson DI, Bray RA (1986) The Hemiuridae (Digenea) of fishes from the north-east Atlantic. Bull Br Mus Nat Hist 36:55–146

  39. Golvan YJ (1969) Systématique des Acanthocéphales (Acanthocephala Rudolphi 1801). Mém Mus Natn Hist Nat 57, Paris

  40. Grano-Maldonado MI, Gisbert E, Hirt-Chabbert J, Paladini G, Roque A, Bron JE, Shinn AP (2011) An infection of Gyrodactylus anguillae Ergens, 1960 (Monogenea) associated with the mortality of glass eels (Anguilla anguilla L.) on the north-western Mediterranean Sea board of Spain. Vet Parasitol 180:323–331

  41. Hatcher MJ, Dick JTA, Dunn AM (2012) Diverse effects of parasites in ecosystems: linking interdependent processes. Front Ecol Environ 10:186–194

  42. Hechinger R (2013) A metabolic and body-size scaling framework for parasite within-host abundance, biomass, and energy flux. Am Nat 182:234–248

  43. Hervé M (2016) RVAideMemoire: diverse basic statistical and graphical functions. R package version 0.9–55

  44. Jakob EM, Marshall SD, Uets GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67

  45. Johnson PTJ, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, Orloske SA, Poulin R, Thieltges DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371

  46. Jolly MT, Aprahamian MW, Hawkins SJ, 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 159:675–687

  47. Kabata Z (1964) Clavellisa emarginata (Krøyer, 1873): morphological study of a parasitic copepod. Crustaceana 7:1–10

  48. Kania PW, Taraschewski H, Han YS, Cone DK, Buchmann K (2010) Divergence between Asian, European and Canadian populations of the monogenean Pseudodactylogyrus bini indicated by ribosomal DNA patterns. J Helminthol 84:404–409

  49. Kennedy CR (1981) The occurrence of Eubothrium fragile (Cestoda: Pseudophyllidae) in twaite shad, Alosa fallax (Lacépède) in the River Severn. J Fish Biol 19:171–177

  50. Kennedy CR (1994) The distribution and abundance of the nematode Anguillicola australiensis in eels Anguilla reinhardtii in Queensland, Australia. Folia Parasit 41:279–285

  51. Kennedy CR (2006) Ecology of the Acanthocephala. Cambridge University Press

  52. Kennedy CR (2009) The ecology of parasites of freshwater fishes: the search for patterns. Parasitology 136:1653–1662

  53. 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 110:1147–1157

  54. Klimpel S, Rückert S (2005) Life cycle strategy of Hysterothylacium aduncum to become the most abundant anisakid fish nematode in the North Sea. Parasitol Res 97:141–149

  55. Køie M (1993) Aspects of the life-cycle and morphology of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda, Ascaridoidea, Anisakidae). Can J Zool 71:1289–1296

  56. Kuchta R, Hanzelova 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 52:251–260

  57. Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, Lorda J, Mabada L, Mancini FT, Mora AB, Pickering M, Talhouk N, Torchin ME, Lafferty KD (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–518

  58. Lambden J, Johnson PTJ (2013) Quantifying the biomass of parasites to understand their role in aquatic communities. Ecol Evol 3:2310–2321

  59. Legendre P, Legendre L (2012) Numerical ecology (3rd ed). Elsevier, the Netherlands

  60. Lenth R (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33

  61. Locke SA, McLaughlin JD, Marcogliese DJ (2013) Predicting the similarity of parasite communities in freshwater fishes using the phylogeny, ecology and proximity of hosts. Oikos 122:73–83

  62. MacKenzie K (2002) Parasites as biological tags in population studies of marine organisms: an update. Parasitology 124:S153–S163

  63. Maitland PS, Lyle A (2005) Ecology of Allis Shad Alosa alosa and Twaite Shad Alosa fallax in the Solway Firth, Scotland. Hydrobiologia 534:205–221

  64. Marcogliese DJ (2002) Food webs and the transmission of parasites to marine fish. Parasitology 124:83–99

  65. Marcogliese DJ (2004) Parasites: small players with crucial roles in the ecological theater. EcoHealth 1:151–164

  66. Marcogliese DJ (2005) Parasites of the superorganism: are they indicators of ecosystem health? Int J Parasitol 35:705–716

  67. 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 72:991–1003

  68. Mattiucci S, Nascetti G (2006) Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite 13:99–113

  69. Mattiucci S, Nascetti G (2008) Chapter 2: advances and trends in the molecular systematics of Anisakid nematodes, with implications for their evolutionary ecology and host—parasite co-evolutionary processes. Adv Parasitol 66:47–148

  70. McElroy E, De Buron I (2014) Host performance as a target of manipulation by parasites: a meta-analysis. J Parasitol 100:399–410

  71. Mota M, Antunes C (2012) A preliminary characterisation of the habitat use and feeding of Allis shad (Alosa alosa) juveniles in the Minho River tidal freshwater wetlands. Limnetica 31:165–172

  72. 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 Fisheries 25:395–412

  73. 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 64:233–236

  74. Nadler SA, Hudspeth DS (2000) Phylogeny of the Ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: hypotheses of structural and sequence evolution. J Parasitol 86:380–393

  75. Neff BD, Cargnelli LM (2004) Relationships between condition factors, parasite load and paternity in bluegill sunfish, Lepomis macrochirus. Environ Biol Fish 71:297–304

  76. Nelson PA, Dick TA (2002) Factors shaping the parasite communities of trout-perch, Percopsis omiscomaycus Walbaum (Osteichthyes: Percopsidae), and the importance of scale. Can J Zool 80:1986–1999

  77. 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 the rivers Wye, Usk and Towy, UK. Hydrobiologia 614:209–218

  78. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MH Wagner H (2016) Vegan: Community ecology package. R package version 2.3–5

  79. Pante E, Simon-Bouhet B (2013) Marmap: a package for importing, plotting and analyzing bathymetric and topographic data in R. PLoS One 8:e73051

  80. Pasternak AF, Mikheev VN, Valtonen ET (2000) Life history characteristics of Argulus foliaceus L. (Crustacea: Branchiura) populations in Central Finland. Ann Zool Fennici 37:25–35

  81. Poulin R (1998) Evolutionary ecology of parasites—from individuals to communities. Chapman and Hall

  82. Poulin R (2010) Decay of similarity with host phylogenetic distance in parasite faunas. Parasitology 137:733–741

  83. Price EW (1961) North American monogenetic trematodes. IX. The families Mazocraeidae and Plectanocotylidae. Proc Biol Soc Wash 74:453–458

  84. Price PW, Westoby M, Rice B, Atsatt PR, Fritz RS, Thompson JN, Mobley K (1986) Parasite mediation in ecological interactions. Annu Rev Ecol Syst 17:487–505

  85. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna URL http://www.R-project.org /

  86. Råberg L (2014) How to live with the enemy: understanding tolerance to parasites. PLoS Biol 12:e1001989. doi:10.1371/journal.pbio.1001989

  87. Robar N, Burness G, Murray DL (2010) Trophics, trophics and taxonomy: the determinants of parasite-associated host mortality. Oikos 119:1273–1280

  88. Rushton-Mellor SK, Boxshall GA (1994) The developmental sequence of Argulus foliaceus (Crustacea: Branchiura). J Nat Hist 28:763–785

  89. Sekalovic S, de Ruiter PC, Heesterbeek H (2014) Infectious disease agents mediate interaction in food webs and ecosystems. Proc R Soc B 281:20132709

  90. Shields BA, Bird P, Liss WJ, Groves KL, Olson R, Rossignol PA (2002) The nematode Anisakis simplex in American shad (Alosa sapidissima) in two Oregon Rivers. J Parasitol 88:1033–1035

  91. 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 41:24–32

  92. Smit NJ, Bruce NL, Hadfield KA (2014) Global diversity of fish parasitic isopod crustaceans of the family Cymothoidae. Int J Parasitol Parasites Wildl 3:188–197

  93. 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. Bul Bull Fr Pêche Piscic 362/363:803–821

  94. 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. Bul Bull Fr Pêche Piscic 362/363:837–852

  95. Taverny C, Elie P (2010) Les lamproies en Europe de l’Ouest – Ecophases, espèces et habitats. Editions Quæ, Versailles

  96. Thomas F, Guégan JF, Renaud F (2007) Ếcologie et évolution des systèmes parasités. De Boeck and Larcier, Bruxelles

  97. Trilles JP (1975) Les Cymothoidae (Isopoda, Flabellifera) des collections du Muséum national d’Histoire naturelle de Paris. II. Les Anilocridae Schioedte et Meinert, 1881. Genres Anilocra Leach, 1818, et Nerocila Leach, 1818. Bull Mus natn Hist nat, 3ème série, 290 (zool 200): 303–346

  98. Valentini A, Mattiucci S, Bondanelli P, Webb SC, Mignucci-Giannone AA, Colom-Llavina MM, Nascetti G (2006) Genetic relationships among Anisakis species (Nematoda : Anisakidae) inferred from mitochondrial Cox2 sequences, and comparison with allozyme data. J Parasitol 92:156–166

  99. Zelmer DA (2014) Size, time, and asynchrony matter: the species-area relationship for parasites of freshwater fishes. J Parasitol 100:561–568

  100. Zhu X, Gasser RB, Podolska M, Chilton NB (1998) Characterisation of anisakid nematodes with zoonotic potential by nuclear ribosomal DNA sequences. Int J Parasitol 28:1911–1921

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Acknowledgments

This study was funded by the French Ministry of Ecology and Sustainable Development (‘Programme de connaissances Natura2000 amphihalins en mer’). Authors warmly thank the numerous fishermen and local angling federation for providing the fish. We gratefully acknowledge Valérie Briand (UMR ECOBIO 6553) for her bibliographical support and the colleagues (E. Chavance, C. Oudard, E. Sola, and T. Lavigne) who collaborated to the study.

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Correspondence to Claudia Gérard.

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Gérard, C., Hervé, M., Gay, M. et al. Metazoan parasite communities in Alosa alosa (Linnaeus, 1758) and Alosa fallax (Lacépède, 1803) (Clupeidae) from North-East Atlantic coastal waters and connected rivers. Parasitol Res 116, 2211–2230 (2017). https://doi.org/10.1007/s00436-017-5525-8

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Keywords

  • Alosa spp.
  • Metazoan parasites
  • Host developmental stage
  • Marine vs freshwater phases
  • Fitness loss