Parasitology Research

, Volume 116, Issue 6, pp 1729–1743 | Cite as

Pathogenic endoparasites of the spotted seatrout, Cynoscion nebulosus: patterns of infection in estuaries of South Carolina, USA

  • Stephen A . Arnott
  • Iva Dyková
  • William A. Roumillat
  • Isaure de Buron
Original Paper


Six types of pathogenic endoparasites in an economically important fish, spotted seatrout Cynoscion nebulosus, were studied in order to test whether prevalence of infection and assemblage richness varied with season, host sex, host size, or host age. Fish were collected from South Carolina estuaries, USA, over 12 months (n = 216; total lengths 15–663 mm). They were screened histologically for presence of Henneguya cynoscioni (Myxozoa) and Cardicola spp. (Digenea) in the heart, Kudoa inornata (Myxozoa) in the skeletal muscle, Sinuolinea dimorpha (Myxozoa) in the urinary system, Ichthyophonus sp. (Mesomycetozoea) in the kidney, and an unidentified microsporidian in the liver. Prevalence of infection was 29.8, 38.6, 47.2, 41.2, 13.6, and 2.8%, respectively. All factors had significant, but varying effects on the parasites. Parasite infections were more prevalent in winter than other seasons for Cardicola spp. and H. cynoscioni, more prevalent in winter and spring for Ichthyophonus sp., and more prevalent in male fish than female fish for K. inornata, S. dimorpha, and Ichthyophonus. Prevalence of infection by the three myxosporeans and Cardicola spp. increased with fish length, whereas prevalence of Ichthyophonus increased with length among young fish, but decreased with length among older fish. None of the factors affected the liver microsporidian, although statistical power was low due to its rareness. Assemblage richness varied between 0 and 5, was greater during winter and in male fish, and increased with fish length and fish age. Our results demonstrate that spotted seatrout are commonly co-infected by multiple pathogenic endoparasites, suggesting these parasites likely play an import role in controlling fish population numbers.


Sciaenidae Myxozoa Aporocotylidae Ichthyosporea Histology Richness 


  1. Abdel-Baki A-AS, Sakran T, Zayed E, Al-Quraishy S (2014) Seasonal fluctuation and histopathology of Henneguya ghaffari (Myxozoa: Myxosporea) infection in the gills of the Nile perch, Lates niloticus, in the River Nile: a new locality record. Parasitol Res 113:1459–1463. doi: 10.1007/s00436-014-3786-z
  2. Aiken HA, Hayward CJ, Nowak BF (2015) Factors affecting abundance and prevalence of blood fluke, Cardicola forsteri, infection in commercially ranched southern bluefin tuna, Thunnus maccoyii, in Australia. Vet Parasitol 210:106–113PubMedCrossRefGoogle Scholar
  3. Alama-Bermejo G, Šima R, Raga JA, Holzer AS (2013) Understanding myxozoan infection dynamics in the sea: seasonality and transmission of Ceratomyxa puntazzi. Int J Parasitol 43:771–780PubMedCrossRefGoogle Scholar
  4. Álvarez-Pellitero P, Sitjà-Bobadilla A (1993) Population dynamics of Ceratomyxa spp. (Protozoa: Myxosporea) infection in wild and cultured sea bass, Dicentrarchus labrax (L.) from the Spanish Mediterranean area. J Fish Biol 42:889–901CrossRefGoogle Scholar
  5. Anweiler KV, Arnott SA, Denson MR (2014) Low-temperature tolerance of juvenile spotted seatrout in South Carolina. Trans Am Fish Soc 143:999–1010Google Scholar
  6. Arnott SA, Roumillat WA, Archambault JA, Wenner CA, Gerhard JI, Darden TL, Denson MR (2010) Spatial synchrony and temporal dynamics of juvenile red drum (Sciaenops ocellatus) populations in South Carolina, USA. Mar Ecol Prog Ser 415:221–236CrossRefGoogle Scholar
  7. Barber I, Huntingford FA (1995) The effect of Schistocephalus solidus (Cestoda: Pseudophyllidea) on the foraging and shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus. Behaviour 132:1223–1240CrossRefGoogle Scholar
  8. Barber I, Poulin R (2002) Interactions between fish, parasites and disease. In: Handbook of fish biology and fisheries; Volume 1: fish biology. Blackwell Science Ltd., OxfordGoogle Scholar
  9. Barber I, Berkhout BW, Ismail Z (2016) Thermal change and the dynamics of multi-host parasite life cycles in aquatic ecosystems. Int Comp Biol 56:561–572. doi: 10.1093/icb/icw025 CrossRefGoogle Scholar
  10. Barber I, Hoare D, Krause J (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fish 10:131–165CrossRefGoogle Scholar
  11. Bartholomew JL (1998) Host resistance to infection by the myxosporean parasite Ceratomyxa shasta: a review. J Aquat Anim Health 10:12–20CrossRefGoogle Scholar
  12. Belem AMG, Pote LM (2001) Portals of entry and systemic localization of proliferative gill disease organisms in channel catfish Ictalurus punctatus. Dis Aquat Org 48:37–42PubMedCrossRefGoogle Scholar
  13. Benesh DP, Kalbe M (2016) Experimental parasite community ecology: intraspecific variation in a large tapeworm affects community assembly. J Anim Ecol 85:1004–1013PubMedCrossRefGoogle Scholar
  14. Binuramesh C, Prabakaran M, Steinhagen D, Michael RD (2006) Effect of sex ratio on the immune system of Oreochromis mossambicus (Peters). Brain Behav Immun 20:300–308PubMedCrossRefGoogle Scholar
  15. Bjork SJ, Bartholomew JL (2009) Effects of Ceratomyxa shasta dose on a susceptible strain of rainbow trout and comparatively resistant Chinook and coho salmon. Dis Aquat Org 86:29–37PubMedCrossRefGoogle Scholar
  16. Bjork SJ, Bartholomew JL (2010) Invasion of Ceratomyxa shasta (Myxozoa) and comparison of migration to the intestine between susceptible and resistant fish hosts. Int J Parasitol 40:1087–1095PubMedCrossRefGoogle Scholar
  17. Blaylock RG, Overstreet RM (2003) Parasites and diseases of spotted seatrout. In: Bortone SA, Boca Raton FL (eds) Biology of the spotted seatrout. CRC Press, New York U.S.A., pp 197–226Google Scholar
  18. Bortone SA (2003) In: Bortone SA, Boca Raton FL (eds) Biology of the spotted seatrout. CRC Press, New York U.S.A.Google Scholar
  19. Buchmann K, Lindenstrøm T (2002) Interactions between monogenean parasites and their fish hosts. Int J Parasitol 32:309–319PubMedCrossRefGoogle Scholar
  20. Bullard SA, Overstreet RM (2002) Potential pathological effects of blood flukes (Digenea: Sanguinicolidae) on pen-reared marine fishes. Proc. 53rd Gulf and Carib. Fish. Inst., Fort Pierce, Florida: 10–25Google Scholar
  21. Callihan JL, Cowan JH, Harbison MD (2013) Sex differences in residency of adult spotted seatrout in a Louisiana estuary. Mar Coast Fish 5:79–92CrossRefGoogle Scholar
  22. Cirtwill AR, Stouffer DB, Poulin R, Lagrue C (2016) Are parasite richness and abundance linked to prey species richness and individual feeding preferences in fish hosts? Parasitology 143:75–86PubMedCrossRefGoogle Scholar
  23. Christe P, Arlettaz R, Vogel P (2000) Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecol Lett 3:207–212CrossRefGoogle Scholar
  24. Constenla M, Montero FE, Padrós F, Cartes JE, Papiol V, Carrassón M (2015) Annual variation of parasite communities of deep-sea macrourid fishes from the western Mediterranean Sea and their relationship with fish diet and histopathological alterations. Deep Sea Res Part I 104:106–121CrossRefGoogle Scholar
  25. Cox FEG (2001) Concomitant infections, parasites and immune responses. Parasitology 122:S23–S38PubMedCrossRefGoogle Scholar
  26. Crespo S, Grau A, Padrós F (1992) Sanguinicoliasis in the cultured amberjack Seriola dumerili Risso, from the Spanish Mediterranean area. Bull Eur Assoc Fish Pathol 12:157–159Google Scholar
  27. Cribb TH, Adlard RD, Hayward CJ, Bott N, Ellis D, Evans D, Nowak B (2011) The life cycle of Cardicola forsteri (Trematoda: Aporocotylidae), a pathogen of ranched southern bluefin tuna, Thunnus maccoyi. Int J Parasitol 41:861–870PubMedCrossRefGoogle Scholar
  28. Dantzer R, Kelley KW (2007) Twenty years of research on cytokine-induced sickness behavior. Brain Behav Immun 21:153–160PubMedCrossRefGoogle Scholar
  29. Dennis MM, Landos M, D’Antignana T (2011) Case–control study of epidemic mortality and Cardicola forsteri–associated disease in farmed southern bluefin tuna (Thunnus maccoyii) of south Australia. Vet Pathol 48:846–855PubMedCrossRefGoogle Scholar
  30. Dittmar J, Janssen H, Kuske A, Kurtz J, Scharsack JP (2014) Heat and immunity: an experimental heat wave alters immune functions in three-spined sticklebacks (Gasterosteus aculeatus). J Anim Ecol 83:744–757PubMedCrossRefGoogle Scholar
  31. Diamant A (1997) Fish-to-fish transmission of a marine myxosporean. Dis Aquat Org 30:99–105CrossRefGoogle Scholar
  32. Diamant A, Ram S, Paperna I (2006) Experimental transmission of Enteromyxum leei to freshwater fish. Dis Aquat Org 72:171–178PubMedCrossRefGoogle Scholar
  33. Dyková I, de Buron I, Fiala I, Roumillat WA (2009) Kudoa inornata sp. n. (Myxosporea: Multivalvulida) from the skeletal muscles of Cynoscion nebulosus (Teleostei: Sciaenidae). Folia Parasitol 56:91–98PubMedCrossRefGoogle Scholar
  34. Dyková I, de Buron I, Roumillat WA, Fiala I (2011) Henneguya cynoscioni sp. n. (Myxosporea: Bivalvulida), an agent of severe cardiac lesions in the spotted seatrout, Cynoscion nebulosus (Teleostei: Sciaenidae). Folia Parasitol 58:169–177PubMedCrossRefGoogle Scholar
  35. Dyková I, Kodádková A, de Buron I, Fiala I, Roumillat WA (2013) Sinuolinea infections in the urinary system of Cynoscion species (Sciaenidae) and phylogenetic position of the type species of Sinuolinea Davis, 1917 (Myxozoa: Myxosporea). Int J Parasitol Parasites Wildl 2:10–17. doi: 10.1016/j.ijppaw.2012.11.004 PubMedCrossRefGoogle Scholar
  36. El-Matbouli M, Hoffmann RW (1991) Effects of freezing, aging, and passage through the alimentary canal of predatory animals on the viability of Myxobolus cerebralis spores. J Aquat Anim Health 3:260–262CrossRefGoogle Scholar
  37. Ezenwa VO, Jolles AE (2011) From host immunity to pathogen invasion: the effects of helminth coinfection on the dynamics of microparasites. Int Comp Biol 51:540–551. doi: 10.1093/icb/icr058 CrossRefGoogle Scholar
  38. Fenton A, Brockhurst MA (2008) The role of specialist parasites in structuring host communities. Ecol Res 23:795–804CrossRefGoogle Scholar
  39. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622CrossRefGoogle Scholar
  40. Foo YZ, Nakagawa S, Rhodes G, Simmons LW (2016) The effects of sex hormones on immune function: a meta-analysis. Biol Rev. doi: 10.1111/brv.12243 PubMedGoogle Scholar
  41. Garner MM, Atkinson SD, Hallett SL, Bartholomew JL, Nordhausen RW, Reed H, Adams L, Whitaker B (2008) Renal myxozoanosis in weedy sea dragons, Phyllopteryx taeniolatus (Lacepede), caused by Sinuolinea phyllopteryxa n. sp. J Fish Dis 31:27–35PubMedCrossRefGoogle Scholar
  42. George-Nascimento M, Oliva ME (2015) Fish population studies using parasites from the southeastern Pacific Ocean: considering host population changes and species body size as sources of variability of parasite communities. Parasitology 142:25–35PubMedCrossRefGoogle Scholar
  43. Gómez D, Bartholomew J, Sunyer JO (2014) Biology and mucosal immunity to myxozoans. Dev Comp Immunol 43:243–256PubMedCrossRefGoogle Scholar
  44. Goodman BA, Johnson PTJ (2011) Disease and the extended phenotype: parasites control host performance and survival through induced changes in body plan. PLoS One 6:e20193PubMedPubMedCentralCrossRefGoogle Scholar
  45. Godwin SC, Dill LM, Reynolds JD, Krkosek M (2015) Sea lice, sockeye salmon, and foraging competition: lousy fish are lousy competitors. Can J Fish Aquat Sci 72:1113–1120. doi: 10.1139/cjfas-2014-0284 CrossRefGoogle Scholar
  46. Gozlan RE, Marshall WL, Lilje O, Jessop CN, Gleason FH, Andreou D (2014) Current ecological understanding of fungal-like pathogens of fish: what lies beneath? Front Microbiol. doi: 10.3389/fmicb.2014.00062 PubMedPubMedCentralGoogle Scholar
  47. Granath WO Jr, Vincent ER (2010) Epizootiology of Myxobolus cerebralis, the causative agent of salmonid whirling disease in the rock creek drainage of west-central Montana: 2004–2008. J Parasitol 96:252–257. doi: 10.1645/GE-2285.1 PubMedCrossRefGoogle Scholar
  48. Gregg JL, Powers RL, Purcell MK, Friedman CS, Hershberger PK (2016) Ichthyophonus parasite phylogeny based on ITS rDNA structure prediction and alignment identifies six clades, with a single dominant marine type. Dis Aquat Org 120:125–141. doi: 10.3354/dao03017 PubMedCrossRefGoogle Scholar
  49. Gregg JL, Grady CA, Friedman CS, Hershberger PK (2012) Inability to demonstrate fish-to-fish transmission of Ichthyophonus from laboratory infected Pacific herring Clupea pallasii to naive conspecifics. Dis Aquat Org 99:139–144PubMedCrossRefGoogle Scholar
  50. Griffin MJ, Pote LM, Camus AC, Mauel MJ, Greenway TE, Wise DJ (2009) Application of a real-time PCR assay for the detection of Henneguya ictaluri in commercial channel catfish ponds. Dis Aquat Org 83:223–233CrossRefGoogle Scholar
  51. Gustafson PV, Rucker RR (1956) Studies on an Ichthyosporidium infection in fish: transmission and host specificity. US Department of the Interior, Fish and Wildlife Service, Special Sci Rep Fish 166Google Scholar
  52. Haas W (1992) Physiological analysis of cercarial behavior. J Parasitol 78:243–255PubMedCrossRefGoogle Scholar
  53. Hallett SL, Ray RA, Hurst CN, Holt RA, Buckles GR, Atkinson SD, Bartholomew JL (2012) Density of the waterborne parasite Ceratomyxa shasta and its biological effects on salmon. Appl Environ Microbiol 78:3724–3731PubMedPubMedCentralCrossRefGoogle Scholar
  54. Haaparanta A, Valtonen ET, Hoffmann RW (1994) Pathogenicity and seasonal occurrence of Henneguya creplini (Protozoa, Myxosporea) on the gills of perch Perca fluviatilis in central Finland. Dis Aquat Org 20:15–22CrossRefGoogle Scholar
  55. Hamoutene D, Mitchell JS, Murray HM, Eaves A, Marshall K, Belley R, George S (2016) The effect of light regimen on settlement patterns of sea lice, Lepeophtheirus salmonis, on Atlantic salmon, Salmo salar, post-smolts while taking into account fish size and fin erosion in a static tank system. Aquaculture 465:1–6CrossRefGoogle Scholar
  56. Hatcher MJ, Dick JTA, Dunn AM (2014) Parasites that change predator or prey behaviour can have keystone effects on community composition. Biol Lett 10:20130879. doi: 10.1098/rsbl.2013.0879 PubMedPubMedCentralCrossRefGoogle Scholar
  57. Hawlena H, Abramsky Z, Krasnov BR (2005) Age-biased parasitism and density-dependent distribution of fleas (Siphonaptera) on a desert rodent. Oecologia 146:200–208Google Scholar
  58. Hershberger PK, Stick K, Bui B, Carroll C, Fall B, Mork C, Perry JA, Sweeney E, Wittouck J, Kocan RM (2002) Incidence of Ichthyophonus hoferi in Puget Sound fishes and its increase with age of Pacific herring. J Aquat Anim Health 14:50–56CrossRefGoogle Scholar
  59. Hershberger PK, Hart LM, MacKenzie AH, Yanney ML, Conway CM, Elliott DG (2015) Infecting Pacific herring with Ichthyophonus sp. in the laboratory. J Aquat Anim Health 27:217–221. doi: 10.1080/08997659.2015.1095809 PubMedCrossRefGoogle Scholar
  60. Holzer AS, Sommerville C, Wootten R (2003) Tracing the route of Sphaerospora truttae from the entry locus to the target organ of the host, Salmo salar L., using an optimized and specific in situ hybridization technique. J Fish Dis 26:647–655PubMedCrossRefGoogle Scholar
  61. Jones SRM, Dawe SC (2002) Ichthyophonus hoferi Plehn & Mulsow in British Columbia stocks of Pacific herring, Clupea pallasi Valenciennes, and its infectivity to Chinook salmon, Oncorhynchus tshawytscha (Walbaum). J Fish Dis 25:415–421CrossRefGoogle Scholar
  62. Jones S, Kim E, Bennett W (2008) Early development of resistance to the salmon louse, Lepeophtheirus salmonis (Krøyer), in juvenile pink salmon, Oncorhynchus gorbuscha (Walbaum). J Fish Dis 31:591–600PubMedCrossRefGoogle Scholar
  63. Jones SRM, Cho S, Nguyen J, Mahony A (2016) Acquired resistance to Kudoa thyrsites in Atlantic salmon Salmo salar following recovery from a primary infection with the parasite. Aquaculture 451:457–462CrossRefGoogle Scholar
  64. Kallert DM, Ponader S, Eszterbauer E, El-Matbouli M, Haas W (2007) Myxozoan transmission via actinospores: new insights into mechanisms and adaptations for host invasion. Parasitology 134:1741–1750PubMedCrossRefGoogle Scholar
  65. Kamiya T, O’Dwyer K, Nakagawa S, Poulin R (2014) What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biol Rev 89:123–134. doi: 10.1111/brv.12046 PubMedCrossRefGoogle Scholar
  66. Katahira H, Mizuno K, Nagasawa K (2011) Host size and habitat-dependent intensity of Heuconema longissimus (Nematoda: Physalopteridae) in the Japanese eel (Anguilla japonica). J Parasitol 97:994–998PubMedCrossRefGoogle Scholar
  67. Kocan RM, Hershberger PK, Mehl T, Elder N, Wildermuth BD, Stick K (1999) Pathogenicity of Ichthyophonus hoferi for laboratory-reared Pacific herring Clupea pallasi and its early appearance in wild Puget Sound herring. Dis Aquat Org 35:23–29PubMedCrossRefGoogle Scholar
  68. Kocan RM, Hershberger PK, Winton JR (2004) Ichthyophoniasis: an emerging disease of Chinook salmon in the Yukon River. J Aquat Anim Health 16:58–72CrossRefGoogle Scholar
  69. Kocan RM, LaPatra S, Gregg J, Winton JR, Hershberger PK (2006) Ichthyophonus-induced cardiac damage: a mechanism for reduced swimming stamina in salmonids. J Fish Dis 29:521–527PubMedCrossRefGoogle Scholar
  70. Koie M (1982) The redia, cercaria and early stages of Aporocotyle simplex Odhner, 1900 (Sanguinicolidae). A digenetic trematode which has a polychaete annelid as the only intermediate host. Ophelia 21:115–145CrossRefGoogle Scholar
  71. Koprivnikar J, Lim D, Fu C, Brack SH (2010) Effects of temperature, salinity, and pH on the survival and activity of marine cercariae. Parasitol Res 106:1167–1177PubMedCrossRefGoogle Scholar
  72. Kupschus S (2004) A temperature-dependent reproductive model for spotted seatrout (Cynoscion nebulosus) explaining spatio-temporal variations in reproduction and young-of-the-year recruitment in Florida estuaries. ICES J Mar Sci 61:3–11CrossRefGoogle Scholar
  73. Kurtz J, Kalbe M, Langefors A, Mayer I, Milinski M, Hasselquist D (2007) An experimental test of the immunocompetence handicap hypothesis in a teleost fish: 11-ketotestosterone suppresses innate immunity in three-spined sticklebacks. Am Nat 170:509–519PubMedGoogle Scholar
  74. Lafferty KD (2009) Calling for an ecological approach to studying climate change and infectious diseases. Ecology 90:932–933. doi: 10.1890/08-1767.1 PubMedCrossRefGoogle Scholar
  75. Layland LE, Specht S (2014) Helpful or a hindrance: co-infections with helminths during malaria. In: How helminths alter immunity to infection. Advances in Experimental Medicine and Biology (Eds W. Horsnell) 828:99–129. doi:  10.1007/978-1-4939-1489-0_5
  76. Lester RJG, McVinish T (2016) Does moving up a food chain increase aggregation in parasites? J R Soc Interface 13:20160102. doi: 10.1098/rsif.2016.0102 PubMedPubMedCentralCrossRefGoogle Scholar
  77. Leung TLF, Poulin R (2008) Size-dependent pattern of metacercariae accumulation in Macomona liliana: the threshold for infection in a dead-end host. Parasitol Res 104:177–180. doi: 10.1007/s00436-008-1166-2 PubMedCrossRefGoogle Scholar
  78. Levsen A, Paoletti M, Cipriani P, Nascetti G, Mattiucci S (2016) Species composition and infection dynamics of ascaridoid nematodes in Barents Sea capelin (Mallotus villosus) reflecting trophic position of fish host. Parasitol Res 115:4281–4291. doi: 10.1007/s00436-016-5209-9
  79. Lima LB, Bellay S, Giacomini HC, Isaac A, Lima DP Jr (2016) Influence of host diet and phylogeny on parasite sharing by fish in a diverse tropical floodplain. Parasitology 143:343–349. doi: 10.1017/S003118201500164X PubMedCrossRefGoogle Scholar
  80. Llanso RJ, Bell SS, Vose FE (1998) Food habits of red drum and spotted seatrout in a restored mangrove impoundment. Estuaries 21:294–306CrossRefGoogle Scholar
  81. Louhi K-R, Sundberg L-R, Jokela J, Karvonen A (2015) Interactions among bacterial strains and fluke genotypes shape virulence of co-infection. Proc R Soc B 282:2015–2097. doi: 10.1098/rspb.2015.2097 CrossRefGoogle Scholar
  82. Lutterschmidt WI, Schaefer JF, Fiorillo RA (2007) The ecological significance of helminth endoparasites on the physiological performance of two sympatric fishes. Comp Parasitol 74:194–203. doi: 10.1654/4248.1 CrossRefGoogle Scholar
  83. McElroy EJ, George AB, de Buron I (2015) The muscle dwelling myxozoan, Kudoa inornata, enhances swimming performance in the spotted seatrout, Cynoscion nebulosus. Parasitol Res. doi: 10.1007/s00436-015-4441-z PubMedGoogle Scholar
  84. McMichael RH Jr, Peters KM (1989) Early life history of spotted seatrout, Cynoscion nebulosus (Pisces: Sciaenidae), in Tampa Bay, Florida. Estuaries 12:98–110CrossRefGoogle Scholar
  85. McNab V, Barber I (2012) Some (worms) like it hot: fish parasites grow faster in warmer water, and alter host thermal preferences. Glob Change Biol 18:1540–1548CrossRefGoogle Scholar
  86. McVay MJ, Bakenhaster MD, Bullard SA (2011) Cardicola laruei Short, 1953 (Digenea: Aporocotylidae) from heart of seatrouts, Cynoscion spp. (Perciformes: Sciaenidae) in the Gulf of Mexico and Atlantic Ocean: taxonomic redescription, first observations of egg and miracidium, and comments on geographic distribution and host specificity. Comp Parasitol 78:291–305CrossRefGoogle Scholar
  87. Miwa S, Kamaishi T, Hirae T, Murase T, Nishioka T (2011) Encephalomyelitis associated with microsporidian infection in farmed greater amberjack, Seriola dumerili (Risso). J Fish Dis 34:901–910PubMedCrossRefGoogle Scholar
  88. Moran JDW, Kent ML (1999) Kudoa thyrsites (Myxozoa: Myxosporea) infections in pen-reared Atlantic salmon in the northeast Pacific Ocean with a survey of potential nonsalmonid reservoir hosts. J Aquat Anim Health 11:101–109CrossRefGoogle Scholar
  89. Moran JDW, Margolis L, Webster JM, Kent ML (1999) Development of Kudoa thyrsites (Myxozoa: Myxosporea) in netpen-reared Atlantic salmon determined by light microscopy and a polymerase chain reaction test. Dis Aquat Org 37:185–193PubMedCrossRefGoogle Scholar
  90. Morand S, Cribb TH, Kulbicki M, Rigby MC, Chauvet C, Dufour V, Faliex E, Galzin R, Lo CM, Lo-Ya A, Pichelin S, Sasal P (2000) Endoparasite species richness of New Caledonian butterfly fishes: host density and diet matter. Parasitology 121:65–73PubMedCrossRefGoogle Scholar
  91. Moravec F, de Buron I, Roumillat WA (2006) Two new species of Philometra (Nematoda: Philometridae) parasitic in the perciform fish Cynoscion nebulosus (Sciaenidae) in the estuaries of South Carolina, USA. Folia Parasitol 53:63–70PubMedCrossRefGoogle Scholar
  92. Morris DJ, Adams A, Richards RH (2000) In situ hybridization identifies the gill as a portal of entry of PKX (phylum Myxozoa) the causative agent of proliferative kidney disease in salmonids. Parasitol Res 86:950–956PubMedCrossRefGoogle Scholar
  93. Ogawa K, Egusa S (1986) Two new species of Paradeontacylix McIntosh, 1934 (Trematoda: Sanguinicolidae) from the vascular system of a cultured marine fish, Seriola purpurascens. Fish Pathol 21:15–19CrossRefGoogle Scholar
  94. Ogawa K, Fukudome M (1994) Mass mortality caused by blood fluke (Paradeontacylix) among amberjack (Seriola dumerili) imported to Japan. Fish Pathol 29:265–269CrossRefGoogle Scholar
  95. Ogawa K, Nagano T, Akai N, Sugita A, Hall KA (2007) Blood fluke infection of cultured tiger puffer Takifugu rubripes imported from China to Japan. Fish Pathol 42:91–99CrossRefGoogle Scholar
  96. Padros F, Zarza C, Crespo S (2001) Histopathology of cultured sea bream Sparus aurata infected with sanguinicolid trematodes. Dis Aquat Org 44:47–52PubMedCrossRefGoogle Scholar
  97. Palenzuela O, Sitjà-Bobadilla A, Álvarez-Pellitero P (1997) Ceratomyxa sparusaurati (Protozoa: Myxosporea) infections in cultured gilthead sea bream Sparus aurata (Pisces: Teleostei) from Spain: aspects of the host-parasite relationship. Parasitol Res 83:539–548PubMedCrossRefGoogle Scholar
  98. Palenzuela O, Alvarez-Pellitero P, Sitjá-Bobadilla A (1999) Glomerular disease associated with Polysporoplasma sparis (Myxozoa) infections in cultured gilthead sea bream, Sparus aurata L. (Pisces: Teleostei). Parasitology 118:245–256PubMedCrossRefGoogle Scholar
  99. Pasternak AF, Huntingford FA, Crompton DWT (1995) Changes in metabolism and behaviour of the freshwater copepod Cyclops strenuus abyssorum infected with Diphyllobothrium spp. Parasitology 110:395–399PubMedCrossRefGoogle Scholar
  100. Patterson JEH, Ruckstuhl KE (2013) Parasite infection and host group size: a meta-analytical review. Parasitology 140:803–813PubMedPubMedCentralCrossRefGoogle Scholar
  101. Pedersen AB, Fenton A (2006) Emphasizing the ecology in parasite community ecology. Trends Ecol Evol 22:133–139PubMedCrossRefGoogle Scholar
  102. Perry JA, Kocan RM, Winton JR, Hershberger PK (2004) High doses of corticosteroid suppress resistance to Ichthyophonus in starry flounder. J Aquat Anim Health 16:45–49CrossRefGoogle Scholar
  103. Pickering AD, Pottinger TG (1989) Stress responses and disease resistance in salmonid fish: effects of chronic elevation of plasma cortisol. Fish Physiol Biochem 7:253–258. doi: 10.1007/BF00004714
  104. Postawa T, Nagy Z (2016) Variation of parasitism patterns in bats during hibernation: the effect of host species, resources, health status, and hibernation period. Parasitol Res 115:3767–3778PubMedPubMedCentralCrossRefGoogle Scholar
  105. Poulin R (2000) Variation in the intraspecific relationship between fish and length and intensity of parasitic infection: biological and statistical causes. J Fish Biol 56:123–137CrossRefGoogle Scholar
  106. Rahkonen R, Koski P (1998) Occurrence of cestode larvae in brown trout after stocking in a large regulated lake in northern Finland. Dis Aquat Org 31:55–63CrossRefGoogle Scholar
  107. Ray RA, Holt RA, Bartholomew JL (2012) Relationship between temperature and Ceratomyxa shasta-induced mortality in Klamath river salmonids. J Parasitol 98:520–526PubMedCrossRefGoogle Scholar
  108. Redondo MJ, Palenzuela O, Riaza A, Macias A, Álvaez-Pellitero P (2002) Experimental transmission of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus. J Parasitol 88:482–488PubMedCrossRefGoogle Scholar
  109. Rohde K (1993) The ecology of marine parasites. CAB International, Wallingford, 298 ppGoogle Scholar
  110. Roumillat WA, Brouwer MC (2004) Reproductive dynamics of female spotted seatrout (Cynoscion nebulosus) in South Carolina. Fish Bull 102:473–487Google Scholar
  111. Sato T, Watanabe K, Tokuchi N, Kamauchi H, Harada Y, Lafferty KD (2011) A nematomorph parasite explains variation in terrestrial subsidies to trout streams in Japan Oikos 120:1595–1599. doi:  10.1111/j.1600-0706.2011.19121.x
  112. Scharf FS, Juanes F, Rountree RA (2000) Predator size-prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic-niche breadth. Mar Ecol Prog Ser 208:229–248. doi: 10.3354/meps208229
  113. Scharsack JP, Franke F, Erin NI, Kuske A, Büscher J, Stolz H, Samonte IE, Kurtz J, Kalbe M (2016) Effects of environmental variation on host–parasite interaction in three-spined sticklebacks (Gasterosteus aculeatus). Zoology 119:375–383PubMedCrossRefGoogle Scholar
  114. Schmidt-Posthaus H, Wahli T (2015) Host and environmental influences on development of disease. In: Okamura B, Bartholomew J, Gruhl A (eds) Myxozoan evolution, ecology and development. Springer International Publishing, Cham, pp 281–293. doi: 10.1007/978-3-319-14753-6
  115. Schmidt-Posthaus H, Bettge K, Forster U, Segner H, Wahli T (2012) Kidney pathology and parasite intensity in rainbow trout Oncorhynchus mykiss surviving proliferative kidney disease: time course and influence of temperature. Dis Aquat Org 97:207–218. doi: 10.3354/dao02417 PubMedCrossRefGoogle Scholar
  116. Shirakashi S, Ogawa K (2016) Blood fluke infections in marine cultured fish. Fish Pathol 51:92–98CrossRefGoogle Scholar
  117. Shirakashi S, Tani K, Ishimaru K, Shin SP, Honryo T, Uchida H, Ogawa K (2016) Discovery of intermediate hosts for two species of blood flukes Cardicola orientalis and Cardicola forsteri (Trematoda: Aporocotylidae) infecting Pacific bluefin tuna in Japan. Parasitol Int 65:128–136. doi: 10.1016/j.parint.2015.11.003 PubMedCrossRefGoogle Scholar
  118. Short RB (1953) A new blood fluke, Cardicola laruei n. g., n. sp., (Aporocotylidae) from marine fishes. J Parasitol 39:304–309PubMedCrossRefGoogle Scholar
  119. Silveira TS, Calegaro-Marques C (2016) Helminth parasite diversity discloses age and sex differences in the foraging behaviour of southern lapwings (Vanellus chilensis). Austral Ecol 41:549–558. doi: 10.1111/aec.12344 CrossRefGoogle Scholar
  120. Šimková A, Lafond T, Ondračková M, Jurajda P, Ottová E, Morand S (2008) Parasitism, life history traits and immune defence in cyprinid fish from central Europe. BMC Evol Biol 8:29. doi: 10.1186/1471-2148-8-29
  121. Sitjà-Bobadilla A, Palenzuela O, Riaza A, Macías MA, Alvarez-Pellitero P (2007) Protective acquired immunity to Enteromyxum scophthalmi (Myxozoa) is related to specific antibodies in Psetta maxima (L.) (Teleostei). Scand J Immunol 66:26–34Google Scholar
  122. Sollid SA, Lorz HV, Stevens DG, Bartholomew JL (2003) Age-dependent susceptibility of Chinook salmon to Myxobolus cerebralis and effects of sustained parasite challenges. J Aquat Anim Health 15:136–146CrossRefGoogle Scholar
  123. Steinbach-Elwell LC, Kerans BL, Rasmussen C, Winton JR (2006) Interactions among two strains of Tubifex tubifex (Oligochaeta: Tubificidae) and Myxobolus cerebralis (Myxozoa). Dis Aquat Org 68:131–139CrossRefGoogle Scholar
  124. St-Hilaire S, Ribble C, Whitaker DJ, Kent ML (1998) Prevalence of Kudoa thrysites in sexually mature and immature pen-reared Atlantic salmon (Salmo salar) in British Columbia, Canada. Aquaculture 162:69–77CrossRefGoogle Scholar
  125. Su Z, Segura M, Morgan K, Loredo-Osti JC, Stevenson MM (2005) Impairment of protective immunity to blood-stage malaria by concurrent nematode infection. Infect Immun 73:3531–3539. doi: 10.1128/IAI.73.6.3531-3539.2005 PubMedPubMedCentralCrossRefGoogle Scholar
  126. Su X, White RWG (1996) Frequency distribution and host-parasite relationships of Zschokkella leptatherinae (Myxozoa: Myxiidae), a parasite of atherinid fishes. Aust J Zool 44:97–106CrossRefGoogle Scholar
  127. Sugihara Y, Yamada T, Tamaki A, Yamanishi R, Kanai K (2014) Larval stages of the bluefin tuna blood fluke Cardicola opisthorchis (Trematoda: Aporocotylidae) found from Terebella sp. (Polychaete: Terebellidae). Parasitol Int 63:295–299PubMedCrossRefGoogle Scholar
  128. Sugihara Y, Yamada T, Ogawa K, Yokoyama F, Matsukura K, Kanai K (2015) Occurrence of the bluefin tuna blood fluke Cardicola opisthorchis in the intermediate host Terebella sp. Fish Pathol 50:105–111CrossRefGoogle Scholar
  129. Sures B (2008) Host-parasite interactions in polluted environments. J Fish Biol 73:2133–2142CrossRefGoogle Scholar
  130. Sures B, Knopf K, Kloas W (2001) Induction of stress by the swimbladder nematode Anguillicola crassus in European eels, Anguilla anguilla, after repeated experimental infection. Parasitology 123:179–184PubMedGoogle Scholar
  131. Telfer S, Lambin X, Birtles R, Beldomenico P, Burthe S, Paterson S, Begon M (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science 330:243. doi: 10.1126/science.1190333 PubMedPubMedCentralCrossRefGoogle Scholar
  132. Thomas F, Poulin R, Brodeur J (2010) Host manipulation by parasites: a multidimensional phenomenon. Oikos 119:1217–1223CrossRefGoogle Scholar
  133. Timi JT, Lanfranchi AL (2013) Ontogenetic changes in heterogeneity of parasite communities of fish: disentangling the relative role of compositional versus abundance variability. Parasitology 140:309–317. doi: 10.1017/S0031182012001606 PubMedCrossRefGoogle Scholar
  134. Timi JT, MacKenzie K (2015) Parasites in fisheries and mariculture. Parasitology 142:1–4PubMedCrossRefGoogle Scholar
  135. Vaumourin E, Vourch G, Gasqui P, Vayssier-Taussat M (2015) The importance of multiparasitism: examining the consequences of coinfections for human and animal health. Parasit Vector 8:545. doi: 10.1186/s13071-015-1167-9 CrossRefGoogle Scholar
  136. Voutilainen A, Figueiredo K, Huuskonen H (2008) Effects of the eye fluke Diplostomum spathaceum on the energetics and feeding of the Arctic charr Salvelinus alpinus. J Fish Biol 73:2228–2237CrossRefGoogle Scholar
  137. Wagner E, Arndt R, Brough M (2002) Comparison of susceptibility of five cutthroat trout strains to Myxobolus cerebralis infection. J Aquat Anim Health 14:84–91CrossRefGoogle Scholar
  138. Warren MB, Orélis-Ribeiro R, Ruiz CF, Dang BT, Arias CR, Bullard SA (2017) Endocarditis associated with blood fluke infections (Digenea: Aporocotylidae: Psettarium cf. anthicum) among aquacultured cobia (Rachycentron canadum) from Nha Trang Bay, Vietnam. Aquaculture 468:549–557. doi: 10.1016/j.aquaculture.2016.11.009 CrossRefGoogle Scholar
  139. Watson MJ (2013) What drives population-level effects of parasites? Meta-analysis meets life-history. Int J Parasitol Parasites Wildl 2:190–196PubMedPubMedCentralCrossRefGoogle Scholar
  140. Wegner KM, Kalbe M, Milinski M, Reusch TBH (2008) Mortality selection during the 2003 European heat wave in three-spined sticklebacks: effects of parasites and MHC genotype. BMC Evol Biol 8:124. doi: 10.1186/1471-2148-8-124 PubMedPubMedCentralCrossRefGoogle Scholar
  141. Wenner C, Archambault J (1996) Spotted seatrout natural history and fishing techniques in South Carolina. Marine Resources Research Institute South Carolina Department of Natural Resources, educational report 18Google Scholar
  142. White VC, Morado JF, Friedman CS (2014) Ichthyophonus-infected walleye pollock Theragra chalcogramma (Pallas) in the eastern Bering Sea: a potential reservoir of infections in the North Pacific. J Fish Dis 37:641–655PubMedCrossRefGoogle Scholar
  143. Wood CL, Byers JE, Cottingham KL, Altman I, Donahue MJ, Blakeslee AMH (2007) Parasites alter community structure. Proc Natl Acad Sci U S A 104:9335–9339. doi: 10.1073/pnas.0700062104 PubMedPubMedCentralCrossRefGoogle Scholar
  144. Wright HA, Wootton RJ, Barber I (2006) The effect of Schistocephalus solidus infection on meal size of three-spined stickleback. J Fish Biol 68:801–809. doi: 10.1111/j.1095-8649.2006.00966.x CrossRefGoogle Scholar
  145. Yokota M, Watanabe S, Hatai K, Kurata O, Furihata M, Usui T (2008) Transmission of the parasite Ichthyophonus hoferi in cultured rainbow trout and comparison of epidemic models. J Aquat Anim Health 20:207–214PubMedCrossRefGoogle Scholar
  146. Yokoyama H, Kawakami H, Yasuda H, Tanaka S (2003) Henneguya lateolabracis sp. n. (Myxozoa: Myxosporea), the causative agent of cardiac henneguyosis in Chinese sea bass Lateolabrax sp. Fish Sci 69:1116–1120CrossRefGoogle Scholar
  147. Yokoyama H, Itoh N, Tanaka S (2005) Henneguya pagri n. sp. (Myxozoa: Myxosporea) causing cardiac henneguyosis in red sea bream, Pagrus major (Temminck & Schlegel). J Fish Dis 28:479–487PubMedCrossRefGoogle Scholar
  148. Yokoyama H, Grabner D, Shirakashi S (2012) Transmission biology of the Myxozoa, health and environment in aquaculture, Carvalho E (Ed.). doi: 10.5772/29571
  149. Yong RQY, Cutmore SC, Miller TL, Adlard RD, Cribb TH (2013) The ghost of parasites past: eggs of the blood fluke Cardicola chaetodontis (Aporocotylidae) trapped in the heart and gills of butterflyfishes (Perciformes: Chaetodontidae) of the Great Barrier Reef. Parasitology 140:1186–1194PubMedCrossRefGoogle Scholar
  150. Zajac RN (1991) Population ecology of Polydora ligni (Polychaeta, Spionidae). 2. Seasonal demographic variation and its potential impact on life-history evolution. Mar Ecol Prog Ser 77:207–220. doi: 10.3354/meps077207 CrossRefGoogle Scholar
  151. Zuo S, Huwer B, Bahlool Q, Al-Jubury A, Christensen N, Korbut R, Kania P, Buchmann K (2016) Host size-dependent anisakid infection in Baltic cod Gadus morhua associated with differential food preferences. Dis Aquat Org 120:69–75. doi: 10.3354/dao03002 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.South Carolina Department of Natural ResourcesMarine Resources Research InstituteCharlestonUSA
  2. 2.Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  3. 3.Department of BiologyCollege of CharlestonCharlestonUSA

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