Abstract
Anadromous river herring have declined in many parts of their range, leading to fisheries management efforts to help repopulate this species by improving connectivity of rivers and restoring populations by fish transfers. With data lacking on parasites in these species, this study sought to better understand myxozoans across various life stages and habitats in river herring populations in New Jersey, USA. We compared fish from riverine habitats during early-life growth and adults returning to spawn, marine-phase fish, and landlocked Alewife populations. Three myxozoan species were identified in young-of-the-year (YOY) anadromous river herring, including Kudoa clupeidae in the skeletal musculature, Myxobolus mauriensis in the rib cartilage, and an uncharacterized coelozoic myxozoan within the lumen of mesonephric tubules. In YOY river herring, Blueback Herring were 2 times more likely to be infected by K. clupeidae than Alewife (p = 0.019) and in the Maurice River, fish were 4 times more likely to be infected with M. mauriensis than fish from Great Egg Harbor River (p = 0.000) and 11 times more likely than the Delaware River (p = 0.001). Spawning adult river herring were infected with a previously undescribed myxozoan parasite infecting the kidney. Sequencing the 18S rDNA indicated this species is closely related to Ortholinea species. Myxobolus mauriensis and the Ortholinea-like species were absent from marine-phase river herring indicating that infections were linked to river environments occurring during early-life growth and spawning, respectively. No myxozoans were present in landlocked Alewife, showing that similar infections occurring in rivers were absent in lake environments in the region.
Similar content being viewed by others
Availability of data and material
Additional data and materials can be made available upon request to the corresponding author.
Code availability
Not applicable.
References
Alama-Bermejo G, Hernández-Orts J (2018) Ortholinea concentrica n. sp. (Cnidaria: Myxozoa) from the Patagonian seabass Acanthistius patachonicus (Jenyns, 1840) (Perciformes: Serranidae) off Patagonia. Argentina Parasitol Res 117:3953–3963. https://doi.org/10.1016/j.ijpara.2006.06.016
Atlantic States Marine Fisheries Commission (ASMFC) (2012) River herring benchmark stock assessment volume I. Stock Assessment Report No. 12–02. Arlington, VA, pp 4–37
Atlantic States Marine Fisheries Commission (ASMFC) (2017) River herring stock assessment update volume II: state specific reports. Available from: https://www.asmfc.org/uploads/file/59c2ac1fRiverHerringStockAssessmentUpdateVolumeII_State-Specific_Aug2017.pdf. Accessed 25 Jun 2021
Bartholomew JL, Rohovec JS, Fryer JL (1989) Ceratomyxa shasta, a myxosporean parasite of salmonids. US Fish and Wildlife Service, Fish Disease Leaflet 80. https://www.arlis.org/docs/vol1/18960816/18960816.htm. Accessed 9 Sep 2021
Bochenek AE (1981) Age, growth, and feeding habits of the landlocked alewife, Alosa pseudoharengus, in two New Jersey lakes (Master’s thesis). East Stroudsburg University pp138
Burger MA, Adlard RD (2011) Low host specificity in the Kudoidae (Myxosporea Multivalvulida) including seventeen new host records for Kudoa thalassomi. Folia Parasitol 58:1–16. https://doi.org/10.14411/fp.2011.001
Canning EU, Okamura B (2004) Biodiversity and evolution of the Myxozoa. Adv Parasitol 56:43–131. https://doi.org/10.1016/s0065-308x(03)56002-x
Cuhel RL, Aguilar C (2013) Ecosystem transformations of the Laurentian Great Lake Michigan by nonindigenous biological invaders. Ann Rev Mar Sci 5:289–320. https://doi.org/10.1146/annurev-marine-120710-100952
De Castro F, Bolker B (2005) Mechanisms of disease-induced extinction. Ecol Lett 8:117–126. https://doi.org/10.1111/j.1461-0248.2004.00693.x
Eszterbauer E (2004) Genetic relationship among gill-infecting Myxobolus species (Myxosporea) of cyprinids: molecular evidence of importance of tissue-specificity. Dis Aquat Org 58:35–40. https://doi.org/10.3354/dao058035
Fay CW, Neves RJ, Pardue GB (1983) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (mid-Atlantic) – alewife/blueback herring. US Fish and Wildlife Service, Division of Biological Servces, FWS/OBS-82111.9. US Army Corps of Engineers, TR EL-82–4
Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1534. https://doi.org/10.1016/j.ijpara.2006.06.016
Fiala I, Bartošová-Sojková P, Whipps CM (2015) Classification and phylogenetics of myxozoa. In: Okamura B, Gruhl A, Bartholomew JL (eds) Myxozoan evolution, ecology and development. Springer International Publishing, Cham, pp 85–110
Gross R (1951) Some observations on the landlocked alewife Pomolobus pseudoharengus (Wilson) in New Jersey. N.J Fisheries Survey 2:157–164
Grunberg RL, Brianik CJ, Lovy J, Sukhdeo MVK (2019) Divergence in Alewife Alosa pseudoharengus (Actinopterygii, Clupeidae), life history alters parasite communities. Hydrobiol 826:307–318. https://doi.org/10.1007/s10750-018-3743-4
Hahn CW (1917) On the sporozoon parasites of the fishes of Woods Hole and vicinity. III On the Chloromyxum clupeidae of Clupea harengus (Young), Pomolobus pseudoharengus (Young), and P. aestivalis (Young). J Parasitol 14:13–20
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98
Hall CJ, Jordaan A, Frisk MG (2010) The historic influence of dams on diadromous fish habitat with a focus on river herring and hydrologic longitudinal connectivity. Landsc Ecol 26:95–107. https://doi.org/10.1007/s10980-010-9539-1
Hall CJ, Jordaan A, Frisk MG (2012) Centuries of anadromous forage fish loss: consequences for ecosystem connectivity and productivity. BioSci 62:723–731. https://doi.org/10.1525/bio.2012.62.8.5
Hallett SL, Bartholomew JL (2008) Effects of water flow on the infection dynamics of Myxobolus cerebralis. Parasitol 135:371–684. https://doi.org/10.1017/S0031182007003976
Hedrick RP, El-Matbouli M, Adkison MA, MacConnell E (1998) Whirling disease: re-emergence among wild trout. Immunol Rev 166:365–376. https://doi.org/10.1111/j.1600-065x.1998.tb01276.x
Hillis DM, Dixon MT (1991) Ribosomal DNA: Molecular Evolution and Phylogenetic Inference. Q Rev Biol 66:411–453. https://doi.org/10.1086/417338
Hoffmaster JL, Sanders JE, Rohovec JS, Fryer JL, Stevens DG (1988) Geographic and seasonal distribution of the myxosporean parasite, Ceratomyxa shasta Noble, 1950, in the Columbia River basin, USA. J Fish Dis 11:97–100
Kaeser AJ, Rasmussen C, Sharpe WE (2006) An examination of environmental factors associated with Myxobolus cerebralis infection of wild trout in Pennsylvania. J Aquat Anim Health 18:90–100. https://doi.org/10.1577/H05-017.1
Karlsbakk E, Køie M (2011) Morphology and SSU rDNA sequences of Ortholinea orientalis (Shul’man and Shul’man-Albova, 1953) (Myxozoa, Ortholineidae) from Clupea harengus and Sprattus sprattus (Clupeidae) from Denmark. Parasitol Res 109:139–145. https://doi.org/10.1007/s00436-010-2237-8
Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J, Hallett SL, Lester RJG, Longshaw M, Palenzeula O, Siddall ME, Xiao C (2001) Recent advances in our knowledge of the Myxozoa. Eukaryot Microbiol 48(4):395–413. https://doi.org/10.1111/j.1550-7408.2001.tb00173.x
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Lafferty KD, Kuris AM (1999) How environmental stress affects the impacts of parasites. Limnol Oceanogr 44:925–931. https://doi.org/10.4319/lo.1999.44.3_part_2.0925
Lazim MN, Learner MA (1987) The influence of sediment composition and leaf litter on the distribution of tubificid worms (Oligochaeta). Oecol 72:131–136. https://doi.org/10.1007/BF00385057
Lepak JM, Kraft CE (2008) Alewife mortality, condition, and immune response to prolonged cold temperature. J Great Lakes Res 34:134–142
Limburg KE, Waldman JR (2009) Dramatic declines in North Atlantic diadromous fishes. BioSci 59:955–965. https://doi.org/10.1525/bio.2009.59.11.7
Lom J, Dykova I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36
Lovy J, Friend SE (2015) Intestinal coccidiosis of anadromous and landlocked alewives, Alosa pseudoharengus, caused by Goussia ameliae n. sp. and G. alosii n. sp. (Apicomplexa: Eimeriidae). Int J Parasitol Parasites Wildl 4:159–170. https://doi.org/10.1016/j.ijppaw.2015.02.003
Lovy J, Hutcheson JM (2016) Myxobolus mauriensis n. sp. infecting rib cartilage of young-of-the-year river herring in New Jersey: notes on pathology, prevalence, and genetics. J Parasitol 102:419–428. https://doi.org/10.1645/15-939
Marcogliese DJ, Gendron AD, Cone DK (2009) Impact of municipal effluents and hydrological regime on myxozoan parasite communities of fish. Int J Parasitol 39:1345–1351. https://doi.org/10.1016/j.ijpara.2009.04.007
Mattocks S, Hall CJ, Jordaan A (2017) Damming, lost connectivity, and the historical role of anadromous fish in freshwater ecosystem dynamics. BioSci 67:713–728. https://doi.org/10.1093/biosci/bix069
Morris DJ (2010) Cell formation by myxozoan species is not explained by dogma. Proc R Soc B 277(1693):2565–2570. https://doi.org/10.1098/rspb.2010.0282
National Oceanographic and Atmospheric Association (NOAA). (2021). River herring. Available from: https://www.fisheries.noaa.gov/species/river-herring#management (Accessed on: 29 Mar 2021)
Nei M, Kumar S (2000) Molecular Evolution and Phylogenetics. Oxford University Press, New York
Palkovacs EP, Dion KB, Post DM, Caccone A (2008) Independent evolutionary origins of landlocked alewife populations and rapid parallel evolution of phenotypic traits. Mol Ecol 17:582–597. https://doi.org/10.1111/j.1365-294X.2007.03593.x
Reimschuessel R, Gieseker CM, Driscoll C, Baya A, Kane AS, Blazer VS, Evans JJ, Kent ML, Moran JD, Poynton SL (2003) Myxosporean plasmodial infection associated with ulcerative lesions in young-of-the-year Atlantic menhaden in a tributary of the Chesapeake Bay, and possible links to Kudoa clupeidae. Dis Aquat Org 53:143–166. https://doi.org/10.3354/dao053143
Ryce EKN, Zale AV, MacConnell E (2004) Effects of fish age and parasite dose on the development of whirling disease in rainbow trout. Dis Aquat Org 59:225–233. https://doi.org/10.3354/dao059225
Smith TA, Kraft CE (2005) Stream fish assemblages in relation to landscape position and local habitat variables. Trans Am Fish Soc 134(2):430–440. https://doi.org/10.1577/T03-051.1
Stinson MET, Atkinson SD, Bartholomew JL (2018) Widespread distribution of Ceratonova shasta (Cnidaria: Myxosporea) genotypes indicates evolutionary adaptation to its salmonid fish hosts. J Parasitol 104(6):645–650. https://doi.org/10.1645/18-79
Sudhagar A, Kumar G, El-Matbouli M (2020) The Malacosporean myxozoan parasite Tetracapsuloides bryosalmonae: a threat to wild salmonids. Pathog 9:16. https://doi.org/10.3390/pathogens9010016
Turner SM, Limburg KE (2016) Juvenile river herring habitat use and marine emigration trends: comparing populations. Oecol 180:77–89. https://doi.org/10.1007/s00442-015-3443-y
Webb SR, Garman GC, McIninch SP, Nerad TA, Peglar MT, Gillevet PM, Brown BL (2005) Etiology of ulcerative lesions of Atlantic menhaden (Brevoortia tyrannus) from James River, Virginia. Parasitol Res 97:358–366. https://doi.org/10.1007/s00436-005-1437-0
West DC, Walters AW, Gephard S, Post DM (2010) Nutrient loading by anadromous alewife (Alosa pseudoharengus): contemporary patterns and predictions for restoration efforts. Can J Fish Aquat Sci 67:1211–1220. https://doi.org/10.1139/F10-059
Whipps CM (2011) Interrenal disease in bluegills (Lepomis macrochirus) caused by a new genus and species of myxozoan. J Parasitol 97:1159–1165. https://doi.org/10.1645/GE-2763.1
Whipps CM, Kent ML (2006) Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). J Eukaryot Microbiol 53:364–373. https://doi.org/10.1111/j.1550-7408.2006.00114.x
Whipps CM, Adlard RD, Bryant MS, Kent ML (2003) Two unusual myxozoans, Kudoa quadricornis n. sp. (Multivalvulida) from the muscle of godspotted trevally (Carangoides fulvoguttatus) and Kudoa permulticapsula n. sp. (Multivalvulida) from the muscle of Spanish mackerel (Scomberomorus commersoni) from the Great Barrier Reef, Australia. J Parasitol 89:168–173. https://doi.org/10.1645/0022-3395(2003)089[0168:TUMKQN]2.0.CO;2
Wünnemann H, Holzer AS, Pecková H, Bartošová-Sojková P, Eskens U, Lierz M (2016) Repatriation of an old fish host as an opportunity for myxozoan parasite diversity: the example of the allis shad, Alosa alosa (Clupeidae), in the Rhine. Parasite Vectors 9:505. https://doi.org/10.1186/s13071-016-1760-6
Acknowledgements
We would like to thank the Bureau of Marine Fisheries: Brian Neilan, Heather Corbett, Hugh Carberry, Gregory Hinks and the Bureau of Freshwater Fisheries: Chris Smith, Ross Shramko as well as Josette Hutcheson in the Office of Fish and Wildlife Health and Forensics for their assistance in collecting fish for this project. We would also like to thank Lana Castellano from the Animal Health Diagnostic Laboratory, New Jersey Department of Agriculture for her assistance with sample processing.
Funding
This project was funded by the Federal Aid in Sport Fish Restoration Act, Project FW-69-R-18 and FW-69-R-19, and the New Jersey Hunters and Anglers Fund.
Author information
Authors and Affiliations
Contributions
S.E. Friend, sample processing and preparing the manuscript; N.L. Lewis, statistical analyses and preparing the manuscript; J. Lovy, data analysis, overseeing the study, and manuscript preparation. S.E. Friend and N.L. Lewis had equal contributions to this work.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional declarations for articles in life science journals that report the results of studies involving humans and/or animals
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Section Editor: Christopher Whipps
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Friend, S.E., Lewis, N.L. & Lovy, J. Myxozoan parasites vary in river herring according to life history stage and habitat. Parasitol Res 120, 3709–3723 (2021). https://doi.org/10.1007/s00436-021-07329-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-021-07329-y