Skip to main content
Log in

First documentation and molecular confirmation of three trematode species (Platyhelminthes: Trematoda) infecting the polychaete Marenzelleria viridis (Annelida: Spionidae)

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Polychaete worms are hosts to a wide range of marine parasites; yet, studies on trematodes using these ecologically important species as intermediate hosts are lacking. During examination of the spionid polychaete Marenzelleria viridis collected on the north shore of Long Island, New York, putative trematode cysts were discovered in the body cavity of these polychaetes. In order to verify these cysts as metacercariae of trematodes, specimens of the eastern mudsnail Ilyanassa obsoleta (a very common first intermediate host of trematodes in the region) were collected for molecular comparison. DNA barcoding using cytochrome C oxidase I regions confirmed the presence of three species of trematodes (Himasthla quissetensis, Lepocreadium setiferoides, and Zoogonus lasius) in both M. viridis and I. obsoleta hosts. Brown bodies were also recovered from polychaetes, and molecular testing confirmed the presence of L. setiferoides and Z. lasius, indicating an immune response of the polychaete leading to encapsulation of the cysts. From the 125 specimens of M. viridis collected in 2014, 95 (76.8 %) were infected with trematodes; of these 95 infected polychaetes, 86 (90.5 %) contained brown bodies. This is the first confirmation that trematodes use M. viridis as a second intermediate host and that this intermediate host demonstrates a clear immune response to metacercarial infection. Future research should explore the role of these polychaetes in trematode life cycles, the effectiveness of the immune response, and transmission pathways to vertebrate definitive hosts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ambrose WG Jr (1986) Estimate of removal rate of Nereis virens (Polychaeta: Nereidae) from an intertidal mudflat by gulls (Larus spp.). Mar Biol 90:243–247

    Article  Google Scholar 

  • Barber KE, Caira JN (1995) Investigation of the life cycle and adult morphology of the avian blood fluke Austrobilharzia variglandis (Trematoda: Schistosomatidae) from Connecticut. J Parasitol 81:584–592

    Article  CAS  PubMed  Google Scholar 

  • Beschin A, Bilej M, Brys L, Torreele E, Lucas R, Magez S, De Baetselier P (1999) Convergent evolution of cytokines. Nature 400:627–628

    Article  CAS  PubMed  Google Scholar 

  • Bilej M (1994) Cellular defense mechanisms in immunology of annelids. CRC Press, Boca Raton, pp 183–184

    Google Scholar 

  • Blakeslee AMH, Fowler AE (2012) Aquatic introductions and genetic founder effects: how do parasites compare to hosts? In: Caliskan M (ed) Analysis of Genetic Variation in Animals, InTech, pp 315–336

  • Blakeslee AM, Altman I, Miller AW, Byers JE, Hamer CE, Ruiz GM (2012) Parasites and invasions: a biogeographic examination of parasites and hosts in native and introduced ranges. J Biogeogr 39:609–622

    Article  Google Scholar 

  • Blank M, Laine AO, Jurss K, Bastrop R (2008) Molecular identification key based on PCR/RFLP for three polychaete sibling species of the genus Marenzelleria and the species’ current distribution in the Baltic Sea. Helgol Mar Res 62:129–141

    Article  Google Scholar 

  • Bravo M (1956) Trematodos de peces marinos de aguas Mexicanas. XI. Estudio de 17 digeneos de las costas del Pacifico, incluyendo seis especies nuevas y un genero nuevo. Anales del Instituto de Biología, Universidad Nacional Autónoma de México 27:245–277

    Google Scholar 

  • Bray RA (1987) A revision of the family Zoogonidae Odhner, 1902 (Platyhelminthes: Digenea): introduction and subfamily Zoogoninae. Syst Parasitol 9:3–28

    Article  Google Scholar 

  • Bray RA, Gibson DI (1986) The Zoogonidae (Digenea) of fishes from the north-east Atlantic. Bull Br Mus Nat Hist Zool 51:127–206

    Google Scholar 

  • Brown B, Prezant RS (1986) Occurrence of a digenetic trematode in a polychaete. J Invertebr Pathol 48:239–241

    Article  Google Scholar 

  • Cosson N, Sibuet M, Galeron J (1997) Community structure and spatial heterogeneity of the deep-sea macrofauna at three contrasting stations in the tropical northeast Atlantic. Deep Sea Res Part I: Oceanogr Res Pap 44:247–269

    Article  CAS  Google Scholar 

  • Cribb TH (2005) Digenea (endoparasitic flukes) In: Rohde K (ed) Marine Parasitology, CSIRO Publishing pp 76–87

  • Cribb TH, Bray RA, Littlewood DTJ (2001) The nature and evolution of the association among digeneans, molluscs and fishes. Int J Parasitol 31:997–1011

    Article  CAS  PubMed  Google Scholar 

  • Curtis LA (1997) Ilyanassa obsoleta (Gastropoda) as a host for trematodes in Delaware estuaries. J Parasitol 83:793–803

    Article  CAS  PubMed  Google Scholar 

  • Curtis LA (2009) The gastropod Ilyanassa obsoleta as a resource: utilization by larval trematodes in a low-prevalence system. J Parasitol 95:799–807

    Article  PubMed  Google Scholar 

  • Cuvillier-Hot V, Boidin-Wichlacz C, Tasiemski AA (2014) Polychaetes as annelid models to study ecoimmunology of marine organisms. J Mar Sci Technol 22:9–14

    Google Scholar 

  • Dales RP (1983) Observations on granulomata in the polychaetous annelid Nereis diversicolor. J Invertebr Pathol 42:288–291

    Article  Google Scholar 

  • Delefosse M, Banta GT, Canal-Verges P, Penha-Lopes G, Quintana CO, Valdemarsen T, Kristensen E (2012) Macrobenthic community response to the Marenzelleria viridis (Polychaeta) invasion of a Danish estuary. Mar Ecol Prog Ser 461:83–94

    Article  Google Scholar 

  • Derrick P, Kennedy V (1997) Prey selection by the hogchoker, Trinectes maculatus (Pisces: Soleidae), along summer salinity gradients in Chesapeake Bay, USA. Mar Biol 129:699–711

    Article  Google Scholar 

  • Dhainaut A, Scaps P (2001) Immune defense and biological responses induced by toxics in Annelida. Can J Zool 79:233–253

    Article  CAS  Google Scholar 

  • Efron B (1982) The jackknife, the bootstrap and other resampling plans. SIAM, Stanford

    Book  Google Scholar 

  • Ehrhardt W, Harkema R, Miller G (1966) Trematodes from two species of gulls from North Carolina. J Elisha Mitchell Sci Soc 82:208–212

    Google Scholar 

  • Esch GW, Barger MA, Fellis KJ (2002) The transmission of digenetic trematodes: style, elegance, complexity. Integr Comp Biol 42:304–312

    Article  PubMed  Google Scholar 

  • Essink K, Kleef HL (1991) Distribution and life cycle of the North American apionid polychaete Marenzelleria viridis (Verrill, 1873) in the Ems eastuary. Neth J Aquat Ecol 27:237–246

    Article  Google Scholar 

  • Field SG, Kurtz J, Cooper EL, Michiels NK (2004) Evaluation of an innate immune reaction to parasites in earthworms. J Invertebr Pathol 86:45–49

    Article  CAS  PubMed  Google Scholar 

  • Hall B (2011) Phylogenetic trees made easy: a how-to manual, 4th edn. Sinauer Assoc, Sunderland

    Google Scholar 

  • Heard RW (1982) Observations on the food and food habits of clapper rails (Rallus longirostris Boddaert) from tidal marshes along the East and Gulf Coasts of the United States. Gulf Res Rep 7:125–135

    Google Scholar 

  • Hunter WS (1967) Notes on the life history of Pleurogonius malaclemys Hunter 1961, (Trematoda: Pronocephalidae) from Beaufort, North Carolina, with a description of the cercaria. Proc Helminthol Soc Wash 34:33–40

    Google Scholar 

  • Johnson PTJ, Thieltges DW (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. J Exp Bio 213:961–970

    Article  CAS  Google Scholar 

  • Jovanovic Z, Larsen M, Quintana CO, Kristensen E, Glud R (2014) Oxygen dynamics and porewater transport in sediments inhabited by the invasive polychaete Marenzelleria viridis. Mar Ecol Prog Ser 504:181–192

    Article  Google Scholar 

  • Køie 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 21:115–145

    Article  Google Scholar 

  • Køie M (2000) The life-cycle of the flatfish nematode Cucullanus heterochrous. J Helminthol 74:323–328

    PubMed  Google Scholar 

  • Koppel EM, Leung TLF, Poulin R (2011) The marine limpet Notoacmea scapha acts as a transmission sink for intertidal cercariae in Otago harbor, New Zealand. J Helminthol 85:160–163

    Article  CAS  PubMed  Google Scholar 

  • Kotta J, Orav H, Sandberg-Kilpi E (2001) Ecological consequence of the introduction of the polychaete Marenzelleria cf. viridis into a shallow-water biotope of the northern Baltic Sea. Sea Res 46:273–280

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Leopold MF, van Damme CJ (2003) Great cormorants Phalacrocorax carbo and polychaetes: can worms sometimes be a major prey of a piscivorous seabird. Mar Ornithol 31:83–87

    Google Scholar 

  • Leung TLF, Donald KM, Keeney DB, Koehler AV, Peoples RC, Poulin R (2009a) Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: life cycles, ecological roles and DNA barcodes. N Z J Mar Freshwater Res 43:857–865

    Article  CAS  Google Scholar 

  • Leung TLF, Keeney DB, Poulin R (2009b) Cryptic species complexes in manipulative echinostomatid trematodes: when two become six. Parasitol 136:241–252

    Article  CAS  Google Scholar 

  • Li K (2003) ClustalW-MPIL ClustalW analysis using distributed and parallel computing. Bioinformatics 19:1585–1586

    Article  PubMed  Google Scholar 

  • Machida RJ, Knowlton N (2012) PCR primers for metazoan nuclear 18S and 28S ribosomal DNA sequences. PLoS ONE 7, e46180. doi:10.1371/journal.pone.0046180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maciolek NJ (1984) New records and species of Marenzelleria Mesnil and Scolecolepides Ehlers (Polychaeta; Spionidae) from Northeastern North America. In: Hutchings PA (ed) Proceedings of the First International Polychaete Conference. Linnean Society of New South Wales, pp 48–62

  • Marcogliese DJ (2002) Food webs and the transmission of parasites to marine fish. Parasitol 124:83–89

    Article  Google Scholar 

  • Margolis L (1971) Polychaetes as intermediate hosts of helminth parasites of vertebrates: a review. Fish Res Board Can 28:1385–1392

    Article  Google Scholar 

  • Margolis L (1973) Additional notes on polychaetes as intermediate hosts of helminth parasites of vertebrates. Fish Res Board Can 30:469–470

    Article  Google Scholar 

  • Martin WE (1939) Studies on the trematodes of Woods Hole II. The life cycle of Stephanostomum tenue (Linton). Biol Bull 77:65–73

    Article  Google Scholar 

  • McCurdy DG (2001) Asexual reproduction in Pygiospio elegans Claparède (Annelida, Polychaeta) in relation to parasitism by Lepocreadium setiferoides (Miller and Northup) (Platyhelminthes, Trematoda). Biol Bull 201:45–51

    Article  CAS  PubMed  Google Scholar 

  • McCurdy DG, Moran B (2004) Parasitism and soft-bottom community structure: studies in a polychaete-amphipod system. J Mar Biol Assoc UK 84:165–169

    Article  Google Scholar 

  • McCurdy DG, Boates JS, Forbes MR (2000) Spatial distribution of the intertidal snail Ilyanassa obsoleta in relation to parasitism by two species of trematodes. Can J Zool 78:1137–1143

    Article  Google Scholar 

  • McDermott J Jr (1951) Larval trematode infection in Nassa obsoleta Say, from New Jersey waters. Unpublished master’s thesis, Rutgers University, New Brunswick

    Google Scholar 

  • Miller DC, Bock MJ, Turner EJ (1992) Deposit and suspension feeding in oscillatory flows and sediment fluxes. J Mar Res 50:489–520

    Article  Google Scholar 

  • Moszczynska A, Locke SA, McLaughlin JD, Marcogliese DJ, Crease TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Mol Ecol Resour 9(Suppl 1):75–82

    Article  CAS  PubMed  Google Scholar 

  • Mouritsen KN, Poulin R (2005) Parasitism can influence the intertidal zonation of non-host organisms. Mar Biol 148:1–11

    Article  Google Scholar 

  • Peoples RC (2013) A review of the helminth parasites using polychaetes as hosts. Parasitol Res 112:3409–3421

    Article  PubMed  Google Scholar 

  • Peoples RC, Poulin R (2011) Encystment patterns and metacercarial size of an opecoelid trematode in two polychaete hosts. Parasitol Res 109:865–870

    Article  PubMed  Google Scholar 

  • Peoples RC, Randhawa HS, Poulin R (2012) Parasites of polychaetes and their impact on host survival in Otago Harbour, New Zealand. J Mar Biol Assoc UK 92:449–455

    Article  Google Scholar 

  • Poinar GO Jr, Hess RT (1977) Immune responses in the earthworm, Aporrectodea trapezoides (Annelida), against Rhabditis pellio (Nematoda). In: Bulla LJ Jr, Cheng TC (eds) Comparative Pathobiology. Volume 3: Invertebrate Immune Responses. Springer, pp 69–84

  • Porchet-Henneré E (1990) Cooperation between different coelomocyte populations during the encapsulation response of Nereis diversicolor demonstrated by using monoclonal antibodies. J Invertebr Pathol 56:353–361

    Article  Google Scholar 

  • Porchet-Henneré E, M'Berri M (1987) Cellular reactions of the polychaete annelid Nereis diversicolor against coelomic parasites. J Invertebr Pathol 50:58–66

    Article  Google Scholar 

  • Porchet-Henneré E, Vernet G (1992) Cellular immunity in an annelid (Nereis diversicolor, Polychaeta): production of melanin by a subpopulation of granulocytes. Cell Tissue Res 269:167–174

    Article  PubMed  Google Scholar 

  • Porchet-Henneré E, M'Berri M, Dhainaut A, Porchet M (1987) Ultrastructural study of the encapsulation response of the polychaete annelid Nereis diversicolor. Cell Tissue Res 248:463–471

    Article  Google Scholar 

  • Poulin R, Cribb TH (2002) Trematode life cycles: short is sweet? Trends Parasitol 18:176–183

    Article  PubMed  Google Scholar 

  • Procházková P, Silerová M, Stijlemans B, Dieu M, Halada P, Josková R, Beschin A, De Baetselier P, Bilej M (2006) Evidence for proteins involved in prophenoloxidase cascade Eisenia fetida earthworms. J Comp Physiol B 176:581–587

    Article  PubMed  Google Scholar 

  • Quintana CO, Hansen T, Delefosse M, Banta G, Kristensen E (2011) Burrow ventilation and associated porewater irrigation by the polychaete Marenzelleria viridis. Exp Mar Biol Ecol 397:179–187

    Article  Google Scholar 

  • Rangel LF, Santos MJ (2009) Diopatra neapolitana (Polychaeta: Onuphidae) as a second intermediate host of Gymnophallus choledochus (Digenea: Gymnophallidae) in the Aveiro Estuary (Portugal): distribution within the host and histopathology. J Parasitol 95:1233–1236

    Article  CAS  PubMed  Google Scholar 

  • Reinhart M, Dollahon N (2003) Responses of coelomocytes from Lumbricus terrestris to native and non-native eukaryotic parasites: The 7th international symposium on earthworm ecology - Cardiff - Wales - 2002. Pedobiologia 47:710–716

  • Renz JR, Forster S (2013) Are similar worms different? A comparative tracer study on bioturbation in the three sibling species Marenzelleria arctia, M. viridis, and M. neglecta from the Baltic Sea. Limnol Oceanogr 58:2046–2058

    Article  Google Scholar 

  • Sanna D, Lai T, Francalacci P, Curini-Galletti M, Casu M (2009) Population structure of the Monocelis lineata (Proseriata, Monocelididae) species complex assessed by phylogenetic analysis of the mitochondrial cytochrome C oxidase subunit I (COI) gene. Genet Mol Biol 32:864–867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sardá R, Foreman K, Werme CE, Valiela I (1998) The impact of epifaunal predation on the structure of macroinfaunal invertebrate communities of tidal saltmarsh creeks. Estuar Coast Shelf Sci 46:657–669

    Article  Google Scholar 

  • Schell SC (1970) How to know the trematodes. WC Brown Company Publishers, Dubuque

    Google Scholar 

  • Shaw CR (1933) Observations on Cercariaeum lintoni Miller and Northup and its metacercarial development. Biol Bull 64:262–275

    Article  Google Scholar 

  • Sikorski AV, Bick A (2004) Revision of Marenzelleria Mesnil, 1896 (Spionidae, Polychaeta). Sarsia 89:253–275

    Article  Google Scholar 

  • Sima P (1994) Coelomocytes and hemoctyes: roles in cellular immune reactions. In: Vetvicka V, Síma P, Cooper EL, Bilej M, Roch P (eds) Immunology of Annelids, vol 5. CRC Press, Boca Raton, pp 115–166

    Google Scholar 

  • Smith NF, Ruiz GM, Reed SA (2007) Habitat and host specificity of trematode metacercariae in fiddler crabs from mangrove habitats in Florida. J Parasitol 93:999–1005

    Article  PubMed  Google Scholar 

  • Stunkard HW (1938) Distomum lasium Leidy, 1891 (syn. Cercariaeum lintoni Miller and Northup, 1926), the larval stage of Zoögonus rubellus (Olsson, 1868)(syn. Z. mirus Looss, 1901). Biol Bull 75:308–334

    Article  Google Scholar 

  • Stunkard HW (1970) The marine cercariae of the woods hole Massachusetts Region. Biol Bull 138:66–76

    Article  Google Scholar 

  • Stunkard HW (1972) Observations on the morphology and life-history of the digenetic trematode, Lepocreadium setiferoides (Miller and Northup, 1926) Martin, 1938. Biol Bull 142:326–334

    Article  CAS  PubMed  Google Scholar 

  • Stunkard HW (1983) The marine cercariae of the woods hole, Massachusetts region, a review and a revision. Biol Bull 164:143–162

    Article  Google Scholar 

  • Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101:1130–11035

    Google Scholar 

  • Valembois P, Lassègues M, Roch P (1992) Formation of brown bodies in the coelomic cavity of the earthworm Eisenia fetida andrei and attendant changes in shape and adhesive capacity of constitutive cells. Dev Comp Immunol 16:95–101

    Article  CAS  PubMed  Google Scholar 

  • Valembois P, Seymour J, Lassègues M (1994) Evidence of lipofuscin and melanin in the brown body of the earthworm Eisenia fetida andrei. Cell Tissue Res 277:183–188

    Article  CAS  Google Scholar 

  • Vilas R, Criscione C, Blouin M (2005) A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species for platyhelminth parasites. Parasitol 131:839–846

    Article  CAS  Google Scholar 

  • Walsh SP, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513

    CAS  PubMed  Google Scholar 

  • Winkler H, Debus L (1996) Is the polychaete Marenzelleria viridis an important food item for fish? In: Proceedings of the 13th Symposium of Baltic Marine Biologists, Riga (Latvia), pp 147–151

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguti S (1975) A synoptical review of life histories of digenetic trematodes of vertebrates with special reference to the morphology of their larval forms. Keigaku Publishing Co, Tokyo

    Google Scholar 

  • Zander CD, Reimer LW (2002) Parasitism at the ecosystem level in the Baltic Sea. Parasitol 124:S119–S135

    Article  Google Scholar 

  • Zettler ML (1997a) Population dynamics, growth and production of the neozoon Marenzelleria cf. viridis (Verrill, 1873) (Polychaeta: Spionidae) in a coastal water of the southern Baltic Sea. Aquat Ecol 31:177–186

    Article  Google Scholar 

  • Zettler ML (1997b) Bibliography on the genus Marenzelleria and its geographical distribution, principal topics and nomenclature. Aquat Ecol 31:233–258

    Article  Google Scholar 

Download references

Acknowledgments

The support of Hofstra University is appreciated, particularly Faculty Research and Development Grants to MKK and JDW.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jason D. Williams.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1

(DOC 34 kb)

Supplementary Fig. 1

(DOC 50 kb)

Supplementary Fig. 2

(DOC 84 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Phelan, K., Blakeslee, A.M.H., Krause, M. et al. First documentation and molecular confirmation of three trematode species (Platyhelminthes: Trematoda) infecting the polychaete Marenzelleria viridis (Annelida: Spionidae). Parasitol Res 115, 183–194 (2016). https://doi.org/10.1007/s00436-015-4734-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4734-2

Keywords

Navigation