Skip to main content

Advertisement

SpringerLink
Log in

Non-host organisms affect transmission processes in two common trematode parasites of rocky shores

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The transmission of free-living trematode stages is mediated by various environmental factors, of which the presence of ambient organisms within the host space is a potential major determinant. In two laboratory mesocosm experiments, we investigated the influence of four intertidal rocky shore species on transmission success of cercariae of the digenean trematodes Echinostephilla patellae (encysting in the tissue of blue mussels Mytilus edulis) and Parorchis acanthus (encysting on mussel shells). Encystment success of both parasite species was significantly lower in the presence of test organisms when compared to controls. Observations revealed that barnacles Austrominius modestus actively filtered cercariae, whereas the larvae were obstructed by the seaweeds Corallina officinalis and Fucus serratus. Anemones Actinia equina both physically disturbed and consumed cercariae. In a further laboratory experiment, grazing gastropods (Littorina littorea, Patella vulgata, and Gibbula umbilicalis) were found to significantly reduce the numbers of P. acanthus metacercariae in artificially prepared dishes by ingestion of cysts. Our results suggest that non-host organisms may play a key role in regulating the transmission of free-living trematode stages in rocky shore ecosystems, which is especially important with regard to the relative diversity and density of species in these habitats. The findings also emphasize the need to include parasites into marine food webs, since cercariae seem to be consumed by certain organisms to a considerable extent and could possibly represent an important energy source.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Barnes H (1959) Stomach contents and microfeeding of some common cirripedes. Can J Zool 37:231–236

    Article  Google Scholar 

  • Bartoli P, Boudouresque C-F (1997) Transmission failure of parasites (Digenea) in sites colonized by the recently introduced invasive alga Caulerpa taxifolia. Mar Ecol Prog Ser 154:253–260. doi:10.3354/meps154253

    Article  Google Scholar 

  • Bertness MD (1999) The ecology of Atlantic shorelines. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Bunnag T, Rabelo de Freitas J, Scott HG (1977) The predatory activity of Lebistes reticulatus (Peters, 1859) on Schistosoma mansoni miracidia in laboratory experiments. Trop Geogr Med 29:411–414

    PubMed  CAS  Google Scholar 

  • Chernin E, Perlstein JM (1971) Protection of snails against miracidia of Schistosoma mansoni by various aquatic invertebrates. J Parasitol 57:217–219. doi:10.2307/3278017

    Article  PubMed  CAS  Google Scholar 

  • Christensen NO (1979) Schistosoma mansoni: interference with cercarial host-finding by various aquatic organisms. J Helminthol 53:7–14

    Article  PubMed  CAS  Google Scholar 

  • Christensen NO, Frandsen F, Nansen P (1980) The interaction of some environmental factors influencing Schistosoma mansoni cercarial host-finding. J Helminthol 54:203–205

    Article  PubMed  CAS  Google Scholar 

  • Copeland MR, Montgomery WI, Hanna REB (1987) Ecology of a digenean infection, Cercaria patellae in Patella vulgata near Portavogie Harbour, Northern Ireland. J Helminthol 61:315–328

    Article  Google Scholar 

  • Crisp DJ (1958) The spread of Elminius modestus Darwin in north-west Europe. J Mar Biol Assoc UK 37:483–520. doi:10.1017/S0025315400023833

    Article  Google Scholar 

  • Crisp DJ, Southward AJ (1961) Different types of cirral activity of barnacles. Phil Trans R Soc Lond B 243:271–307. doi:10.1098/rstb.1961.0003

    Article  Google Scholar 

  • Desclaux C, de Montaudouin X, Bachelet G (2004) Cockle Cerastoderma edule population mortality: role of the digenean parasite Himasthla quissetensis. Mar Ecol Prog Ser 279:141–150. doi:10.3354/meps279141

    Article  Google Scholar 

  • Fernandez J, Goater TM, Esch GW (1991) Population dynamics of Chaetogaster limnaei limnaei (Oligochaeta) as affected by a trematode parasite in Helisoma anceps (Gastropoda). Am Midl Nat 125:195–205

    Article  Google Scholar 

  • Fredensborg BL, Mouritsen KN, Poulin R (2005) Impact of trematodes on host survival and population density in the intertidal gastropod Zeacumantus subcarinatus. Mar Ecol Prog Ser 290:109–117. doi:10.3354/meps290109

    Article  Google Scholar 

  • Fried B (1997) An overview of the biology of trematodes. In: Fried B, Graczyk TK (eds) Advances in trematode biology. CRC Press, Boca Raton, pp 1–30

    Google Scholar 

  • Galaktionov K, Bustness JO (1995) Species composition and prevalence of seabird trematode larvae in periwinkles at two littoral sites in north-Norway. Sarsia 80:187–191

    Google Scholar 

  • Gorbushin AM (1997) Field evidence of trematode-induced gigantism in Hydrobia spp. (Gastropoda: Prosobranchia). J Mar Biol Assoc UK 77:785–800. doi:10.1017/S0025315400036195

    Article  Google Scholar 

  • Hayward P, Nelson-Smith T, Shields C (1996) Seashore of Britain and Europe. Harper Collins Publishers, London

    Google Scholar 

  • Hopper JV, Poulin R, Thieltges DW (2008) Buffering role of the intertidal anemone Anthopleura aureoradiata in cercarial transmission from snails to crabs. J Exp Mar Biol Ecol 367:153–156. doi:10.1016/j.jembe.2008.09.013

    Article  Google Scholar 

  • Hulscher JB (1996) Food and feeding behaviour. In: Goss-Custard JD (ed) The oystercatcher: from individuals to populations. Oxford University Press, Oxford, pp 7–29

    Google Scholar 

  • Huxham M, Raffaelli D, Pike A (1993) The influence of Cryptocotyle lingua (Digenea: Platyhelminthes) infections on the survival and fecundity of Littorina littorea (Gastropoda: Prosobranchia). J Exp Mar Biol Ecol 168:223–238. doi:10.1016/0022-0981(93)90262-M

    Article  Google Scholar 

  • James BL (1968) The distribution and keys of species in the family Littorinidae and of their digenean parasites, in the region of Dale, Pembrokeshire. Field Stud 2:615–650

    Google Scholar 

  • Kaplan AT, Rebhal S, Lafferty KD, Kuris AM (2009) Small estuarine fishes feed on large trematode cercariae: lab and field investigations. J Parasitol 95:477–480. doi:10.1645/GE-1737.1

    Article  PubMed  Google Scholar 

  • Knight WB, Ritchie LS, Liard F, Chiriboga J (1970) Cercariophagic activity of guppy fish (Lebistes reticulatus) detected by cercariae labeled with radioselenium (75SE). Am J Trop Med Hyg 19:620–625

    PubMed  CAS  Google Scholar 

  • Køie M (1975) On the morphology and life-history of Opechona bacillaris (Molin, 1859) Looss, 1907 (Trematoda, Lepocreadiidae). Ophelia 13:63–86. doi:10.1007/BF00927847

    Google Scholar 

  • Kopp K, Jokela J (2007) Resistant invaders can convey benefits to native species. Oikos 116:295–301. doi:10.1111/j.2006.0030-1299.15290.x

    Article  Google Scholar 

  • Krakau M, Thieltges DW, Reise K (2006) Native parasites adopt introduced bivalves of the North Sea. Biol Invasions 8:919–925. doi:10.1007/s10530-005-4734-8

    Article  Google Scholar 

  • Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, 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. doi:10.1038/nature06970

    Article  PubMed  CAS  Google Scholar 

  • Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103:11211–11216. doi:10.1038/nature06970

    Article  PubMed  CAS  Google Scholar 

  • Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546. doi:10.1111/j.1461-0248.2008.01174.x

    Article  PubMed  Google Scholar 

  • Latham ADM, Fredensborg BL, McFarland LH, Poulin R (2003) A gastropod scavenger serving as paratenic host for larval helminth communities in shore crabs. J Parasitol 89:862–864. doi:10.1645/GE-73R

    Article  PubMed  CAS  Google Scholar 

  • McCarthy HO, Irwin SWB, Fitzpatrick SM (1999) Nucella lapillus as a paratenic host for Maritrema arenaria. J Helminthol 73:281–282. doi:10.1017/S0022149X99000463

    Google Scholar 

  • McFarland LH, Mouritsen KN, Poulin R (2003) From first to second and back to first intermediate host: the unusual transmission route of Curtuteria australis (Digenea: Echinostomatidae). J Parasitol 89:625–628. doi:10.1645/0022-3395(2003)089[0625:FFTSAB]2.0.CO;2

    Article  PubMed  CAS  Google Scholar 

  • Morley NJ, Lewis JW (2004) Free-living endohelminths: the influence of multiple factors. Trends Parasitol 20:114–115. doi:10.1016/j.pt.2003.12.002

    Article  PubMed  Google Scholar 

  • Mouritsen KN (2002) The Hydrobia ulvae–Maritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity. J Helminthol 76:341–347. doi:10.1079/JOH2002136

    Article  PubMed  CAS  Google Scholar 

  • Mouritsen KN, Jensen KT (1994) The enigma of gigantism: effect of larval trematodes on growth, fecundity, egestion and locomotion in Hydrobia ulvae (Pennant) (Gastropoda: Prosobranchia). J Exp Mar Biol Ecol 181:53–66. doi:10.1016/0022-0981(94)90103-1

    Article  Google Scholar 

  • Mouritsen KN, Poulin R (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124:S101–S117. doi:10.1017}S0031182002001476

    PubMed  Google Scholar 

  • Mouritsen KN, Poulin R (2003) The mud flat anemone-cockle association: mutualism in the intertidal zone? Oecologia 135:131–137. doi:10.1007/s00442-003-1183-x

    PubMed  Google Scholar 

  • Mouritsen KN, Poulin R (2005) Parasites boost biodiversity and change animal community structure by trait-mediated indirect effects. Oikos 108:344–350. doi:10.1111/j.0030-1299.2005.13507.x

    Article  Google Scholar 

  • Oliver-Gonzales J (1946) The possible role of the guppy Lebistes reticulatus on the biological control of Schistosomiasis mansoni. Science 104:605. doi:10.1126/science.104.2712.605-b

    Article  Google Scholar 

  • Pietrock M, Marcogliese DJ (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends Parasitol 19:293–299. doi:10.1016/S1471-4922(03)00117-X

    Article  PubMed  Google Scholar 

  • Poulin R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132:143–151. doi:10.1017/S0031182005008693

    Article  PubMed  CAS  Google Scholar 

  • Prinz K, Kelly TC, O’Riordan RM, Culloty SC (2009) Infection of Mytilus edulis by the trematode Echinostephilla patellae (Digenea: Philophthalmidae). J Helminthol (in press)

  • Rees FG (1934) Cercaria patellae Lebour, 1911, and its effect on the digestive gland and the gonads of Patella vulgata. Proc Zool Soc Lond 45:45–53

    Google Scholar 

  • Rees FG (1937) The anatomy and encystment of Cercaria purpurae Lebour, 1911. Proc Zool Soc Lond B 107:65–73

    Google Scholar 

  • Schotthoefer AM, Labak KM, Beasley VR (2007) Ribeiroia ondatrae cercariae are consumed by aquatic invertebrate predators. J Parasitol 93:1240–1243. doi:10.1645/GE1129R.1

    Article  PubMed  Google Scholar 

  • Sousa WP (1991) Can models of soft-sediment community structure be complete without parasites? Am Zool 31:821–830. doi:10.1093/icb/31.6.821

    Google Scholar 

  • Thieltges DW (2006a) Effect of metacercarial trematode infections (Renicola roscovita) on growth in intertidal blue mussels (Mytilus edulis). Mar Ecol Prog Ser 319:129–134. doi:10.3354/meps319129

    Article  Google Scholar 

  • Thieltges DW (2006b) Parasite induced summer mortality in the cockle Cerastoderma edule by the trematode Gymnophallus choledochus. Hydrobiologia 559:455–461. doi:10.1007/s10750-005-1345-4

    Article  Google Scholar 

  • Thieltges DW, Rick J (2006) Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Dis Aquat Org 73:63–68. doi:10.3354/dao073063

    Article  PubMed  Google Scholar 

  • Thieltges DW, Bordalo MD, Caballero Hernández A, Prinz K, Jensen KT (2008a) Ambient fauna impairs parasite transmission in a marine parasite-host system. Parasitology 135:1111–1116. doi:10.1017/S0031182008004526

    PubMed  CAS  Google Scholar 

  • Thieltges DW, de Montaudouin X, Fredensborg BL, Jensen KT, Koprivnikar J, Poulin R (2008b) Production of marine trematode cercariae: a potentially overlooked path of energy flow in benthic systems. Mar Ecol Prog Ser 372:147–155. doi:10.3354/meps07703

    Article  Google Scholar 

  • Thieltges DW, Jensen KT, Poulin R (2008c) The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135:407–426. doi:10.1017/S0031182007000248

    PubMed  CAS  Google Scholar 

  • Thieltges DW, Reise K, Prinz K, Jensen KT (2009) Invaders interfere with native parasite–host interactions. Biol Invasions 11:1421–1429. doi:10.1007/s10530-008-9350-y

    Article  Google Scholar 

  • Thomas F, Cezilly F, de Meeüs T, Crivelli A, Renaud F (1997) Parasitism and ecology of wetlands: a review. Estuaries 20:646–654

    Article  Google Scholar 

  • Upatham ES, Sturrock RF (1973) Field investigations on the effect of other aquatic animals on the infection of Biomphalaria glabrata by Schistosoma mansoni miracidia. J Parasitol 59:448–453. doi:10.2307/3278770

    Article  PubMed  CAS  Google Scholar 

  • Warren KS, Peters PA (1968) Cercariae of Schistosoma mansoni and plants: attempt to penetrate Phaseolus vulgaris and Hedychium coronarium produces a cercaricide. Nature 217:647–648. doi:10.1038/217647a0

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

K. Prinz received funding from the Irish Research Council for Science, Engineering and Technology (IRCSET) under the National Development Plan.

Author information

Authors and Affiliations

  1. Department of Zoology, Ecology and Plant Science, University College Cork, Distillery Fields, North Mall, Cork, Ireland

    Katrin Prinz, Thomas C. Kelly, Ruth M. O’Riordan & Sarah C. Culloty

Authors
  1. Katrin Prinz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas C. Kelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ruth M. O’Riordan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sarah C. Culloty
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katrin Prinz.

Additional information

Communicated by F. Bulleri.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Prinz, K., Kelly, T.C., O’Riordan, R.M. et al. Non-host organisms affect transmission processes in two common trematode parasites of rocky shores. Mar Biol 156, 2303–2311 (2009). https://doi.org/10.1007/s00227-009-1258-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-009-1258-2

Keywords

Search

Navigation