Skip to main content

Non-host organisms impact transmission at two different life stages in a marine parasite


The potential for local biodiversity to ‘dilute’ infection risk has been shown to be particularly important in aquatic trematodes, where non-host organisms can feed on free-living infective stages (cercariae) and reduce transmission rates to target hosts. Non-host organisms could also impact transmission during other stages of the trematode life cycle. In Philophthalmus spp., cercariae encyst as metacercariae on external surfaces, where they remain exposed to the adverse effects of non-host organisms. In laboratory experiments, we tested the potential for a range of non-host organisms to (i) prey on cercariae, (ii) induce early (i.e., faster) encystment and (iii) prey on or destroy metacercariae. Our results show that intertidal anemones, and to a lesser extent clams, can consume substantial numbers of cercariae. However, we found no strong evidence that the presence of these predators causes cercariae to encyst faster as a way to escape from predation. We also found that grazing snails can reduce numbers of encysted metacercariae, either by eating or crushing them. Our findings add to the growing evidence that trematode transmission success can be strongly affected by the local diversity of non-host organisms. They also reinforce the notion that parasites are potentially important food items for many organisms, thus playing roles other than consumers in many food webs.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3


  • Galaktionov KV, Dobrovolskij AA (2003) The biology and evolution of trematodes. Kluwer Academic Publishers, Dordrecht

    Book  Google Scholar 

  • Guilloteau P, Poulin R, MacLeod CD (2016) Impacts of ocean acidification on multiplication and caste organisation of parasitic trematodes in their gastropod host. Mar Biol 163:96

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Johnson PTJ, Ostfeld RS, Keesing F (2015) Frontiers in research on biodiversity and disease. Ecol Lett 18:1119–1133

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones MB, Marsden ID (2005) Life in the estuary: illustrated guide and ecology. Canterbury University Press, Christchurch

    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

    Article  PubMed  Google Scholar 

  • Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498

    Article  CAS  PubMed  Google Scholar 

  • Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647–652

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Lei F, Poulin R (2011) Effects of salinity on multiplication and transmission of an intertidal trematode parasite. Mar Biol 158:995–1003

    Article  Google Scholar 

  • Martorelli SR, Fredensborg BL, Leung TLF, Poulin R (2008) Four trematode cercariae from the New Zealand intertidal snail Zeacumantus subcarinatus (Batillariidae). New Zealand J Zool 35:73–84

    Article  Google Scholar 

  • Mironova E, Gopko M, Pasternak A, Mikheev V, Taskinen J (2018) Trematode cercariae as prey for zooplankton: effect on fitness traits of predators. Parasitology.

  • Mouritsen KN, Poulin R (2003) The mud flat anemone–cockle association: mutualism in the intertidal zone? Oecologia 135:131–137

    Article  PubMed  Google Scholar 

  • Mouritsen KN, McKechnie S, Meenken E, Toynbee JL, Poulin R (2003) Spatial heterogeneity in parasite loads in the New Zealand cockle: the importance of host condition and density. J Mar Biol Assoc UK 83:307–310

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Neal AT, Poulin R (2012) Substratum preference of Philophthalmus sp. cercariae for cyst formation under natural and experimental conditions. J Parasitol 98:293–298

    Article  PubMed  Google Scholar 

  • O’Dwyer K, Poulin R (2015) Taken to the limit: is desiccation stress causing precocious encystment of trematode parasites in snails? Parasitol Int 64:632–637

    Article  PubMed  Google Scholar 

  • Orlofske SA, Jadin RC, Johnson PTJ (2015) It’s a predator-eat-parasite world: how characteristics of predator, parasite and environment affect consumption. Oecologia 178:537–547

    Article  PubMed  Google Scholar 

  • Ostfeld RS, Keesing F (2000) The function of biodiversity in the ecology of vector-borne zoonotic diseases. Can J Zool 78:2061–2078

    Article  Google Scholar 

  • Pietrock M, Marcogliese D (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends Parasitol 19:293–299

    Article  PubMed  Google Scholar 

  • Prinz K, Kelly TC, O’Riordan RM, Culloty SC (2009) Non-host organisms affect transmission processes in two common trematode parasites of rocky shores. Mar Biol 156:2303–2311

    Article  Google Scholar 

  • Randolph SE, Dobson ADM (2012) Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139:847–863

    Article  CAS  PubMed  Google Scholar 

  • Salkeld DJ, Padgett KA, Jones JH (2013) A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecol Lett 16:679–686

    Article  PubMed  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Thieltges DW, Amundsen P-A, Hechinger RF, Johnson PTJ, Lafferty KD, Mouritsen KN, Preston DL, Reise K, Zander CD, Poulin R (2013) Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos 122:1473–1482

    Google Scholar 

  • Welsh JE, van der Meer J, Brussaard CPD, Thieltges DW (2014) Inventory of organisms interfering with transmission of a marine trematode. J Mar Biol Assoc UK 94:697–702

    Article  Google Scholar 

  • Welsh JE, Liddell C, van der Meer J, Thieltges DW (2017) Parasites as prey: the effect of cercarial density and alternative prey on consumption of cercariae by four non-host species. Parasitology 144:1775–1782

    Article  PubMed  Google Scholar 

  • Wood CL, Lafferty KD (2013) Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends Ecol Evol 28:239–247

    Article  PubMed  Google Scholar 

Download references


CS was supported financially by a postdoctoral fellowship from the German Research Foundation (DFG, SE 2728/1-1).

Author information

Authors and Affiliations


Corresponding author

Correspondence to Christian Selbach.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Vielma, S., Lagrue, C., Poulin, R. et al. Non-host organisms impact transmission at two different life stages in a marine parasite. Parasitol Res 118, 111–117 (2019).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:


  • Biodiversity
  • Cercariae
  • Dilution effect
  • Metacercariae
  • Philophthalmus sp.
  • Predation
  • Transmission success